22_ENVIRONMETAL PHISIOLOGY OF ANIMAL 2005_779

636 CHAPTER 16 Nest of Atta (leafcutter ant)
0
Transverse section of
Macrotermes nest

35°C

29.3 Temperature (°C) 25.5 18°C
2.9 CO2 (%) 2.7

Air flow Depth (m) −5

30.0 17°C
24.4

2.7
8

29.7
2.6

25.3 −10
1.3

(a) (b)

Fig. 16.21 (a) Termite and (b) ant nest architecture and temperatures. Getting the right food

limits, and not surprisingly the females are a very pale cream color, Feeding in deserts is necessarily opportunistic, and many species
cream models being shown to stay cooler than black models. live close to starvation for large parts of their lives. Invertebrates are
particularly subject to long periods when there is no food available,
However, the nests of ants and termites are the most spectacular between intermittent rains. Desert spiders, for example, may make a
examples of managed microclimate, with the insulation, ventilation, capture on fewer than 5% of all nights, and on only 1.5% of all nights
and orientation of the nest all attended to. Termites, for example, during drought periods.
are mound builders in most of Africa and in Australia; in forest areas
their nests are compact domes, whereas in semiarid areas the nests Most of the desert insects are herbivores, many feeding on seeds,
may appear as complex turreted and ridged mounds. But in the hot which survive for very long periods between rains because the rate of
and/or dry deserts of central Asia termites are mostly subterranean, decomposition in a desert is very low. Rodents and some reptiles use
while in the Sahara there are just a few species and they live almost the same food resource. Relatively few insects (aphids and hoppers,
entirely underground, feeding on remnant semifossilized tree trunks orthopterans, and a few caterpillars) and a few small mammals
from more humid Pleistocene periods. The best known examples of use the other more succulent parts of plants (often below ground).
sophisticated termite nest architecture are the “compass termites”, A small guild of nectarivores usually occurs, often dominated by
their nests always being built with the long axis running north/ solitary or semisocial bees from the family Anthophoridae in par-
south, so that the structure warms up quickly after dawn but keeps ticular (“flower bees” and “carpenter bees”, particularly diverse in
relatively cool in the middle of the day with minimum surface deserts) with some bee-flies (Bombylidae) and small sphinx moths
exposed to the sun. Elaborate patterns of vertical shafts provide (Sphingidae).
ventilation systems (Fig. 16.21a).
The selection of plant food in deserts may perhaps be more
Ants’ nests are usually underground, and may extend down for relaxed than in other terrestrial habitats. Granivores certainly col-
several meters (Fig. 16.21b), providing different microclimates at lect seeds that are higher in protein content and lower in secondary
different levels for different functions. For example, Pogonomyrmex metabolites by preference, but may be forced to take a wider range
rugosus, a seed-harvesting species, constructs its storage chambers in xeric climates than in mesic zones. Foliar feeders may face par-
in the upper 0.7 m of the soil profile, but has its workers (mainly) ticularly well-defended plants, since no desert plant can easily afford
and larvae (almost entirely) living in galleries 1.5–2 m down. the desiccating effects of being damaged; physical defenses such as
spines are ubiquitous and require careful manipulation by any

EXTREME TERRESTRIAL HABITATS 637

intending herbivore. Chemical defenses are also very common, and of the desert rodents will store food at times of plenty to use later.
it is perhaps no coincidence that so many desert plants are used by Sometimes this involves storing within the body itself: laying down
local human populations as medicines. It might be a fair general- fat reserves prior to estivation is one example, but a more extra-
ization to say that desert herbivores are more likely to be either very ordinary version of the same principle is found in the honeypot
generalist, taking whatever is available at any one time, or very ants (Myrmecocystus and other genera), which use a few members
specialist, having a coevolved dependence on a very few species of of the colony as living underground storage jars, their abdomens
relatively abundant well-defended plants. It is the oligophagous hugely distended with gathered nectar.
species that are quite rare.
Extracorporeal stores are more normal though. Here, storing
Generalist adaptations for desert herbivory probably involve seeds is a particularly sensible strategy given the low rate of attack by
large-capacity but relatively simple guts, able to provide flexibility fungi and other decomposing agents, and is also favored because
in dealing with whatever may be available. This is exemplified by the many seeds will take in water hygroscopically when stored in a
desert tortoise, Xerobates agassizii, which eats very fibrous grasses or burrow at raised humidity, so giving the prudent gatherer an extra
much softer herbaceous plants according to the season, utilizing source of water in the future. For example, dry seeds collected by
colonic fermentation (see Chapter 15). Its gut constitutes up to 21% gerbils above ground at 10% RH contained 3.7 g water per 100 g
of the body mass, and is heavily endowed with mucous glands to of seed; stored at 75% RH in a relatively short burrow, their water
provide some protection from abrasion, but is otherwise relatively content increases to 18.0 g per 100 g. Rodents with cheek pouches
unmodified. for gathering seeds should be best equipped to exploit this effect.
However, it has recently been realized that a “normal” rodent with
Certain desert plants are halophytic (growing on very salty soils) internal pouches actually loses a significant amount of salivary water
and attract only specialist feeders because of their high electrolyte to dry seeds when these are held in the pouch for just a few minutes,
content. A classic case is the saltbush, Atriplex, common in deserts and cannot recover this water as it mainly stays in the indigestible
of the Middle East. Fat sand rats (Psammomys obesus) are diurnal seed coat. Only some specialist desert rodents with external fur-
rodents that feed specifically on saltbush tissues, but they always lined cheek pouches can avoid this. This phenomenon allows many
scrape off the outermost saltiest layers of the plant leaves before desert heteromyid rodents, such as kangaroo rats, pocket mice, and
ingesting the underlying tissues. kangaroo mice, to survive on little else but seeds. The kangaroo rats
(Dipodomys) of the Mojave desert may eat nothing but dry Larrea
Conspicuous guilds of specialist feeders may also occur on highly (creosote bush) seeds for 9 months of the year, without needing any
toxic plants such as asclepiads (milkweeds) and solanaceous herbs drinking water.
(the deadly nightshade family). These specialist herbivores can be
picked out as they are often aposematically colored, warning of their The sheer volume of stored food in a desert can be astounding:
own acquisition of some of the plant’s chemicals. In some cases a single termite colony can accumulate 0.5 kg of dried grass, and a
desert herbivores can get around this problem of secondary plant nest of harvester ants may contain at least 100 g of seeds, more than
chemicals by selectively feeding on plants at times when such four times the total biomass of the ants. One nest of Messor ants was
defenses are reduced. For example, in North American deserts the calculated to contain around 170,000 seeds!
creosote bush (Larrea) has reduced levels of translocated defensive
chemicals in the evenings and is then much more strongly grazed. Estivation
It has also been suggested that after rains many desert plants are
bound to invest more in growth than in defense and so may be par- Many semiarid and desert animals that are essentially evaders use a
ticularly favored by herbivores at such times, many animals taking period of physiological inactivity as part of their survival repertoire,
in plants that they would have avoided during droughts when and this is conventionally termed estivation (summer sleep) as it
chemical defenses were stronger. is usually timed to avoid the hottest and driest periods. Metabolic
rates are reduced, and usually the thermal tolerance limits are
Given a range of generalist and specialist herbivores, there are expanded. Growth and reproduction cease, and the animal becomes
clearly niches for a limited number of predators, and in most deserts relatively unresponsive to external stimuli.
the arachnids and the snakes are pre-eminent. They survive largely
by eating the plant-feeding insects, but with the use of poisons they As with winter dormancy and torpor, terminology is confusing
can also take on much bigger creatures such as lizards and rodents. and different terms are used in different fashions. A period of beha-
By eating animal flesh, they automatically acquire a well-balanced vioral inactivity without much physiological adjustment is often
and relatively moist diet (about 70% water content), so may need termed quiescence, whereas deeper states of withdrawal including
little or no extra drinking water. Spiders have very low metabolic modified physiological states are termed estivation, and the deepest
rates and can recycle their silk and recoup its energy, giving very high forms of metabolic suppression (with no visible sign of life) are
starvation resistance. Sand-vipers locate their prey in an unusual called cryptobiosis (see Chapter 14). Where the dormant state is
manner partly by detecting ground-borne vibrations, and can thus triggered internally and occurs as a regular and defined part of the
feed even if their visual and olfactory systems are blocked. Likewise life cycle, particularly in arthropods, it is usually termed diapause.
scorpions are extremely sensitive to vibrational information from These states also differ in the method of arousal, since quiescence
prey, transmitted through the sand. normally ends automatically when conditions improve whereas
diapause requires specific signals and internal control mechanisms.
For all desert animals it is advantageous to take in as much food as
possible during the transient periods of plenty. An active desert snail Many burrowing desert invertebrates show periods of quiescence,
(Sphincterochila) may take in nearly 50 times as much energy as it usually plugging up their burrows, both at the individual level as in
uses in 1 day of foraging activity. Many social insects and also most

638 CHAPTER 16

spiders and sun-spiders, and at the colony level as in ants. More pro- breeding are rare. Different species may be more to the r-selected or
longed dormancy (estivation) is very characteristic of desert snails, K-selected end of the spectrum within these broad generalizations,
which may spend a large part of their life in this state (up to 98% of and in some ways desert animals therefore represent a mixture of
their life for Sphincterochila in the Negev). In snails such as Helix, the classic r- and K-characteristics, conflicting with the normal
metabolic rate is suppressed by 84% after a month in estivation, and demarcations of life-history strategies.
in the more drought-resistant snail Rhagada this rises to over 90%,
with a 97% reduction in evaporative water loss (and thus relatively Cryptobiotic nematodes living in the sands can become active
little lowering of body water content). In the snail Otala, estivation- and lay eggs within minutes of their first wetting, and certain
specific proteins are synthesized in the hepatopancreas during the collembolans, mites, and isopods can complete a generation within
process of reducing the metabolic rate. This state, with the shell a week or two. At least some invertebrates appear to be able to
sealed off by a calcareous lid (epiphragm), can prolong survival time oviposit in anticipation of rain, and the juveniles therefore appear
to several years. Different species of snail arrange themselves with just as the flush of green plants and associated insects occurs. Many
the body suspended in air on the coolest side of a desert shrub, or on of these examples are underground cryptic species, and they pro-
the least insolated side of a rock; the air space within the shell serves duce very large numbers of offspring with every onset of rain, most
as extra insulation for the tissues (see Fig. 16.14b). A few species esti- of which do not survive.
vate in large aggregations, with those at the base of the clump having
the best survival chances as they are protected from the sun. Producing relatively few young in each breeding episode, and
investing heavily in those few offspring, is also favored, particularly
Diapause, as we saw in Chapters 8 and 10, is a complex phe- among surface dwellers, where maternal care is therefore rather
nomenon of arrested growth and development occurring in arthro- common. In some special cases the mother may control the micro-
pods in response to environmental adversity, and it may affect climate of the juveniles herself: ants move the brood around the nest
physiology, behaviour, and even morphology. It is normally trig- to the most favorable microhabitats, and many spiders carry their
gered well in advance of the onset of really harsh conditions (see eggs around in an egg sac. Spiders also take care of their spiderlings,
Fig. 8.45). Desert species often lack the photoperiodic cues com- and the Namib dune spider (Leucorchestris) is known to feed its
monly used by mesic species, relying instead on triggering by food young within the burrow. Scorpions are particularly renowned for
scarcity or climatic factors, always acting cumulatively some time in prolonged care of juveniles, these being carried around on the
advance of the onset of the diapause state and so allowing extra con- mother’s back.
trol of its occurrence. Thus diapause may persist over many months
or even several years in the absence of desert rains. Most of the arthropod evaders burrow and therefore also lay eggs
underground. Even the large migratory locust, unable to burrow,
Estivation in ectothermic vertebrate evaders occurs in many achieves underground eggs with its very long ovipositor at the end
amphibians and reptiles, which burrow into the soil and in the case of a telescopic abdomen. Alternatively eggs may be laid on or in the
of amphibians may form a cocoon. Estivation is particularly well host food plant, taking advantage of microclimates on the underside
studied in the genus Scaphiopus and in several frog genera from of leaves or within stems or flowers.
Australia, with the metabolic rate declining by 50–67%. Scaphiopus
can spend 10 months of every year in estivation utilizing stored lipid The spadefoot toads (Scaphiopus) are well known for their spe-
reserves, with reduced hemolymph volume and increased hemo- cialized tricks for reproducing in deserts, although they retain the
lymph concentration accompanied by urea accumulation, as we saw aquatic egg-laying habit of most mesic amphibians. They depend on
above. In this species the antioxidant enzymes (needed to protect careful timing and very rapid development for their success. During
the tissues during arousal and reoxygenation; see Chapter 6) are the seasons when rain might be “expected” their gonads mature and
both abundant and unusually insensitive to urea. they move each night close to their burrow surface, retreating down
again by day if there is no rain. But when rain does come (even a
Estivation also occurs in desert endotherms in drought periods, light shower, <0.5 mm of rain) individuals emerge almost instantly
with behavioral lethargy and a reduction of Tb to a level close to and seek out a temporary surface pool of water, arriving at this
ambient. It is well known in desert ground squirrels, gerbils, and “breeding pond” on the same day as the first rain and laying eggs
some possums, where Tb values during the “summer rest” are com- that night. By the next morning the embryos are well developed and
monly around 25–30°C. Gerbils and other burrowers may also have acquired moderate thermal tolerance (unusual in amphibian
show circadian patterns of torpor during daylight, allowing Tb to eggs); they complete their metamorphosis in 2–3 weeks instead of
drop to the burrow temperature of about 30°C (occasionally as low the 10–12 weeks of “normal” frogs and toads. The pools they live
as 19–20°C), thereby saving considerably on both food and water. in may start to dry up and become very crowded, and this triggers a
further response, as some of the tadpoles then turn cannibalistic and
Reproduction: protecting the eggs and young develop hypertrophied jaws, speeding up their own development
even further with a high-quality tadpole diet!
Life-history strategies consisting of short lifespan, high repro-
ductive output, and frequent breeding are usually debarred by the The desert tortoises, whose seasonal cycle was referred to earlier,
scarcity of resources in deserts; infrequent but regular cycles are manage to reproduce every year despite the variation in water and
also difficult given the unpredictability of the habitat. Many desert food availability, reducing their field metabolic rate in drought years
animals are therefore long-lived and breed opportunistically and and forfeiting body condition to produce a few eggs. This “bet-
very quickly whenever there is rain, being effectively sterile in some hedging” life-history strategy is probably typical for a relatively large
years. Certainly the more traditional terrestrial patterns of seasonal and long-lived desert ectotherm.

Desert rodents use a variety of different reproductive patterns.
Some are “pulse averagers”, with slow prolonged reproductive effort

EXTREME TERRESTRIAL HABITATS 639

matching the historical probability of rainfall timing; some are normally preferable for desert animals, and it can be combined with
“pulse matchers”, responding directly to rain and food availability; countercurrent systems in the nose to save water as described for the
some, which store foods or use completely reliable foods, are “pulse smaller evader animals. Desert sandgrouse show a very pronounced
ignorers”; and yet others are “pulse gamblers”, producing large gular flutter (see Fig. 8.44b) to supplement normal panting, and
litters at the end of their hibernation period irrespective of condi- have markedly enhanced evaporative thermoregulation compared
tions, some of which fail completely. with less arid-adapted relatives. The pin-tailed sandgrouse, Pterocles
alchata, dissipates 89% of its metabolic heat production by evapora-
The most striking factor in many desert-breeding species is their tion at 40°C, which is 152% of the allometric prediction. Some xeric
ability to detect and respond to the very smallest quantities of rain birds are particularly well suited to be evaporators by virtue of feed-
almost instantly. Spadefoot toads appear to use the low-frequency ing on nectar. The Australian honeyeater Manorina flavigula has a
sound of rain drops on the ground as their cue. Some desert birds very high daily water turnover and a high and variable urine concen-
use even the distant sight of rain, or the accompanying slight rise of tration, reflecting the water inputs it gets from plants.
humidity, as their cue for initiating nesting and egg laying.
One group of desert invertebrates deserve honorable mention as
Sociality being part of the “evaporator” cohort; these are the insects that can
use evaporative water loss for cooling, again because of a reliable
We have already noted that social insects are particularly common watery food supply. The desert cicadas are best known, their tran-
in deserts, exploiting the advantages of stable nest microclimates in spiration rate increasing at least five-fold when exposed to temper-
providing thermal refugia, bulk storage of ephemeral resources, and atures above a specific setpoint. Species such as Diceroprocta apache
defense against predators and parasites. The utility of sociality has release water from pores on their dorsal cuticular plates, allowing
been realized in other taxonomic groups as well. Very arid habitats them to maintain a body temperature of only 39–45°C when (in the
house a few species of social isopods, of social spiders, and of at case of males) singing to attract a mate in ambient temperatures of
least one social tenebrionid beetle. Southern African deserts are also up to 48°C. This particular cicada feeds on the abundant mesquite
the home of a now famous rodent, the truly social mammal known plants of the North America deserts. The cicada Okanagodes gracilis
as the naked mole rat, Heterocephalus glaber. This has a queen and is even more impressive, maintaining activity even through the
nonreproductive workers living together in a burrow network, and hottest days (Ta > 50°C) while feeding and evaporatively cooling.
its lifestyle is ideal as a strategy for exploiting limited and patchy Control of sweating in the cicada Diceroprocta is turning out to be
food resources and sharing the costs of tunneling in hard, baked rather complex, involving internal and surface sensors and at least
soils. It is also noteworthy for being the only mammal that is two regulatory pathways involving prostaglandin-like chemical
approximately ectothermic, having noninsulated surfaces with very signals.
high heat-loss rates and thus a potentially variable Tb (though it
can produce heat endothermically in the laboratory). Its preferred A less familiar example of the evaporative strategy in desert
Tb is 33°C, which is also the temperature at which its gut flora, insects is the grasshopper Poekilocerus bufonius, which gets enough
performing the cecal fermentation of the very high fiber diet, work water from its asclepiad food plant to be able to afford some evapor-
fastest. ative cooling. It seems probable that other desert xylem feeders may
use a similar technique. We should also mention some social bees,
16.2.3 Evaporators and their strategies particularly in the genus Apis, that must cool their bodies and also
their whole colony using gathered water when temperatures rise too
The evaporators are the “middle-sized” animals of the deserts, high, inevitably causing them to be restricted to oases and desert
including some birds, plus dogs, cats, smaller antelope, foxes, etc. fringes.
The group could also be said to include domesticated goats and
sheep, and man himself where he lives on desert fringes. Other thermal and water balance strategies

These animals are all dependent on a reasonable water supply to Inevitably the desert evaporators use most of the behavioral and
allow them to cool down by the use of evaporation, at ambient tem- postural strategies already described above for their smaller counter-
peratures where other cooling modes are impossible. Evaporators parts; behavior continues to be a major part of the overall adaptive
are therefore inevitably few and far between, mostly living only at pattern. Huddling is perhaps more common than burrowing,
the desert fringes and where there is access to water at oases. They do which can be difficult for these larger animals. The wood hoopoes
rather better in the margins of rocky deserts, where there is more of the sub-Saharan savannas huddle in response to low ambient
microclimatic variation to exploit on a scale that is useful to them temperatures, with metabolic rates 30–60% lower at night than for
(e.g. sheltering behind boulders). Moderately sized creatures, such solitary birds, saving up to 29% of the daily energy expenditure.
as the rock wren and the elf owl, can survive by sheltering in crevices
in such habitats. Desert birds such as babblers, finch larks, and sandgrouse show
some particular tricks to survive quite deep into the deserts. The
Evaporative cooling mobility endowed by flight enables them to gather seeds over a very
wide area, and more importantly to get water from oases. In the
As with all other animals, either panting or sweating may be used as sandgrouse genus (Pterocles) the males are adapted to carry water
the means of evaporation; as we saw in Chapter 8, the latter is less back to the nest and to the young; they wade chest high into the
controllable and also loses salts, but it uses up less energy. Panting is water and return with it soaked into and below their specialized
breast feathers, carrying up to 40 ml per trip over astonishing

640 CHAPTER 16

distances of up to 80 km. Other desert birds use a special kind of Table 16.2 Urine concentrations and urine : plasma ratios in desert vertebrates.
“shading behavior” at the nest, squatting just above the eggs rather
than nestling down on them. This may be more important for cool- Taxon Urine concentration Urine : plasma
ing the parent’s lower body by raising it above the boundary layer, (mOsm) ratio
than for allowing convective cooling from the eggs themselves.
Reptiles 337 1.0
However, there are some additional physiological components in Desert tortoise
the repertoire of these animals. The carotid rete system for selective 900 2.7
brain cooling (see Chapter 8) appears to be relatively common in Birds 944 2.7
these medium to large mammals. It is best developed in those that Struthio (ostrich) 1005 2.8
pant, especially artiodactyls, canids, and felids, where the necessary Kookaburra 2020 5.8
cool blood is that returning from the nasal area, cooled by evapora- Zebra finch
tion. The carotid rete linked to the cold nose in these panting Savanna sparrow 1880 6
animals can cool the blood to the brain by 2°C or more, which in 2200 7
a heat-stressed desert species is very important in that it avoids Mammals 2700 8
triggering the brain-based receptors that normally turn on extra Eland 3200 8
panting mechanisms to cool the body down, and which if activated Bedouin goat 5500 16
could lead to disastrous evaporative water loss. Megaleia (kangaroo) 9370 25
Camelus (camel)
Similar brain cooling occurs in other mammals (even in man), Dipodomys (kangaroo rat)
where there is no panting mechanism, and then seems to involve Notomys (hopping mouse)
cool blood from the facial veins entering the cavernous sinus at the
base of the skull where the carotid artery, though not subdivided and food is rare. The metabolic rate of a black goat may be 25%
into a rete, follows a fairly tortuous course so that its blood can be lower than that of a white one, because they can absorb more heat
slightly cooled. In desert birds brain cooling has also been demon- from the sun and have less need to shiver. Furthermore, remember
strated, with a countercurrent operating in the ophthalmic rete and that in all these cases we are considering environments where
involving cooled venous blood from the nose, mouth, and eye areas. reradiated longwave radiation from the bare ground, the absorp-
Brain cooling by heat exchange occurs in at least some reptiles, tion of which is largely independent of color, may be a particularly
too, where the brain tissues can be 2–3°C lower than the core body large component of the total heat spectrum.
temperature or rectal temperature. This is achieved in desert lizards
by a rapid and shallow breathing through the open mouth, allowing Desert goats also show an unusual ability to reduce metabolic
the pharynx area to cool evaporatively. While this does not actually rates when food is scarce and maintain their body weights on less
achieve much body cooling in the sense that true panting can do for than half their normal food intake. Unusually, this involves reduced
a mammal or bird, it does provide a brain temperature-regulating metabolism mainly in the muscles, whereas in most mammals it is
system, for the carotid artery runs very superficially through this the gut that is “turned down” most conspicuously.
pharyngeal area and thus the arterial supply into the brain is again
cooled. Medium-sized desert animals also show a pronounced ability to
produce hyperosmotic urine (Table 16.2), well beyond the levels
Some of the desert birds may also demonstrate a lowered meta- seen in temperate species of similar body mass (cf. Table 15.8).
bolic rate (e.g. 26% below the allometric prediction in Houbara Mammals with more numerous long loops of Henle inevitably suc-
bustards, and 46% lower in the double-banded sandgrouse Pterocles ceed best, with high urine : plasma solute ratios.
bicinctus). There may also be a tolerance of some hyperthermia, and
a high upper critical temperature permitting survival at somewhat Migration
elevated Tb. In the Negev the great gray shrike (Lanius excubitor)
shows an increase of Tb with rising Ta even within its normal ther- Many evaporators are essentially nomadic, using migration as part
moneutral zone (30–36°C), and this controlled hyperthermia gives of their strategy to track the patchy resources, moving between
it a saving of water by allowing extra dry heat loss rather than evapo- water sources as they fluctuate and become exhausted. This may
rative water loss. However, this and other desert birds also exhibit a involve regular movements outward from a fairly permanent cen-
rather high rate of increase of EWL with temperature, a puzzling tral refugium, or a more random wandering between chance-found
observation not yet adequately explained. resource foci. However, migration does impose substantial meta-
bolic costs, and is a risky strategy since location of future supplies
Many of these medium-sized animals from hot climates seem can rarely be guaranteed.
anomalous in having very dark surfaces (e.g. desert goats, sheep,
and ravens). The phenomenon of black desert mammals and birds Following on from this point, it could also be said that the famous
may be explained by several factors. The individual black feathers examples of migratory desert insects come into the “evaporator”
and hairs can become exceptionally hot at the tip (80°C is not category rather than being evaders. Many species of locusts and
uncommon), enough to actually encourage heat loss to cooler air grasshoppers are neither particularly impermeable nor particularly
by convection and radiation, while at the same time the trapped cryptic in lifestyle, by desert standards. Instead they move in vast
insulating air layer prevents the heat of the pelage being relayed to numbers between patches of water or areas of recent rainfall that
the skin surface. Black color may also be appropriate in the winter are sustaining food resources, ranging over grassland and into
months for animals such as desert goats, when nights are very cold deserts, their ability to fly allowing them access to the occasional
areas of plenty within profoundly arid areas. Indeed, the true desert
locust, Schistocerca gregaria, is almost entirely restricted to the hot
Palaearctic deserts, moving continuously between wadis and oases.

EXTREME TERRESTRIAL HABITATS 641

20° 15° 10° 5° 0° 5° 10°

35°

500 km

30° Breeding areas
occupied by
25° Northeast Schistocerca
tradewinds gregaria

20° First monsoon
Southwest Second monsoon
Winter
monsoon winds
Areas occupied
15° by bivoltine
acridoids
10°
5° Breeding area
(later rains)
Breeding area
(early rains)

Dry season range

Fig. 16.22 Locust migrations around the Sahara
desert. (Adapted from Farrow 1990.)

Its movements within the Sahara are shown in Fig. 16.22, and are scrub vegetation, orientating head-on to the sun, locating the
largely determined by the seasonal movements of air masses. slightest breeze on a hillock, or wallowing in patches of mud.

16.2.4 Endurers and their strategies However, the great compensation offered by large size is that of
high thermal inertia, opening up the possibility of substantial heat
Camel, oryx, and other large mammals storage and the strategy of adaptive hyperthermia. Here the body
temperature is allowed to fluctuate rather widely on a daily basis,
The camel and oryx are the famous examples of enduring desert with heat stored during the day giving a barely tolerable peak Tb just
animals, being large endothermic mammals. The camel of the before sunset, and then dissipated during the night so that there is
Arabian and Sahara deserts is Camelus dromedarius, which in some a just tolerable minimum Tb around dawn. Using this technique
parts of its range routinely endures air temperatures up to 55°C in the camel is able to survive even when dehydrated and in the hottest
the daytime and below freezing at night. The oryx (Oryx beisa) is of deserts over a 24 h cycle (Tb range 34 – 41°C, exceptionally up to
almost equally famous as an Arabian desert gazelle with an excep- 45°C briefly; Fig. 16.23). Effectively it is acting as a storage radiator,
tional ability to withstand aridity. In the same functional category, and this is particularly obvious when the camel Tb is compared with
although less highly specialized, come some of the large gazelles of the much more rapidly fluctuating Tb of a small rodent in the same
dry grasslands and deserts, including the eland and the springbok, environment (see Fig. 16.8a). Storing heat in the daylight hours can
and perhaps also the two species of African rhinoceros and the reduce the daily water loss of a camel by up to 5 l, since it need not
African elephant. use EWL to regulate Tb tightly.

Because they are large, such mammals have real difficulties in This type of thermal behavior is aided by a light color and thin
losing excess heat through their surfaces. Much of their body is con- curly coat, especially dorsally. In stark contrast to the situation in
spicuously lacking in thick fur, as insulation would compromise cold climates, the fur of mammals from hot arid habitats reduces
heat loss even further, but many do have large appendages (ears and in thickness as body size increases (Fig. 16.24; cf. Fig. 8.17). Most
tails, or long necks and legs) where heat can be dissipated. Elephant desert gazelles are pale brown, but commonly have a darker flank or
ears viewed with infrared thermography show a remarkable rate of an almost black strip along the flank (e.g. Thomson’s gazelle,
heat dissipation of up to 70 W at a Ta of 32°C, allowing them to shed Grant’s gazelle, and springboks; Fig. 16.25), which is known to facil-
almost 100% of the animal’s total heat-loss needs when maximally itate heat gain when the animals stand side-on to the sun in the early
vasodilated and flapped gently. morning. For exactly opposite reasons many also have a white rump
and will orientate parallel to the sun’s rays at midday (Fig. 16.26),
These large mammals also tend to be very inactive in the heat of paralleling the behaviors of ectotherm evaders. Having long ears,
the day, avoiding any metabolic overload; and they will use beha- long necks, and long legs may also be adaptive in providing a range
vioral strategies to exploit any source of cooling, such as spread- of postural options for controlling heat gain and loss. Long horns
eagling against cooler rocks, seeking the shade under any desert also serve as heat dissipators, and the horns of desert wild sheep are

642 CHAPTER 16

44

42Body temperature (°C) 40
40 Body temperature (°C)
38 38
36 Dehydration Hydration
34 36
(a) 06:00 12:00 18:00 2 345 6
Time of day 34 Time (days)
1

(b)

Fig. 16.23 Daily patterns of body temperature (Tb) in a camel: (a) a single cycle of its own body weight in one drinking bout lasting just 3 min. It can
with daytime heat storage and nocturnal heat dissipation, and (b) the effects of dehydrate without compromising its blood viscosity; the fluid lost
hydration, allowing cooling by evaporation and so reducing the need for the comes from the tissues rather than blood, so that the blood com-
heat-storage effect. (Adapted from Schmidt-Nielsen 1964.) position and volume remain reasonably constant, the hemoglobin
functioning remains normal, and explosive heat death due to
notable for large internal vascularized cores useful for shedding heat reduced blood circulation is avoided. During rehydration, large
from the blood. inputs of drinking water are stored temporarily (up to 24 h) in the
gut to avoid an equally dangerous rapid dilution of the blood. Camels
A camel is also substantially aided by an ability (unusual amongst and other arid-dwelling vertebrates, including kangaroos, also have
large mammals) to endure up to 30% water loss, without losing unusually robust red blood cells that are resistant to potential
its ability to behave normally and to feed. For comparison, humans osmotic shock accompanying changes in body water content.
and other mesic mammals cannot tolerate more than 10–12%
losses (cf. Table 15.5). A camel’s special ability is that of drinking There are many special physiological tricks in the camel and the
very rapidly to replenish this deficit, up to 200 l or around one-third antelopes to help all this endurance. Some assistance comes from
good water conservation mechanisms. They have relatively low water
Klipspringer loss rates for their size (around 3 – 4 mg cm−2 h−1 in the dehydrated
1.4 oryx and Grant’s gazelle), and can produce very dry fecal pellets by

Ribbok

1.2

Grysbok Black wildebeest
1.0
Log pelage depth (mm) Blesbok Oryx
0.8
Steenbok Impala Sable antelope
Bontebok Blue wildebeest
0.6 Tsessebe
Springbok Kudu

0.4

0.2

0 Zebra
1.1 Eland

1.5 1.9 2.3 2.7
Log body mass (kg)

Fig. 16.24 The negative relation between fur depth and body size for various Fig. 16.25 Gazelle color pattern, typical of desert antelopes. (From Louw 1993.)
African desert and savanna ungulates (cf. Fig. 8.17). (From Louw 1993.)

EXTREME TERRESTRIAL HABITATS 643

Sun obscured

104 Eutherians

100 32
Desert eutherians

Percentage of animals orientating 103 Desert birds
Ta (°C)
80 30
Water flux (ml day–1)102 Marsupials

Birds
28
60 101

40 100
Desert reptiles

10–1 Reptiles

20

10–2 106
10–1 100 101 102 103 104 105
0 Body mass (g)

09:15 11:15 13:15 15:15 Fig. 16.27 Water flux in desert animals compared with nondesert species.
(From Nagy & Petersen 1987.)
Time of day

Fig. 16.26 The percentage of gazelles showing an orientation head into or away thereby saving about 60% of the water unloaded to the air in the
from the sun (white face or rump exposed); in cool periods when the sun is more lungs.
obscured they are more likely to turn sideways, when the dark flanks absorb heat
better. Ta, ambient temperature. (From Louw 1993.) The net effect of all these features that reduce water loss is a
steeper regression between water flux and body mass for larger
mammalian standards (e.g. about 40–50% water in the camel and desert animals as compared with the regressions for all species taken
the dik-dik, compared with 70–80% in temperate ungulates). As together (Fig. 16.27). This steepened regression is observed espe-
might be expected many of them also have very concentrated urine: cially in eutherian mammals, but also in birds and in reptiles.
about 4000 mOsm in the dik-dik, and over 3000 mOsm in the
springbok and camel. Of all these large enduring mammals, the Reproduction also produces some constraints in these large desert
dik-dik and the oryx are perhaps the most spectacular in their ability endurers. Most of them produce rather dilute milk (e.g. rhinoceros
to survive for very long periods with no drinking water, but of the milk has only 0.3% fat and 1.2% protein, compared with 4.0 and
two only the much larger oryx does so in real desert conditions. 3.4%, respectively, in a cow; see Table 15.13), presumably helping to
The camel, in similar conditions, can survive without drinking for offset evaporative water loss in the juvenile. Also, antelopes and
14 days. These mammals have a series of highly regulated hormonal camels need very precocial young as the habitat gives no chance to
responses to dehydration that maintain sodium and other ionic hide and the young must escape predation and be able to seek shade.
balances and water compartmentalization. Allied with precocity they are often also rather large proportional
to the adult at birth, so that they can experience the advantages of
In desert antelopes and other ungulates the occasional need to thermal inertia as soon as possible.
run in the daylight hours may involve a 30–40-fold increase in
metabolic rate, and thus an enormous heat load. While hyper- In addition to physiological features, remember some of the
thermia may be possible for most of the tissues, there is a vital need detailed morphological factors that assist the largest mammals in
to keep the brain functioning at a normal temperature. The carotid deserts. They have large flattened hooves to avoid sinking in the
rete system was first described in desert gazelles, and soon after- sand; dense protective eyelashes and strong eyelids to avoid sand
wards in the camel, where it is very well developed. This serves the damage during sandstorms; pelage that is dense on the back but
“brain cooler” function, where cool blood from the nasal heat sparse elsewhere; and a trunk shaped to give a minimal surface area
exchanger is used to reduce the temperature of the carotid artery to volume ratio when resting head-on to the sun in the heat of the
blood passing to the brain. Blood cooled in the nasal cavity is day.
diverted to the brain sinuses via the nasal and angular veins. The
muscular tone in these veins is particularly temperature sensitive, Finally, of course, we come to the famous camel’s hump. Hope-
with relaxation occurring during small thermal increments in the fully, the old wives’ tales scarcely need to be refuted: it is not full of
range 33–45°C; under the same conditions the facial veins vaso- water, nor is it full of fat as a source of water (remember that fats give
constrict, so that as much cool blood as possible is directed to the more energy per gram, and more metabolic water per gram, but
brain sinuses and carotid rete. A few animals can use the nasal heat- produce less water per kilojoule of energy, and with extra evaporat-
exchange system in a particularly sophisticated manner by expiring ive water loss also incurred when providing the respiratory oxygen
nonsaturated air, thus achieving even greater water economy in the needed for their full metabolism). The camel’s hump is simply fat
“long nose” respiratory system (see Fig. 16.20). The camels are the as a store of food as in most other mammals, but for a large desert
best known examples, as they can exhale air at only about 75% RH, animal it is sensible to concentrate the fat only on the dorsal surface
since there it also has a localized insulating effect, helping to reduce
the uptake of solar radiation from above in the day and allowing the
flanks to be used for thermal emission at night.

644 CHAPTER 16

800Osmoconcentration (mOsm) erecting the rather sparse dorsal feathers to give a thicker insulating
layer but one in which air moves freely to give some convective cool-
Urine ing. The birds also orientate face-on to the sun and droop their
wings laterally away from the thorax, giving the rather bare sides of
600 the thorax some shade and allowing them to act as thermal windows.

400 Ostriches can reduce their urine volume dramatically when
dehydrated (Fig. 16.28), with the concentration rising (though only
Plasma to around 800–1000 mOsm). In such conditions they also become
more selective in food choice, eating plants with a higher water
200 content.

0 1 2 3 4 5 6 7 8 9 10 11 12 13 Large desert birds face a particular problem in keeping their eggs
Time (days) cool; they cannot build large protective insulated nests in such an
environment. The ostrich lays its enormous eggs in a shallow scrape,
Fig. 16.28 Ostrich urine variability; the bird was dehydrated from day 4 to day 12. and relies on its own high thermal inertia and thermoregulatory
Note the minimal variation in blood concentration. (From Louw 1993.) mechanisms of panting and ptiloerection to keep the clutch cool
beneath it.
Ostrich and rhea
The ostrich, Struthio camelus, does particularly well in deserts and The Australian emu (Dromaius) is also worth mentioning as
dry grasslands, as do some other large flightless birds (ratites, its habitat ranges from high snowy mountains to the central con-
including the rhea, emu, and cassowary). Their general buildalong tinental desert, and it can maintain a constant Tb at ambient tem-
legs, long necks, and often long beaksain some ways parallels that of peratures ranging from −5 to +45°C despite being too big to exploit
the large desert mammals. any microclimatic variation. Its large thermal inertia certainly helps
it; in the deserts it uses techniques similar to those of the ostrich and
Their strategies are rather similar to those outlined above, relying rhea, while on snow slopes it maintains Tb largely by reduced con-
particularly on adaptive hyperthermia and countercurrent cooling. ductance and increased heat production, spending much of its
For example, when Rhea americana runs for 20 min at 10 km h−1 time sitting as a huddled ball with all appendages tucked in.
about 75% of the total heat generated is stored, being lost again by
radiation and convection after the bird stops running. In these 16.2.5 Desertification and anthropogenic effects
ratites the surface temperatures of all the extremities appear to be
well regulated. Most obviously, these birds again have characteristic In a sense a desert is the one type of habitat that is not really fragile
long noses and elaborate nasal turbinals (see Fig. 15.37). Ostriches and vulnerable to human interference in the way that the rest of the
are one of the very few animals, apart from camels, that can exhale globe is: for deserts are the “endpoint” of our interference in all low-
unsaturated air (Fig. 16.20); for example, in ambient air at 36°C the latitude zones (Table 16.3). Existing deserts are spreading because
exhalant air from an ostrich is at 85% RH, so recovering about 35% of human influence, agricultural practices, and grazing livestock
of the water initially evaporated into the air during inspiration and herds. In some areas entirely new deserts are being created, for
saving up to 500 g water per day. And again the cooling effect at the example where forests are felled on hill slopes and the land quickly
nose can be used to achieve brain cooling; as in other birds this is erodes into a dustbowl (Fig. 16.29). These processes are unlikely
largely via an elaborate ophthalmic rete just below the brain. to be halted; in fact desertification is almost certainly getting worse
now, and will continue to get worse into the future, because of pres-
An ostrich at risk of severe overheating also uses a combination of sure from growing human populations, especially in sub-Saharan
panting (at about 40 breaths min−1) and alterations of the plumage, Africa, and because of projected anthropogenic climatic changes
(cf. Fig. 15.65).

Once deserts have formed they are of no use to man, and so may
suffer relatively little interference, persisting as zones of low but spe-
cialized biodiversity. There have been attempts to resurrect certain
desert areas by grand irrigation schemes, ongoing particularly in
Israel and projected in other parts of the Middle East (e.g. diverting
water from the Nile to irrigate the Sinai Peninsula). However, such

Regions Fuel/wood Table 16.3 Estimated causes of desertification
Overcultivation Overstocking gathering Salinization Urbanization Other (as percentage of desertified land area).

Northern China 45 16 18 2 3 16
North Africa/Near East 50
Sahel/East Africa 25 26 21 2 1–
Middle Asia 10
Australia 20 65 10 – – –
USA 22
62 –9 10 9

75 – 2 1 2

73 – 5 – –

EXTREME TERRESTRIAL HABITATS 645

Tropic of Cancer
Equator
Tropic of Capricorn

Arid and semiarid
Increasing desertification

Fig. 16.29 Regions where desertification has increased in the last three decades. The biology of deserts is strongly dominated by the presence or
(Adapted from Williams 1986.) absence of water, setting the dynamics of resting, foraging, and repro-
ducing for all animals and imposing an unusually unpredictable
schemes tend to produce localized areas of highly specialized and regime requiring opportunistic adaptive strategies. Life appears to
artificial agricultural productivity rather than returning the land to proceed as a series of pulses of activity with long periods of relative
a natural savanna or subtropical status. quiescence in both flora and fauna. For animals that depend on the
ephemeral parts of plantsaleaves, flowers, sapathese pulses have a
16.2.6 Overview of hot arid environments direct and immediate impact, and the animals’ population densities
may thus be directly related to rainfall. For animals that rely on
Before we move on, it is worth reiterating that while we have pre- more persistent plant parts such as seeds, or which store foods in
sented a series of adaptations that desert animals may show, these nests, and for those that are omnivorous or carnivorous, the pulses
are very strongly interactive and can never be treated in isolation. To can be smoothed out somewhat, and more stable (albeit small)
take a simple example, desert insects may have very low values of population densities can be maintained.
cuticular water loss (CEWL) such that REWL is a larger proportion
of their water balance. They have a number of possible tricks to 16.3 Very cold habitats
reduce REWL, but in addition to these they may also show a lower-
ing of metabolic rate, which lowers their need for oxygen and hence 16.3.1 Types and characteristics of the cold biomes
also lowers REWL. But lowering metabolic rate means a reduction
in cellular ATP production, which leads to a reduced cellular sodium Most of the living space on this planet is rather cold, since the
pumping and a reduced sodium gradient across membranes, in turn majority of it is deep cold seas; the animals that live there were dealt
leading to a reduced sodium-coupled amino acid transport into with in Chapter 11. But even restricting discussion to terrestrial
cells. The hemolymph of these insects may therefore be low in habitats, the world is predominantly a cold place, especially by
sodium and high in amino acids. In most insects this would lead to human standards as we are essentially a tropical species by origin.
substantial urinary loss of amino acids, but since desert insects also
have a very effective rectal resorptive system they are able to sustain However, land-based temperatures that could reasonably be
their internal conditions. In this fashion many of the key physiolo- termed “very cold” are mainly encountered with higher latitude,
gical adaptations are linked together. Similar arguments clearly where the radiant energy from the sun has to travel through a
apply in relation to integrated temperature and water balance in greater thickness of atmosphere, so that it is partially absorbed, and
camels and other large endurers. what does get through must spread out over a larger area of ground
(Fig. 16.30a). The circumpolar ecosystems, sometimes collectively

646 CHAPTER 16

N
a″ b″

a′
b′

S High albedo
polar landmass
Area: a″ > a′
Atmosphere Low
(a) thickness: b ″ > b′ albedo

(b)

Fig. 16.30 Causes of reduced radiation load at high latitude: (a) input spread zones, with snow and minimal low vegetation in the short summer;
over a larger surface area, and (b) reflected by ice (high albedo) over the seas and (iii) the taiga, where coniferous forests survive. Cold biomes
or land masses. could also be said to include some areas of “cold desert”, often
found on relatively high-altitude plateaus in the interior of large
termed the boreal systems, are therefore marked by extreme cold. continents (e.g. the Tibetan plateau).
The records for the lowest temperatures in overland climates are
held by Siberia in the northern hemisphere (−68°C) and by central Polar zones
Antarctica in the southern hemisphere (−89°C). These zones also
show a negative winter energy balance (more heat is lost than is Towards the poles, low temperatures lead to snow and ice forma-
gained from the sun), and a very short growing season. tion, creating a surface of high albedo (high reflectivity), so that
some of the sparse incoming solar energy is reflected at a tangent
In most of these cold habitats there is also ice or lying snow for and lost to the system (Fig. 16.30b). Each of the polar regions
large parts of the year, creating additional and unusual problems. becomes a giant low-pressure center, with unmixed cold air at its
Intense direct and reflected radiation can cause sunburn to center hardly able to mix with the peripheral circulation of milder
unprotected animal surfaces, and “snowblindness” by dazzling and westerly winds (the “circumpolar vortices”).
damaging the eyes. There is also a more general problem with visual
sensations, as land, sea, and sky merge to give a “white-out” with Temperatures of course do vary seasonally, with a “warmer”
no shadows to assist detection of contour or of cracking unstable summer, although the growing season may last only 1 month. The
surfaces. poles experience periods when the planetary tilt means a complete
absence of direct radiation, and by definition beyond the polar
The cold biomes comprise three main biotic types: (i) the polar circles (roughly 66°N and S) there are days when the sun never rises.
zones themselves, with continuous ice or snow cover; (ii) the tundra

EXTREME TERRESTRIAL HABITATS 647

PACIFIC Cold pole SOUTH SOUTHERN OCEAN
CANADA RUSSIA AMERICA ANTARCTICA

ARCTIC
OCEAN

0 1000 AUSTRALIA
km
Midsummer 10°C isotherm
ATLANTIC 0 1000 Antarctic convergence
km Winter extent of pack ice
Midsummer 10°C isotherm Antarctic Circle
Treeline Tundra
Arctic Circle Arctic maritime
boundary
Limits of taiga

Fig. 16.31 Defining the Arctic and Antarctic, and regions of tundra and of taiga. midsummer 10°C isotherm (the line joining all places having a
(Adapted from Davenport 1992.) mean air temperature of 10°C in the warmest summer month),
which has the advantage of applying to both land and sea.
But there is a marked difference between the two hemispheres. The
Arctic is merely a frozen sea (see Plate 9c, between pp. 386 and 387), Polar areas are in many senses best seen as “cold deserts”, suffer-
but is fringed by land masses, whereas the Antarctica is a real con- ing in effect from the same kind of aridity that we met earlier in the
tinent, 3000–4000 m above sea level in parts and with another few hot deserts. This is because precipitation rate is low (zero in some
hundred or thousand meters of ice on top. The south polar region is parts of Antarctica), and any snow falls largely onto ice, so that any
therefore always colder for a given latitude, because of the presence water present is unavailable to either plants or animals, which exist
of a large icy polar continent instead of a thermally buffering polar in a “physiological drought”. The Antarctic probably contains 90%
sea. The coldest northern hemisphere temperatures are recorded of the planet’s fresh water, but in a form that is almost entirely use-
around the so-called “cold pole” of eastern Siberia, and the northern less for supporting life. In many valleys within Antarctica, at tem-
fringes of the land masses of Russia, Canada, and Greenland are peratures below −50°C where there is no snowfall, the air becomes
routinely colder than the true North Pole, again due to the amelior- extraordinarily dry, giving the most arid places on Earth with
ating effects of the thermally stable Arctic oceanic mass, which is fiercely desiccating winds. On the other hand, when snow does fall
never less than −1.86°C. However, the coldest temperatures in the it creates a covering for overwintering animals where the enclosed
south occur deep into the continent of Antarctica itself, and may be air is saturated, in equilibrium with the vapor pressure of the ice and
20°C lower than in the north. snow; thus animals burrowing within the snow are protected
against desiccation.
The polar zones are conventionally defined as the areas within the
Arctic and Antarctic circles (and thus confusingly excluding a small polar microclimates and vegetation
part of the land mass of Antarctica). However, it is more useful to a Ground temperatures towards the poles are greatly affected by
biologist to define these zones in terms of actual temperatures or in seasonal and daily changes in solar altitude, and small variations of
terms of vegetational zones. Figure 16.31 shows the possibilities. slope can have marked effects on soil temperatures. In the Antarctic
The Arctic may be defined by the treeline on the three surrounding the generally colder air and extensive ice cover produce more
land masses, although this has been substantially modified by human extreme conditions, where microclimatic amelioration may be
activities. The Antarctic may be defined by the extent of pack ice irrelevant over large areas. However, the Antarctic fringes do pro-
in winter. Alternatively each polar zone could be delimited by the vide areas where soil is protected by a thermal blanket of snow, with
relatively stable conditions 50–100 mm below the surface. In the

648 CHAPTER 16

gravelly substrates at the melt line in summer, many small inverte- semiaquatic seals, but only one truly terrestrial carnivore, the polar
brates do survive, with summer temperatures rising just above bear (Thalarctos maritimus), although in the Arctic fringes both
freezing for a few hours a day even though Ta may remain below wolves and Arctic foxes are to be found.
zero. The Antarctic has just two species of flowering plant, together
with an abundant fringe of lichens and algae. It might be thought Since in all these habitats the species number is low, the commun-
that there is little scope for microclimatic variation in such a shallow ity structure is inevitably very simple, the individual community
layer of vegetation, but in fact thermal gradients on a very small members above all requiring great capacities for endurance of cold,
scale can be most striking: for example, the surface of lichens and dark, and at times near-starvation.
mosses in the maritime Antarctic may reach 50°C at noon on cloud-
less summer days even though the air temperature 1 m above the Tundra zones
ground is only 5°C.
Tundra is a biome of low treeless vegetation, occurring in northern
In the terrestrial Arctic fringes, topography and the influence Asia and Canada, mostly within the Arctic Circle, often defined as
of the sea have a substantial influence on local climate. Hills and being where temperatures remain below 0°C for at least 7 months of
mountains lead to cloud formation and may interrupt the solar the year. It does not really occur in the southern hemisphere, simply
insolation since the sun may be close to the horizon. Hill slopes because there are no large land masses at appropriate latitudes. The
also give rise to “katabatic winds”, with warmer air flowing down tundra climate is an extreme version of continental climate, with
the slopes and giving favorable conditions; by contrast, low temper- very short summers between long, cold, dry winters. Tundra in
atures occur where the air is stagnant in valleys. Temperatures are mid-continents is so cold all year that the deep ground is in the con-
always highest in summer within the reasonably substantial plant dition known as permafrost, with no penetration of free liquid
boundary layer, where there may be a temperature excess of at least water. In the shallow layer of “active” soil, above the permafrost in
20°C above ambient amongst small plants. Temperatures may also summer, there may be a negative thermocline, i.e. temperatures
be raised by several degrees in the soils up to 10 cm below such vege- may decline with depth down to the permanently cold permafrost
tation and also below lichens and moss turf. Wind speeds may limit layer; this layer may also be almost permanently waterlogged.
this temperature augmentation, however, especially in areas of very Alternating freezing and thawing also make this layer physically
patchy discontinuous vegetation. unstable, and it may become highly fractured.

polar fauna Nearer the coasts the soil and climate can be much more variable,
In the true Antarctic there are no entirely terrestrial animals except a depending on the extent of snow cover. Here an abundance of snow
few mites and two species of midge; the mite Nanorchestes antarc- keeps conditions less cold, but also delays the onset of spring growth.
ticus is the most southerly invertebrate known, occurring within 5°
latitude of the South Pole. Even on the fringing maritime Antarctic tundra microclimates and vegetation
islands the species diversity is remarkably low, with a limited soil The characteristic vegetation is abundant moss and lichen; at best
fauna of nematodes, tardigrades, and rotifers, and further mites and there may also be very sparse and very low-growing trees (especially
insects, including some lice and fleas associated with semiaquatic dwarf willow), and some coarse grasses (see Plate 9d, between pp. 386
birds and mammals. This probably reflects the geographic isolation and 387). No large trees or shrubs can survive, because the permafrost
from sources of invading species and the unfavorable direction of precludes taproot penetration, and tall plants with shallow roots
winds for dispersal of small species (most of which are wingless). would inevitably be blown down. The majority of the living plant
The paucity of animal species is also partly because the Antarctic has tissue exists underground as roots and extensive rhizomes, and in
nothing like a continuous cover of plants, so that there can be no fact most of the organic carbon is in the form of undecomposed dead
real herbivores. All the larger animals present are semiaquatic and remains, with only 2% of it “alive” (compared with perhaps 50% in
instead depend on the sea for food, with seals, whales, and penguins most of the forests of the world). Low cushion-like growth helps to
dominant, subsisting on the fish and the often very large (see section trap this dead material and allow local, slow nutrient recycling.
11.1.4) marine invertebrates. Of all animals, penguins are the most
profoundly adapted for polar life, the emperor penguins (Aptenodytes At these high latitudes thick snow may cover the ground to a
forsteri) breeding in midwinter in continuous dark at temperatures depth of several meters during most of the winter months, and this
down to −70°C. Antarctic birds in general, and penguins in particu- provides a whole range of possible habitats. Thick snow has poor
lar, are the most important members of their ecosystem, in terms of thermal conductivity and acts as an excellent insulating layer
both biomass and of interactions with other components of the between cold air and the soil surface, which in many areas is warmed
environment; they also import organic material from the sea onto to around 0°C by geothermal energy so that it remains unfrozen.
the land. In fact the lowest soil temperatures through most of the tundra
zones are typically recorded in the fall rather than in winter. Even
The Arctic, by contrast, having a fringe of plant life on the enclos- in extreme inland regions the minimum winter temperatures at the
ing land masses, possesses a surprisingly abundant invertebrate soil surface under leaf litter and snow are only − 4 to −7°C.
fauna, notably spiders, mites, springtails, biting flies, lice, and a
reasonable range of butterflies. There is also a substantial burrowing Tundra lichens are so well protected biochemically (usually
fauna, including enchytraeid oligochaete worms but surprisingly by glycerol) that they never freeze, providing year-round food to
lacking in beetles (at least when compared with their abundance anything that can find them. Many of the larger evergreen plants
in other habitats). Above ground there is again a wide range of have small leaves with thickened and hairy cuticles, and most have
vegetative budding from runners with protected ground-level buds
to allow rapid growth in spring.

Abundance (numbers m–2) Tundra Abundance (numbers m–2) EXTREME TERRESTRIAL HABITATS 649
107
106 Northern coniferous forest (taiga)
105 107
104 106
103 105
102 104
10 103
102
1 10
0
OGAlATiaACNMPpamgsrttryoetIPporaeelrRdpisrrhicmcaoioeoayygthahnppiprpptggfanaoooiooaoooreeddttidtdddddraaaaaaaaaaaaa 1
0
OGAlATiaACNMPpamgsrttryoetIPporaeelrRdpisrrhicmcaoioeoayygthahnppiprptpggfanaoooiaoooooreeddttidtdddddraaaaaaaaaaaaa

Biomass (g live wt m–2) 16 16Biomass (g live wt m–2)
14 14
12OGAlATiaACNMpPamgsrttyroetIPporaeelrRdpsihrricmcaoioeoayygthahnppiprpptggfanaoooiooaoooreetddtiddtddddraaaaaaaaaaaaa 12 OGAlATiaACNMpPamgsrttyroetIPporaeelrRdpishrricmcaoioeaoyygthahnppipprptggfanaoooaoiooooreeddttiddddtddraaaaaaaaaaaaa
10 10
8 8
6 6
4 4
2 2
0 0

(a) (b)

Fig. 16.32 (a) Abundance and (b) biomass of tundra and taiga fauna. mites, springtails, and nematodes present in particular abundance,
(Adapted from Little 1990, courtesy of Cambridge University Press.) and with a surprisingly high biomass of enchytraeid earthworms.
Some gall-forming insects occur on dwarf willow at most latitudes.
tundra fauna
The fauna is inevitably sparse, but there is scope for a reasonable The tendency described in the introduction to this chapter to be
range of rather specialist herbivores. The large herbivores, such as large or small, but relatively rarely in the middle size ranges, there-
reindeer or caribou (Rangifera), migrate south to the timberline in fore clearly applies (except perhaps for the special case of migrating
winter and move back to the tundra to breed. Medium-sized herbi- bird species). There are also many examples in the tundra illustrat-
vores such as musk ox (Ovibos), dall sheep, and snow sheep (Ovis) ing “Allen’s rule”, where animals have relatively small extremities
stay put and survive the winter feeding on lichens. In addition there compared with their temperate relatives, to avoid undue heat loss.
are small vertebrate herbivores such as Arctic hares and above all The tundra rodents and mustelids generally have small ears and toes
lemmings (microtine rodents). In summer, the tundra is invaded by and short tails, as do many polar birds and mammals, particularly in
waterfowl, especially geese, using the long daylight hours to feed. their juvenile stages. The rule is particularly well illustrated by foxes,
There are relatively few large predators, the commonest being vari- where the relative sizes of ears, noses, and paws decrease progres-
ous mustelids and wolves; avian predators include the snowy owl sively from desert species (kit fox and fennec fox) through the ubi-
and the gyr falcon. Many of these mammals and birds turn white in quitous temperate red fox to the Arctic fox. The same rule may apply
winter, giving a high degree of crypsis. to ectotherms: legs, antennae, and mouthparts may be shortened in
northern insects, and the incidence of brachyptery (reduced or absent
The conspicuous fauna is therefore almost entirely composed of wings) is also higher in Alaskan dipterans than in other faunas.
endotherms. Towards the southern edge of the Arctic tundra the
species diversity increases though, with a few reptiles surviving; the Boreal forests (taiga)
common adder (Vipera berus) occurs throughout northern Norway
well into the Arctic Circle, and lizards of various kinds are also The more northerly forests of the world are often labeled “taiga”,
found in Norway, as well as in the southern tip of South America from a Russian word for “swamp forest”. They stretch in a wide belt
within the Antarctic Circle. across Canada (see Plate 9e), Scandinavia and northern Europe, and
most of Russia, from the northernmost treeline down to a gradual
There is, of course, also a cryptic invertebrate fauna living in and merger with more deciduous temperate forests (see Fig. 16.31).
on the vegetation and thin decomposing layer (Fig. 16.32a), with These northern boreal coniferous forests are not really matched in

650 CHAPTER 16

Nest (lined by grass/leaves) –10°C
Lemming

10 –20°C Vegetation
Burrow
10 –20°C

1– 8°C

Soil (unfrozen) Ptarmigan in snow hole Fig. 16.33 Microclimate within snowathe
subnivean habitat. (Adapted from Davenport 1992.)

the southern hemisphere, again because land masses are much The fauna of cold biomes is clearly dominated by small inverte-
smaller at the relevant latitudes, although some of the southern brate ectotherms and by relatively large bird and mammal endo-
beech forests of southern Chile and Argentina do present some therms, each of which have their special adaptations. Although we
substantial parallels. will deal with these separately, it is important to remember that
some of the adaptations discussed apply to both groups. In par-
The climate allows only a short growing period (2–3.5 months), ticular, all the animals that survive at high latitude use behavioral
since it is too cold for much of the year and the fairly warm summers strategies as a first line of defense against the cold, and this is true for
have limited rainfall. Soils are nutrient poor and strongly acidic, both ectotherms and endotherms. The major behavioral strategies
commonly called “podzols” and turning with time into peats; to be found are exploitation of favorable microhabitats, migration,
remember that peats warm up only slowly but dry out rather easily and the development of gregarious habits. Similarly all of them are
(see section 15.1.2). likely to share biochemical strategies of enzymes with lower tem-
perature optima and membranes with homeoviscous adaptation.
taiga microclimates and vegetation For each category of animal we cover behavioral strategies first and
Conifers always dominate, usually in low diversity, so that these then move on to physiological adaptations.
regions have a dense layer of decomposing conifer needles up to
100 mm deep, producing a very acid effect but providing a ther- 16.3.2 Small ectotherm evaders and their strategies
mally buffered zone. There may be larger areas of peaty swampland,
dominated by mosses. These swamps are in part created by inter- Use of microhabitats
mittent bouts of tree loss in natural wildfires that sweep through the
forests, feeding on the resinous undergrowth and litter and some- As always the utility of behavioral tricks is much enhanced for smaller
times clearing thousands of hectares at a time. Within snow-covered animals. In the polar zones their choice, and exploitation, of some-
areas a subnivean habitat results where temperatures in burrows what less severe and more sheltered microhabitats is particularly
may be quite mild (Fig. 16.33) especially when gregarious endo- evident. The winter temperature range beneath the snow cover (sub-
therms are present. nivean zone) is markedly less than the range of air temperature above
snow, and this microhabitat is exploited by a whole range of animals
taiga fauna (see Fig. 16.33). The advantages of this way of life are greatly enhanced
Apart from the moose, herbivores tend to be of only moderate size by the penetration of light through snow, allowing plants to stay
(usually smaller than those of the tundra): marmots, squirrels, and green and edible. Many invertebrate herbivores exploit this resource,
voles are common, many relying on seeds and berries and also taking and some are specialized as gall-formers, getting added protection
invertebrates as food. Small carnivores are drawn especially from the from the modified plant tissue they induce (see Chapter 15).
mustelid group (martens, sables, ermineathese zones are the center
of the fur trade). Larger carnivores include bears, wolves, snow To create and manipulate microclimates, burrows can be dug
leopard, Siberian tiger, and lynx. There are many owls and raptors, into the snow itself, or below it into the litter or soil layers. Some
and specialist conifer-feeding birds such as grouse and crossbills. toads in the taiga zones can burrow down more than 1 m to get
Few ectotherm vertebrates live in these forests, although there are below the frost line; large numbers of beetles and other ground-
rare amphibians such as the wood-frog (Rana sylvatica) and a few dwelling insects also occur at this depth in winter.
cold-tolerant reptiles (again including the adder) right up to the
Arctic Circle. Huddling and aggregation

Invertebrates in the soils are dominated again by nematodes, Huddling behavior is the commonest form of gregariousness used
springtails, and a particularly high abundance of mites (Fig. 16.32b). as a thermal strategy, and is very obvious in a whole range of animals
Sawflies, gall-midges and weevils (insect groups often specialized in from cold habitats. Its effectiveness increases as the difference
feeding on conifers), and a plethora of biting flies, are evident above between air temperature and preferred Tb increases, and with the
ground.

EXTREME TERRESTRIAL HABITATS 651

Midday

am pm

Corolla

Highly
reflective
surface

(a) (b)

Fig. 16.34 Arctic flowers acting as (a) parabolic reflectors and (b) sun trackers to at low temperatures, relative to temperate species. But they must
give a warm microclimate around their ovules, exploited by many small insects. also be good thermoregulators of necessity, and must make any pos-
(Adapted from Kevan 1975.) sible use of the minimal heat inputs available. Most boreal animals
are highly adept at behavioral thermoregulation by microhabitat
number of participating individuals. Examples among the smaller choice and aggregation, as described above, but can also utilize
invertebrate ectotherms are not particularly well studied. The mite sophisticated basking techniques, as with the examples we looked at
Alaskozetes aggregates in clusters under rocks, and other mites and in temperate habitats (see Chapter 15).
some collembolans also aggregate, although it is debatable whether
this is real thermally advantageous huddling or just a shared pre- A small ectotherm may raise its Tb at least 25°C above ambient by
ference for the same microhabitat. Amongst the reptiles several basking in the polar summer. Basking butterflies from Greenland
cases are well known, with winter aggregations occurring in many and Canada have been studied in some detail, and they can warm
snakes and lizard. The adder is a familiar example, with dens of up to themselves very substantially above ambient using their wings as
80 individuals having been found in Finland. Similarly the red-sided heat gatherers. Many are melanic, the darker color improving
garter snake, which occurs in western Canada (where the winter absorption. Arctic fritillaries are dorsal baskers (see Fig. 15.22), the
temperature is often −40°C), shelters in huge groups of thousands at dorsum of the wings being dark, while Colias butterflies are lateral
a time in sink-holes beneath the snow. baskersathe Arctic species (e.g. C. hecla) are unusually dark in color
especially on the ventral sides of the hind wings; their extra melan-
Migration ism allows them to achieve an excess temperature up to 80% greater
than lighter forms. Note that, in addition to basking, contact with
Long-range migration is not a very common strategy for ectotherms the substrate is also used to warm the body in many of these Arctic
from cold climates. There are, however, just a few spectacular ex- insects. Butterflies use bare ground for contact warming, seeking
amples: the monarch butterflies (Danaus plexippus) that move en warm and sheltered spots.
masse from sites in Canada and the northern USA each year to over-
winter in Mexico are the best studied case, though only some of them Basking also occurs in wingless insects, the best example being
come from really cold habitats. These butterflies then spend the winter the “woolly bear” caterpillars, Gynaephora groenlandica, which may
in huge aggregations, subsisting largely on their stored lipid reserves spend up to 60% of their active time in basking and only 20% in
(triglycerides, derived from summer feeding on nectar) as there are feeding. This species may spend as long as 14 years in the caterpillar
inadequate nectar supplies to maintain them in the Mexican forests. stage, reflecting its very slow growth rate.
Colias butterflies also migrate seasonally from genuinely Arctic
habitats in northern Scandinavia to the southern Baltic regions. There are also some specialist cases where insects use particular
species of flowers as basking warm-up sites (e.g. Dryas integrifolia
Thermoregulation and the Arctic poppy Papaver radicatum). These flowers are shaped
like bowls, and they rotate by phototropism so that the corolla
Small terrestrial animals from cold climates must have highly cold- always points towards the sun as it passes across the sky each day
adapted enzymes and membranes. For example, the mite Alaskozetes (solar tracking). Their shape acts as a parabolic reflector to concen-
shows low enzyme activation energies and elevated metabolic rates trate radiation into the center of the bowl of the flower, raising it by
5–8°C above ambient (Fig. 16.34). Mosquitoes, hoverflies, blowflies,
and danceflies all exhibit a raised Tb in association with sitting in
these flowers.

652 CHAPTER 16

Larger polar ectotherms may also use basking as a key component 400
of their thermal strategy. The adders and lizards of northern Norway
may bask for large parts of the 20 or more hours of daylight in the Concentration (µmol g−1 wet wt) 300
summer, feeding between basking bouts to permit lipid stores to be
built up for the winter. Glycerol
200
In the case of a few large insects, although nominally ectothermic,
remember that a component of endothermy also comes into play Sorbitol
in achieving thermoregulation. The Arctic bumble-bee, Bombus Glycogen
polaris, found in northern Canada, is able to fly at low temperatures 100
due to its inherent endothermic warm-up (see Chapter 15), and the Trehalose
same almost certainly applies to several Bombus species found in
northern Scandinavia. These species also use endothermic warm- 0 0 –10 –20 –30
up at times of egg production, the queen pumping warm blood to 20 10 Acclimation temperature (°C)
her abdomen to speed up egg maturation, and then staying at an
elevated Tb to brood the larvae within the nest. Fig. 16.35 Sorbitol and glycerol synthesis in the gall-fly Eurosta at decreasing
acclimation temperatures, using up glycogen stores to make the cryoprotectants.
Coping with freezing (Adapted from Storey et al. 1981.)

Diverse taxa have adopted the “freeze tolerance” strategy discussed small crystalline particles within key tissues such as the Malpighian
in Chapter 8, involving some tolerance of extracellular ice forma- tubules.
tion, with cryoprotectant polyols or sugars to prevent damage.
Examples include many terrestrial insects, a few other arthropods Many animals show seasonal patterns of glycerol content, of
such as centipedes, a range of gastropods, annelids, and nematodes, supercooling point, and of melting and freezing points (Fig. 16.36).
and several species of frogs, lizards, and turtles that overwinter on Examples of the supercooling points (SCPs), and the solutes used to
land. Recent evidence shows that in polar nematodes freezing may produce them, are shown in Table 16.4 for a range of terrestrial
also occur intracellularly, an otherwise unheard of phenomenona ectotherms that are freeze tolerant; the values are not exceptionally
the worms freeze in all body compartments, and can subsequently low, with a slow controlled freezing at moderately high subzero
melt, grow, and reproduce apparently normally. temperatures being preferable. Values of −5 to −25°C are clearly
quite common, and there is a general correspondence between SCP
Among the insects, freeze tolerance is the exception rather than and the normal site of overwintering: species that survive in vegeta-
the rule, but is widespread in some families from the Coleoptera, tion have lower values than those that spend the winter in caves or
Diptera, Hymenoptera, and Lepidoptera, especially in larvae and other more protected locations. Remember that polyols also give
pupae but rarely in adults and apparently never in eggs. In many protection against desiccation, which may be an important factor in
insects low temperature is the immediate trigger for polyol syn- insects that overwinter in very cold dry air. For example Fig. 16.37
thesis, in conjunction with other environmental cues, which might shows the variation in glycerol content in relation to humidity in the
include photoperiod, humidity, food availability, and to a lesser polar mite Alaskozetes. Cold and drought are both potential prob-
extent endogenous factors such as hormones and the physical lems for high-latitude animals, but the biochemical and physiolo-
changes of diapause. Among the best studied insects are a parasitic gical strategies to deal with both problems are often complementary.
wasp, Bracon cephi, the high Arctic caterpillar Gynaephora, and the
larvae of the goldenrod gall-fly, Eurosta solidaginis. In Bracon larvae, Many of the polar arthropods can tolerate substantial ice forma-
which overwinter in frozen Canadian prairies, glycerol is present at tion in their extracellular fluids. In some species up to 90% of this
up to 25% body weight in winter, giving a supercooling point as low water may freeze, particularly when the animal is in contact with
as − 47°C. Gynaephora caterpillars can spend as long as 10 months external ice and undergoes “inoculative freezing” from the outside
every year in a frozen state, at −50°C or lower. In field populations of inwards. Precautions against contact with ice are often present to
Eurosta, which survive a mere 12 weeks in the frozen state, long- limit the risk; examples include the use of silken cocoons in many
term chilling at the right time of year is required to initiate glycerol lepidopterans, or galls as in Eurosta, or specially impregnated winter
production: at least six consecutive days with daily average temper- burrow walls in some beetles. Where ice contact is unavoidable,
atures of less than 5°C in mid-November. Laboratory experiments slow, safe freezing is promoted by INAs in the hemolymph, and pro-
show that glycerol is synthesized first, followed by sorbitol as the tein nucleators are fairly common in insects as part of the protective
temperature falls (Fig. 16.35). Glycogen is clearly the source of these
polyols, and the glycogen phosphorylase enzyme in the fat body is
cold-activated, with low temperature causing a rapid conversion
from the inactive to the active form. From September to November
the larvae also accumulate monounsaturated fatty acids at the
expense of saturated forms, suggesting activation of a ∆9-desaturase
enzyme (see Chapter 8). However, traditional ice-nucleating agents
(INAs) have never been identified in Eurosta, and recent evidence
indicates that calcium phosphate performs this role, existing as

EXTREME TERRESTRIAL HABITATS 653

–5

30 –20

–4

25 –25 Supercooling point (°C) Freezing point
Freezing and melting points (°C)
Per cent glycerol 20 –30 –3
Glycerol –35
–40 –2
15 –45
Supercooling points –1
Melting point
10
0
5 Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul
(b) Month
Oct Nov Dec Jan Feb Mar Apr
(a) Month

Fig. 16.36 (a) Seasonal changes in glycerol contents and supercooling points in Table 16.4 Supercooling points (SCPs) in species living at subzero temperatures.
the larvae of a caterpillar, and (b) in the melting point and freezing point of a
larval beetle. (From Hansen 1973.) Species SCP (°C) Known solutes

Glycerol concentration (µg mg–1 body water)70 26% 42% Spiders −15.4 Glycerol, AFP
60 Clubiona −26.2 Glycerol, AFP
50 55% Philodromus
40 −30 Glycerol, polyols
30 Mites
20 Alaskozetes −5.0 Glycerol
−18.2 Glycerol, sorbitol
10 Lepidoptera −26.1 Trehalose, amino acids
Pringleophora −26.2 Trehalose, amino acids
5 Isia −31.5 Glycerol, trehalose
100% Nemapogon −44.6 Glycerol
Pieris
1 7 14 21 28 35 49 Laspeyresia −10.0 Glycerol
0 Days Alsophila −10.3 AFP
−12 Glycerol, sorbitol, AFP
Fig. 16.37 Glycerol contents (means ± standard errors) of the mite Alaskozetes at Beetles −32.4 Ethylene glycol
4°C are moderated in relation to humidity, with glycerol gradually disappearing Pterostichus −34 Glycerol
at high humidities. (From Cannon & Block 1988.) Meracantha
Dendroides −8.6 Trehalose
mechanism. For larvae of the crane fly Tipula trivittata, both protein Ips −27.7 Glycerol
and lipoprotein nucleators have been identified in the hemolymph. Dendroctonus −28.7 Glycerol
The ice-nucleating protein from the wasp Vespula maculata has −41.2 Glycerol
been purified and is a protein of relative molecular mass 74,000, Hymenoptera −49.2 Glycerol
with an amino acid content that includes 20% glutamate/glutamine, Trichiocampus
12% serine, and 11% threonine. Megachile −6.0 Sugars, amino acids
Camponotus −7 Sorbitol, INP
Amongst vertebrates, at least four species of North American Bracon −10.3 Glycerol, sorbitol, trehalose
frog, the Siberian salamander (Salamadrella keyserlingii), and even Eurytoma −32.7 Glycerol
some reptile species can also tolerate freezing. Either glycerol (in the −49.1 Glycerol
Flies
Xylophagus −2.0 Glycerol, glucose
Tipula −2.0 Glucose
Eurosta −3.0 Glucose
Diplolepis −3.3 Glucose, amino acids
Rhabdophaga −2.9 ?None

Vertebrates
Hyla
Pseudacris
Rana sylvatica
Turtle
Northern ground squirrel

AFP, antifreeze protein; INP, ice-nucleating protein.

654 CHAPTER 16

25 wood-frogs (liver, heart, and brain) compared with 1–5 µmol g−1
in unfrozen frogs. The rapid distribution of glucose from the liver
20 is critically aided by the ability to move this sugar across cell
membranes, out of the liver and into other organs via glucose
Tb (°C) 15 Frog temperature transporters (see Chapter 4); cAMP and protein kinase A are also
10 mobilized during this process. For wood-frog liver the vmax value
for glucose transport by membrane vesicles is 70 nmol mg−1 s−1 at
5 10°C, compared with only 8 nmol mg−1 s−1 for the common tem-
perate frog Rana pipiens. The total number of transporter sites is
0 4.7-fold higher in the liver of the freeze-tolerant species, and varies
seasonally in that species by about eight-fold. There is also a gradi-
–5 ent of glucose concentration from the core to the peripheral tissues,
which enables the frog to thaw uniformly, thereby avoiding tissue
300 Liver damage in the spring. The thawing of frogs can now be studied by
proton magnetic resonance imaging, since the signal undergoes a
Glucose content (µmol g–1) 200 Blood large change during the transition from ice to water; protons in ice
are invisible to this technique and frozen areas therefore show up as
100 Leg black. From such studies it is clear that the liver and heart thaw first
muscle during recovery from freezing, so that their vital functions can begin
while the rest of the frog is still thawing out. We are also beginning
0 38 to understand the processes that occur at a gene transcription level
Time (days) during freezing in this species.

Fig. 16.38 Levels of glucose in the tissues of the freeze-tolerant frog Rana sylvatica Freeze-tolerant animals must survive and maintain some degree
as its body temperature (Tb) declines. (From Storey & Storey 1984.) of homeostasis despite a lack of circulating fluids. Their enzymes
must be able to tolerate very low temperatures and very high salt
tree-frog Hyla versicolor) or glucose (in some wood-frogs and in the concentrations. For many of them, in the frozen state energy pro-
lizard Lacerta vivipara) is used as a cryoprotectant in the few cases duction switches to the hydrolysis of phosphagens, phosphoargi-
that have been studied. The wood-frog Rana sylvatica, which is nine (PAr), or phosphocreatine (PCr) (see Chapter 6), followed by
found north of the Arctic Circle, is by far the best studied vertebrate anaerobic glycolysis with lactate and alanine as end-products. The
freeze tolerator. Here the levels of glucose in the muscle, liver, and metabolic rate is usually greatly depressed (to 5–10% of normal
blood begin to rise about 14 days after Tb reductions are induced in resting values), giving a typical hypometabolic state.
laboratory studies (Fig. 16.38). But at least some of the frogs do not
back up their cryoprotectants with nucleating agents, and instead Avoiding freezing
appear to rely on their relatively large size to keep the cooling rate
slow enough to insure that ice only forms extracellularly. Frog skin Many animals that encounter subzero temperatures are freeze
is highly water permeable, and an important part of the strategy for intolerant but are able to survive by virtue of the phenomenon of
winter survival is the choice of a well-protected and humid hiberna- supercooling alone. Such animals must eliminate or mask all INAs
tion site where temperatures will fall only slowly. as winter approaches. The small terrestrial mites and insects that
cannot tolerate ice formation use additional strategies to assist their
R. sylvatica is famous for its ability to survive repeated freezing of cold-hardiness: they allow the body to become very dehydrated,
its whole body, with all breathing and circulation stopped and the to reduce the availability of freezable water, and they may void their
nerves unresponsive to stimulation. It will survive for 3–14 days in guts as winter sets in, to clear any potential ice nucleators. As a result
any one freezing cycle, and when frozen a single frog may contain of all these mechanisms, a number of Arctic species have lower crit-
7–8 g of ice in its coelom and beneath the skin, indicating that ical temperatures of −55 or even −70°C.
65% of its body water is tied up in the frozen state and all of its
organs must be substantially dehydrated. Nevertheless, on thawing Springtails and mites, among the most important components of
it recovers all its functions, with excitability of the peripheral nerves polar soil fauna, are almost invariably freeze intolerant and rely on
and simple reflexes being reinstated in 5–14 h. There is an in-built their supercooling properties for survival. The supercooling points
seasonality in the frog’s cryobiology, with fall frogs better able to of circulating fluids in these cold-hardy but freeze-intolerant
survive longer and harsher freezing than summer frogs; the fall frogs animals are usually (though not invariably) very low compared with
have higher osmotic concentrations and glucose concentrations in those in freeze-tolerant species. Antarctic mites and Arctic insects
their plasma. Glucose is produced from massive glycogen stores (up can generally supercool down to −30 or even −40°C, with eggs and
to 180 mg g−1 are built up in the liver before hibernation), and syn- pupae showing even lower values. Some animals can remain almost
thesis of the cryoprotectant glucose is triggered by the beginnings fully active at subzero temperatures. For example, Alaskozetes
of ice nucleation in the body (often when ice first begins to form on antarcticus (body mass 150–200 µg) shows peak locomotory activ-
the skin of the frog), via an adrenergic and cAMP-mediated signal ity at 16–24°C but does not enter cold stupor until about −5°C.
transduction system. As Fig. 16.38 shows, glucose concentrations Another Antarctic mite, Nanorchestes antarcticus, has even been
may reach 150 –300 µmol g wet wt−1 in the core organs of frozen observed moving at −11°C, but it has a relatively high temperature

EXTREME TERRESTRIAL HABITATS 655

requirement for optimum activity, reflecting the high temperatures form of torpor/dormancy, probably because full diapause could be
found at the radiative surface on the mosses, algae, and lichen on inappropriately triggered by a period of poor summer weather.
which this species lives. Torpor may also occur in larger animals, including the relatively
rare vertebrate ectotherms in cold climates; in reptiles such as the
In some of the polar insects and mites glycerol acting as an anti- cobra, living on cold plateaus, it leads to a drop in blood sugar and
freeze can reach concentrations of 25% of fresh body mass during pyruvate and an increase in blood lactate, but also to a rise in non-
the winter. In addition, due to their small size these animals protein nitrogen and particularly uric acid levels, indicating protein
undergo substantial dehydration, which reduces their content of catabolism. This is in contrast to endothermic vertebrates, where
freezable water and elevates the effective antifreeze concentration. torpor is accompanied mainly by lipid catabolism.
Antifreeze proteins (AFPs) are also now known to occur in some
mites, spiders, and insects (as well as in the polar fish where they Reproduction itself may also be highly specialized. In insects the
were first identified, described in Chapter 11). The associated anti- females are often wingless and almost immobile (e.g. in crane flies
freeze mRNA has been studied in some northern temperate insect and midges) and males seek them out, presumably using phero-
species, and its activity is inducible at around 2–4°C in the laborat- monal cues. The red-sided garter snake provides another example of
ory, but induction only occurs in winter, and cannot be achieved specialized reproductive behavior; the males emerge synchronously
after about February in these tissues. This suggests that AFP syn- from the winter dens in spring, then the females come out in small
thesis normally involves an interaction of low temperature priming groups and are immediately set upon by males, forming massive
with an endogenous clock system. AFPs tend to be recycled in spring “mating balls”. Each female then bears up to 30 live young. The
as amino acids for growth and egg production. triggers for emergence are unknown, and androgens in both sexes
seem to be at very low levels.
Although freeze tolerance may be a “cheaper” strategy (see Chap-
ter 8), recent evidence suggests that freezing intolerance may be Viviparity in the vertebrate ectotherms is rather common (e.g.
the better strategy in low temperature but thermally quite variable Vipera and Lacerta amongst the reptiles). This may be because
environments, such as the maritime Antarctic margins. Here small retention in the mother’s body, which is undergoing typical
terrestrial springtails and mites are very common, and switching shuttling heliothermy to maintain its Tb, is the best way of keeping
rapidly from inactive to active states may be the ideal way to exploit development of the young at a fast and steady rate.
winter thaws and avoid summer frosts.
Feeding and predation
Life cycles
As in the extreme desert environments, foodstuffs may pose a prob-
Almost all the small “evader” animals from cold climates have lem. Many of the small invertebrates are omnivorous with little diet
specialized life cycles, in which multivoltinism (having many gen- specialization, taking only detritus for much of the year. Macro-
erations per year) is very rare indeed. Usually the invertebrate fauna vegetation may be unavailable or deeply frozen, and is heavily
show very brief active periods during summer, otherwise being in a physically defended, so that animals with food storage habits are
resting state as eggs, pupae, etc. They may achieve fairly “normal” favored. However, lichens remain unfrozen so that caribou, using
growth rates during the brief summer, but inevitably have lower their hooves to dig and tough lips to forage, can survive year-round.
annual growth increments. This results in two main patterns of life Green plants may also remain in a minimally active state within the
history, each requiring substantial flexibility and opportunism. snow layer, with just a little light penetrating, providing enough
food for the burrowing rodent populations. Small populations of
The first strategy involves univoltinism and adult lifespans that carnivores are found in tundra and taiga, and large populations of
are greatly reduced, so that in some insect species the eggs mature biting ectoparasites are also to be found, benefitting both from
within the pupal phase, with emergence, mating, and oviposition blood meals and from the microclimates created by their hosts.
squeezed into just a few days of suitable weather. On the other hand,
while retaining univoltinism and an opportunistic burst of repro- 16.3.3 Large endotherm endurers and their strategies
ductive activity, there may be a life-cycle extension to 2 or more
years in other taxa that normally complete the cycle annually, so Use of microclimates and burrows
that there is much overlap of generations. Mites and springtails have
particularly long lifespans (5 years in Alaskozetes), as does the cater- The subnivean vegetation is a food resource for some small spe-
pillar Gynaephora referred to above. Pardosa wolf-spiders may have cialist herbivorous mammals such as lemmings and shrews. They
a 6-year life cycle, whereas temperate relatives take only 1 year; the in turn become a food source for small carnivores like foxes and
high-latitude populations mature at a much later age. Even within a raptors. Thus a whole submerged community exists through the
species the effect can be striking; for example, the springtail Hypo- winter, and some of the mammals even choose to reproduce in
gastrura tullbergi lives 3–5 years in polar regions and just 2–12 winter because of the benefits of snow cover.
months in temperate regions. Water-striders (bugs living on the sur-
faces of fresh water) have univoltine cycles with an obligate winter These animals all exhibit a form of microhabitat selection, but
diapause in Quebec but show a southwards cline to a bivoltine cycle; for the large ones it is more specifically expressed as a burrowing
interestingly, total reproductive output is similar at all latitudes. behavior. Perhaps the most famous mammalian examples are the
lemmings, found in most of the northern tundra areas throughout
In many Arctic insects “hibernation” can occur at any stage the year. They dig winter burrows within the snow, lined with grass,
except the egg, to facilitate this lengthened life. In some cases this where they live gregariously and do not enter torpor; in fact these
may be a true diapause, but more commonly it may be a less specific

656 CHAPTER 16

Musk ox
Caribou
Birds

Fig. 16.39 Migration patterns in tundra animals. facing into the sun with the wings (or in the case of seals the tail
flippers) raised and splayed out.
winter burrows may be warmer places than the lemmings’ summer
holes dug in the earth. Rodents in the tundra and taiga biomes have Migration
a particular problem in being the major prey for raptorial birds, so
their burrows provide an important escape from predation as well Migration is the most striking behavioral strategy shown by the
as a climatic refuge (though owls can hear lemmings even under a bigger polar animals, and could be seen as a larger scale version of
dense snow layer). Some raptors can also detect rodent abundance the movements between microhabitats discussed above. It is also
by perceiving the ultraviolet emission from deposits of urine and perhaps the equivalent of a life cycle involving resistant stages in
feces. Therefore lemmings in Scandinavia and Canada have elabor- terrestrial polar invertebrates, providing an escape in space rather
ated the architecture of their summer burrow, unusually for a than in time. It is infrequently encountered in ectothermic tetrapods,
rodent, to include a latrine area so that no clues are left above the reptiles and amphibians, since their locomotory speeds and
ground. In winter, when predation risk is much lower, their snow endurance are limited. But there are many endothermic examples,
burrows have no latrine and they defecate freely away from the nest. classic cases being the caribou and reindeer, migratory mammals
The burrows of ground squirrels, used during winter torpor, are that trek overland to the forested taiga zones as winter approaches,
also decidedly elaborate, and are thought to act as biological con- and the lemmings with their fall migrations southward. Polar bears
densing towers, water evaporating from the warm lower levels and also migrate south across the frozen Hudson Bay in winter. Among
recondensing in the upper cold levels, where it may be available as the birds migration is especially common since movement by flight
an important water source for the squirrels when they arouse. is energetically favorable. Penguins of course miss out on this bene-
fit; many of the smaller penguin species merely move away from the
Permanent Arctic residents among the birds also use snow Antarctic mainland and spend the winter at sea or on small islands
burrows, although rarely gregariously; the classic example here such as the Falklands and South Georgia. But high latitudes in
is the burrowing rock ptarmigan, rather larger than a lemming. summer provide areas of high productivity and thus serve as good
Burrowing is also employed quite extensively by seabirds at high feeding grounds for flying birds, with ducks, terns, and many waders
latitudes. Petrels and shearwaters dig into rock crevices, while moving into littoral zones, and martins and swallows moving onto
puffins excavate burrows in the turf above sea cliffs in many cold exposed land areas to exploit the copious insect life. Most of the
maritime areas of the northern hemisphere. Even the largest terres- summer tundra and taiga fauna retreats to more temperate areas
trial animal found at the poles, the polar bear, may dig temporary for the winter months (Fig. 16.39). Some then show quite profound
snow dens in the harshest periods of the winter, with suckling changes of lifestyle; for example, the knot (Calidris canutus)
females spending many months in deep snow dens. switches from being a rufous-feathered, arthropod-eating land bird
in summer in the high Arctic tundra where it breeds, to being a gray-
Polar and tundra endotherms also use basking in association feathered, mollusc-eating temperate shorebird in the nonbreeding
with microclimatic variation, which may have little effect on their winter season. But some birds may avoid this need for a changed
core temperatures but will certainly help to maintain peripheral lifestyle by moving to the opposite hemisphere to enjoy another
temperatures and thus reduce the overall cost of thermoregulation. “summer”. At the extreme, the Arctic tern (Sterna paradisaea) flies
Semiaquatic animals such as penguins and seals bask extensively, from pole to pole every year, spending the northern summer in
to assist in the replacement of heat lost during dives; they may rest

EXTREME TERRESTRIAL HABITATS 657

Greenland or Norway and the southern summer around the shores penguins, in the face of horrendous wind-chill factors in the Antarctic
of Antarctica. winter, may be very limited. But penguins such as the emperor
penguin, Aptenodytes forsteri, and the king penguin, A. patagonica,
Migration may have multiple functions and advantages, and may have the additional advantage of large size and compact shape, lack-
be triggered by multiple cues, but it nearly always results in taking ing protruding “eartufts” and tails. Emperor males may spend
the animals to more equable thermal environments. However, the winter in the Antarctic interior incubating eggs, and fasting for
migrations in the endothermic birds are probably less to do with up to 115 days, when they certainly do gain thermal benefit from
avoiding very low temperatures and rather more to do with leaving huddling. At moderately cold temperatures the emperor penguins
areas where foraging will become unprofitable due to the imminent form fairly loose semicircular huddles, all with their backs to the
snow cover. The same can be said of the large mammals, whose wind. When temperatures drop to the typical −50°C of an Antarctic
lichen food would be inaccessible under a thick snow cover. In winter, with wind speeds over 160 km h−1 (100 mph), the birds
semiterrestrial mammals such as elephant seals (Mirounga leonina), form much denser tight huddles of several thousand individuals,
the situation may be rather different in that migration by swimming giving a biomass of perhaps 100 tonnes. Most of each bird’s surface
may be unrelated to food but necessitated by the requirements is then in contact with other penguins rather than with the cold air,
of breathing through ice holes, so that the seals move north from reducing weight loss per individual (from metabolism of stored fat)
Antarctica to areas where the ice is thin enough to maintain such a by 50% relative to a nonhuddling penguin, and saving as much as
hole; but again temperature itself is not the main problem. It is 80% of the heat loss that would occur from one bird alone. There is a
normally only in small birds and mammals that cold alone would be 25% reduction in metabolic rate, perhaps in part because the birds
likely to be lethal. sleep for long periods.

Migration may be set in train by temperature cues in a few cases, Polar mammals such as seals and walruses exhibit a less dramatic
but is probably more commonly brought about by changing photo- but also thermally effective huddling when hauled out on beaches in
period or by food supply. In most cases, the start of migration is cold weather. In many species, individuals that get too cold on land
inevitably preceded by a period of laying down energy stores as fat, will return to the sea at −1.86°C to “warm up”. However, there are
to fuel the journey. a few species of pinniped, such as elephant seals, that have molt
periods when they have to remain out of water and fairly immobile
Reproduction and life-cycle adjustment for several weeks. In colder periods, these seals will huddle together
as pods of up to 30 individuals, staying warm enough to melt sur-
Endotherms that migrate into high latitudes for the summer com- rounding snow.
monly breed there, exploiting the transiently highly productive
ecosystem. This exposure to prolonged summer day lengths neces- Burrowing combined with huddling may give energetic benefits
sitates a “resetting” of the response to photoperiod, to insure that in cold climates, but it may be effective at least as much due to the
gonadal development is initiated at the correct time, avoiding an local heating of the burrow that a huddle produces, as to the reduced
inappropriately early stimulation of the reproductive system and surface area of each participating individual. For example, in short-
associated behavioral repertoires. Primarily, the relation between tailed voles (Microtus agrestis) the local heating effect is estimated as
day length and gonadotropin secretion must be readjusted. The 55% of the total energy saving.
effect of decreased sensitivity to photoperiod and hence a shorter
reproductive cycle can be seen in birds that have been introduced to Insulation
new latitudes, and in species such as the house sparrow, with a wide
latitudinal distribution, where the period of active spermatogenesis When active (i.e. in less cold periods) the regulation of Tb in cold-
is shortened by about 2 days per degree of latitude the further north climate endotherms is largely at the heat loss end. The larger polar
the birds breed. mammals show an obvious tendency to have long, fine, and densely
packed fur, commonly 30–70 mm thick in the larger species (see
High-latitude reproduction may also require a higher degree of Fig. 8.17) and without any particular correlation with body size.
parental investment from one or both parents. In the hamster However, in small species such as lemmings or weasels the fur is
Podopus, from cold deserts, the reproductive cycle is extremely much shorter, and usually not significantly longer than in an equi-
compressed, requiring rapid milk production, which puts a real valent tropical species, although it is denser, and is spread more
strain on the mother’s water balance, and also maternal hyper- completely over the body including the head and extremities.
thermia. Species from the more arid and cold parts of the desert
show biparental care, the male’s presence increasing humidity in the Fur in boreal mammals also varies with season (Fig. 16.40). Arctic
burrow and so alleviating thermoregulatory and water balance foxes and the stoat (ermine) are also classic examples of sub-Arctic
stresses for the female. Whereas species from areas with more pre- tundra species that grow a denser and highly camouflaged winter
dictable rainfall rear the young without male assistance. coat. The advantages of increased pelt thickness are strictly size
related though: mammals of less than 1 kg show negligible improve-
Huddling and aggregation ments in winter pelt depth, whereas larger mammals such as the
red fox and the timber wolf show depth and insulation increments
Huddling in endotherms has been a favorite topic for polar almost in proportion to body size. Phenotypic acclimatory responses
researchers, as it is so spectacular in some seals and penguins. also occur; domestic dogs, cats, and rabbits may all increase their
Smaller penguins probably huddle largely to insure group cohesion coat length when kept in colder conditions. The fur of large boreal
and aid mating access in the spring. The thermal advantage for these mammals is often so effective that the complete thermal gradient

658 CHAPTER 16

1.5 predators stalking their food or prey trying to avoid being eaten. But
this explanation has recently been supplemented for polar bears by
Wolf a demonstration that the hairs are very unusual in having hollow
Wolverine shafts, which has two effects: firstly the air space reflects visible light
so that the hair appears white (while it is in fact translucent), and
1.2 secondly the hairs act like optical fibers, with total internal reflection
of shortwave UV radiation so that it passes in from the hair tips to
Insulation value (W m–2 °C–1) 0.9 Polar bear the bear’s skin, allowing radiative heating through an apparently
Wolf “reflective” pelt.
Winter coats
Polar bear Summer coats High-latitude birds such as penguins have dense, smooth layers
0.6 of feathers, extending over all their extremities, and particularly
effective in resisting ruffling and loss of insulation at high wind
Wolverine speeds. Beneath the plumage is a substantial adipose layer in winter,
providing insulation during diving and a massive food store for the
0.3 Red squirrel incubating and often nonfeeding adults. King penguin males fast
for a month or more at the start of their breeding cycle, and 93% of
0 20 40 60 their energy is then provided by the subcutaneous fat stores. The
Fur thickness (mm) insulation in penguins is so effective that they can survive in icy
water for days on end, with their feet continuously vasodilated to
Fig. 16.40 Winter coats of four species of mammals that are thicker and better maintain the thermal window effect for heat loss to prevent over-
insulating than summer coats; note that changes are greater for larger species. heating; and can breed on land in air well below freezing point while
(Adapted from Hart 1956.) maintaining high levels of REWL even when motionless, again to
avoid overheating.
Temperature
The terrestrial high-latitude mammals do not have particularly
Air: –10°C thick subcutaneous adipose layers, as these are too heavy and
cumbersome. However, aquatic and amphibious mammals such as
Fur whales, seals, and polar bears match the penguins in investing in a
Epidermis massive “blubber” layer, since for them fur would lose most of its
Dermis value through being wetted (wet fur is up to 50-fold more prone to
heat loss than dry fur). The relative utility of fur to terrestrial and
–10 0 10 20 30 40 aquatic animals is neatly demonstrated by many of the seals, where
the essentially terrestrial pups have much denser fur than the prim-
Temperature (°C) arily aquatic blubber-bearing adults. Baby seals have similar prob-
lems to penguins and can die of overheating rather readily; indeed
Fig. 16.41 The temperature gradient across the surface of a high-latitude sea lions in the Galápagos have to breed in cool caves or behind
mammal; the gradient is largely across the highly effective fur, and skin surface boulders away from the sun. Some amphibious diving mammals,
temperatures are close to core temperatures. such as beavers and mink, have a pelt of dense air-trapping underfur
beneath a coarser wettable outer fur, but these animals normally
from air temperature to normal Tb is contained across the fur and only immerse themselves for short periods. Species that dive in sea
skin (Fig. 16.41). The polar bear is something of an exception in water rather than fresh water, such as the sea otter (Enhydra lutra),
having coarse fur, probably because it frequently dives in the water have an extra problem of salt crystals forming in the pelt, which
between ice floes and must shake water quickly out of the fur again compromises its insulating role both on land and on return to the
when it surfaces. There is an apparent paradox in animal coloration water. These species spend unusually large proportions of their day
here, in that the polar bear and many other polar animals are white, in grooming the fur to remove the salt.
when black fur would appear to be beneficial in absorbing max-
imum solar radiation. For example, the light coat of the Siberian Control of heat loss at extremities
hamster in winter has a thermal reflectance of 43% compared with
the summer coat of 18%, and for the snowshoe hare the relevant Many polar animals suffer from potentially extreme rates of heat
figures are 61% (white in winter) and 23% (brown in summer). An loss at their extremities, which usually have less dense fur to aid
obvious explanation is that white pelage makes the animals less con- maneuvrability and/or sensitivity. In seals and whales, for example,
spicuous against a bright ice or snow background, whether they are it is calculated that 10–30% of heat production in a resting animal
is lost through the flippers, fins, and flukes, rising to 70–80% during
moderate exercise. Most of these animals use countercurrents at
their extremities to prevent these losses being even higher. Seal and
dolphin flippers are among the best studied cases of this regional
heterothermy, with elaborate rete systems (see Fig. 11.42). Each
artery is surrounded by a ring of small veins, normally allowing a

Polar bird EXTREME TERRESTRIAL HABITATS 659

Air: –16°C Lemmings (45–56 g)
300
40°C
TNZ
38°C Metabolic rate (100 = basal rate) 200
24°C
15°C 100
8°C
7°C 0
Snowbuntings (33–53 g)
0–5°C
400
Polar mammal
300
TNZ

200

100

36°C Air: –31°C 0
34°C
24°C 38°C Arctic gull (1500 g)
38°C 300
20°C
TNZ
9°C 200

12°C 100

9°C 0
−40 −30 −20 −10 0 +10 +20 +30 +40
Fig. 16.42 Peripheral countercurrents producing cold extremities in polar Temperature (°C)
mammals and birds. (Adapted from Irving & Krogh 1955.)
Fig. 16.43 Metabolic rates (MR) vs. declining temperature in three polar
countercurrent exchange to reduce heat loss through the uninsu- endotherms. The thermoneutral zone (TNZ) is relatively broad, especially
lated flippers. But when the animal is overheating due to prolonged for the Arctic gull, in which MR does not increase even at –30°C.
exercise, the anatomy of the system is such that the raised blood flow (From Davenport 1992.)
and higher blood pressure cause the central artery to dilate and the
surrounding veins to collapse, bypassing the heat exchanger and warmer blood to give some protection. At very low temperatures the
making blood return from the flipper by alternative more periph- heat transfer to the tip becomes small but continuous (see Fig. 8.40).
eral veins, losing heat to the surrounding water in the process.
Control of heat production
Similar heat exchangers normally keep hot blood away from gull
and penguin feet, from caribou noses and hooves, from beaver tails, Some high-latitude animals have higher basal metabolic rates
and probably even from the small ears of many polar mammals (BMRs) than predicted from the simple allometric equation (see
(Fig. 16.42). Since so many of these animals are standing on or swim- Chapter 3). In rodents such as lemmings it is 200–240% greater
ming in ice-cold environments, they particularly need to insure that than predicted. Metabolic rate can also be modified in many cold-
“frostbite” (cold-induced tissue damage) does not set in, so they adapted animals if food supplies permit. But note that, on the
must also supply the peripheral tissues with occasional pulses of whole, metabolism is less sensitive to temperature than in tropical
animals (Fig. 16.43). Polar animals have a much broader zone of
environmental temperature where they keep “ticking over” at much
the same rate regardless of ambient temperature (i.e. a broader
thermoneutral zone).

Hypothermia and torpor

Hypothermia involves an adaptive decline in core Tb, to a new value
that may be just a few degrees below normal (perhaps 30–35°C) or

660 CHAPTER 16

may be very low indeed, often below 10°C and within 1 or 2°C of Ta. 40
Slight reductions in Tb are best described just as mild hypothermia;
many birds and mammals use this in cold spells, but these animals Brain temperature, Tbrain (°C) 35
can normally become active again more or less instantaneously. The
term torpor is generally used for the phenomenon of a relatively 30
deep hypothermia involving a pronounced naturally occurring
decline in Tb where metabolic rate, respiration, and circulation are 25
strongly depressed. Its occurrence in birds and mammals was out-
lined in Chapter 8. Torpor requires the specific and energetically 24:00 24:00 24:00 24:00 24:00 24:00
expensive phenomenon of arousal to permit subsequent activity.
Time of day
Remember that “hibernation” is a much looser term, sometimes
thought of as synonymous with prolonged and profound torpor Fig. 16.44 The onset of torpor in a ground squirrel, with progressive
but widely misused in relation to such animals as badgers and bears,
both of which sleep for long periods in the winter but readily lowering of brain temperature (Tbrain) on successive nights. (Adapted from
can and do become active when hungry; the descriptive terms Strumwasser 1960.)
“winter sleep” or “carnivore lethargy” are often preferred in modern
literature. Brown bears (Ursus arctos arctos), for example, show of key glycolytic enzymes, especially pyruvate dehydrogenase
“hibernation” at only 4 –5°C below normal Tb, with very minor (although some of the mitochondrial enzymes are surprisingly
modifications to circulatory pattern and a slightly increased red upregulated in torpor, perhaps to minimize damage to the electron
blood cell count, probably triggered by a fall decrease in production transport chain during cold exposure). Many enzymes also become
of thyroid hormones. relatively temperature insensitive, and levels of phosphagens are
decreased. As a result, for example, the oxygen consumption of a
Torpor is not especially common in polar or tundra mammals, torpid bat is only 2.5% that of the active rate (Fig. 16.45), so that its
because rates of heat loss are too high for it to be sustainable at all, fat reserves will last 40 times longer than “normal” under cold con-
the habitats being too unproductive to allow adequate accumula- ditions. In at least some torpid mammals the degree of saturation of
tions of fat reserves. Polar species that do exhibit torpor, such as the the dietary fats affects torpor, with an unsaturated diet giving lower
Arctic ground squirrel (Spermophilus parryi), use it for only brief minimum Tb and longer torpor bouts, possibly via interactions with
periods. It is the small eutherian mammals of the boreal forests that the energy-regulating protein leptin. But this enhanced torpor is at
yield the best examples of prolonged deep torpor. the expense of greater lipid peroxidation during the torpid period.
In ground squirrels the intake of polyunsaturated fatty acids such
Torpor normally has three phases: that is to say, the rapid entry as linoleic and linolenic acids is therefore reduced during the fall
phase and the rather slower arousal phase can be physiologically months.
distinguished from the middle period of relatively steady, low
metabolic rate, when the metabolic rate is much reduced, represent- In full torpor, ventilation may be as low as 1–2 breaths min−1 in a
ing a very large energy saving. In these boreal mammals there is no small mammal, with periods of total apnoea of up to 5 min. Torpid
single trigger for going into a torpid hypothermic state; its onset animals appear unresponsive and uncoordinated, and indeed their
may vary with food supply and with the imposed ambient tem- sensory apparatus may deteriorate. In the Siberian ground squirrel
perature regime, although where there is a yearly cycle the onset of (Citellus undulatus) the taste bud cells have much reduced
torpor is generally regulated in part through photoperiodic changes ribosome, endoplasmic reticulum, and Golgi contents, indicating
acting via the endocrine system. The onset of torpor may be quite reduced protein synthesis and reduced sensory function during
gradual, and it largely results from failure to increase metabolic torpor. However, torpid animals still have some functioning neural
rate as Ta declines, with ventilation slowing rather than increasing. control of their own condition. If the Tb is in danger of dropping
This leads to an inevitable decrease in Tb and a further decrease in too low, with the animal approaching freezing, there may be spon-
metabolism, so that the animal slides rather gently, often over 8– taneous arousal or a gradual increase in heat production to keep the
24 h, into a torpid state without initiating any special effects such as body at 4–5°C without actually initiating expensive full warm-up.
increased conductance. Entry into this state sometimes involves a This is reflected in a rise in oxygen consumption as the air temper-
short series of transient drops in Tb (Fig. 16.44), with “test runs”, ature falls too low, and again indicates that the torpid animals are
followed by reinstatement of regulation, then a single smooth rapid not entirely going over to ectotherm-like thermal biology.
drop to the new low level during which thermoregulation is tem-
porarily abandoned and the body cools largely passively. For a bird Arousal from torpor may occur quite rapidly (1–6 h) relative to
or mammal of about 2 g, the torpid body temperature of 15°C the process of entering torpor. Arousal is also very size dependent
would be reached in only about 40 min, whereas for a 100 kg bear to (see Table 16.5). However, the arousal rate also inevitably depends
become fully torpid would take a week (Table 16.5). Simple calcula- on the starting point of Tb, since metabolic rate and temperature
tions nevertheless show that for any endotherm, despite the rapid are so closely related. In fact at a very low body temperature it is
rate of warm-up required for arousal and its cost in energy and food, impossible for chilled tissues to use oxygen rapidly and metabolic
even short periods of torpor are energetically worthwhile. rate may not be able to get high enough to raise Tb at all. In other

In the fully torpid state, the metabolic rate may be only 2–20% of its
normal resting value, and it is primarily body fat that is catabolized.
Metabolism is suppressed mainly by a reversible phosphorylation

EXTREME TERRESTRIAL HABITATS 661

Table 16.5 Time to enter and arouse from torpor for animals of different body Body temperature (°C) 40
mass. Calculated from allometric equations, for cooling and arousing at 15°C, 30
body temperature (Tb) changing from 17 to 37°C. 20
10
Species Body mass Entry time Arousal time 0

Shrew 2g 35 min 13 min Oxygen uptake (ml O2 h−1) 300
Hummingbird 4g 59 min 17 min
Honey possum 10 g 80 min 24 min Uptake by whole animal
Poorwill 40 g 224 min 41 min 200
Nightjar 86 g 350 min 55 min
Vulture 230 g 39 h 3.2 h
Echidna 3.5 kg 27 h 3.8 h
Marmot 4.0 kg 29 h 4.0 h
Badger 9.0 kg 45 h 5.4 h
Bear 80 kg 138 h 12.3 h

100 25.4%
0
words, for each size of animal there is a theoretical body temper- 23% 10% Uptake by brown
ature threshold below which it cannot fall or arousal becomes bio- adipose tissue
chemically impossible. Each species also in practice has a minimum 30
temperature from which it will initiate arousal, known as the crit- Time (min) 12.6%
ical arousal temperature, and this parameter seems relatively unre-
lated to body size or to phylogeny, perhaps reflecting natural habitat 60
temperatures (e.g. it is 2°C for the boreal pocket mouse Perognathus
longimembris, but as high as 20°C for the pygmy mouse Baiomys tay- Fig. 16.45 Temperature and oxygen consumption in a bat during arousal from
lori). It may also be linked to habitat humidities, since progressive torpor, showing that brown adipose tissue (BAT) metabolism is important but
desiccation may be a real problem for small hibernating mammals forms only part of the whole thermogenic response. (From Davenport 1992;
such as the little brown bat, where EWL during torpor would exceed adapted from Jansky 1973.)
metabolic water production at any humidity less than 99.3% RH.
Winter MR as % of summer MR
Arousal in most boreal mammals is a two-stage process, triggered
by day length and/or rising temperature. At first it is not accom- 100 Fur Hibernation Winter
panied by obvious shivering or muscular activity, because a large 75 insulation weight loss
part of the initial thermogenesis in mammals is achieved not by the (%) 50
muscles but by nonshivering thermogenesis (NST; see Chapter 8) 25 Conductance
in the specific tissue known as brown fat or brown adipose tissue
(BAT). The BAT where NST occurs is found particularly around the Torpor
neck and shoulder areas of torpid mammals (and of many newborn
mammals too, where it may be up to 5% of the birthweight), 0 Small mammals
although it is absent in birds. Its activation results in a very rapid Large
warming of the thoracic and head area, including the heart, spine,
and brain. Rectal temperature lags many minutes behind, indicating mammals
active control of blood distribution during arousal. Tracer studies
show a high blood flow to the heart, to the brown fat itself, and Fig. 16.46 A comparison of the seasonal thermal strategies of large and small
then to skeletal muscles, so that the key organs can be supplied mammals; large species mainly respond to winter with improved insulation,
with oxygenated blood. Only then are corticosteroids and insulin while small mammals use either prolonged torpor (hibernation) or a mixture
released into the blood so that the muscles can initiate shivering of weight loss, improved insulation, and short periods of torpor. MR, metabolic
thermogenesis, to give the second phase of speeded up arousal. Thus rate. (Adapted from Heldmaier et al. 1989.)
in arousing hedgehogs blood insulin secretion does not begin until
Tb has risen to about 25°C, showing the importance of NST in the and a much reduced degree (length and/or depth) of torpor. The
early warming stage. Indeed, NST accounts for about 40% of the winter metabolic rate of these species is about 30–40% of that in
heat needed for full arousal in hamsters, and somewhat less in bats summer, compared with a drop to 15–20% of summer levels in
(Fig. 16.45). small mammals with deep prolonged torpor.

Figure 16.46 summarizes the role of reduced winter metabolism Coping with freezing
and torpor in mammals of different sizes. In large species seasonal Because of their endothermic and thermoregulatory abilities, most
acclimation (with the metabolic rate reduced to about 50% of sum-
mer levels) is largely achieved by extra fur insulation and torpidity is
avoided. In smaller mammals, there may be prolonged deep torpor
in some cases, but in other species winter activity is maintained by a
combination of weight reduction, improved thermal conductance,

662 CHAPTER 16

of the “endurer” animals are not required to cope with freezing and 16.3.4 Anthropogenic effects in the cold biomes
cannot do so if very low temperatures are forced upon them in labor-
atory studies. However, there is at least one endotherm, the Arctic The low overall productivity in boreal zones makes the plants, and
ground squirrel, mentioned above as a true polar user of torpor, that hence the communities as a whole, particularly susceptible to human
has the ability to supercool to −2.9°C to avoid freezing. interference. Humans have occupied the Arctic tundra since at least
the Neolithic, but had little impact before the last century except
Food supplies in reducing some populations of vertebrates through whaling,
hunting, and fur-trapping activities.
As we saw for ectotherms, foodstuffs may pose a problem. Many
tundra and taiga species that do not migrate are food hoarders, hid- In the last 40 or so years, however, exploration and the accom-
ing caches of seeds or nuts for future use, although they normally panying exploitation have boomed, with oil, gas, and minerals
combine this with periods of torpor. Herbivores tend to face rather much sought after and with pipelines, roads, and railways all invad-
nutrient-poor and high-fiber diets, and gut mass may be larger than ing the landscape. The problem is that localized damage to these
normal and may be subject to acclimation, since it has been shown environments is only very slowly repaired by regenerative growth,
to increase markedly as a proportion of body mass in lemmings and soil turnover is even slower, so that we can still see extensive
fed on low-quality high-fiber diets. Polar mammals and birds that surface damage from the early gas and oil pipelines installed across
are herbivorous show more distinct plant preferences than related Alaska and Siberia up to 40 years ago, with damage accentuated
temperate species (e.g. willow ptarmigans select willow, rock by activities causing localized scree flows and the creation of deep
ptarmigans select birch). gullies. Such lines may seriously interrupt animal migrations.

Permanent active residents such as polar bears, penguins, and Global warming also poses particular problems for high-latitude
pinnipeds tend to be carnivores, or more especially piscivores; fish systems. Most of the climate models predict substantially faster and
and other large marine fauna are the only rich dietary items avail- greater changes in temperature at the poles, commonly as much as
able year-round that are not themselves frozen. Polar mammals 6–12°C within the next century, leading to warmer polar winters.
have the additional problem of providing adequate nutrition to An early proposal that this might lead to more snowfall and hence a
their offspring, often in the depths of winter. It is no coincidence thicker, more extensive area of snow and ice field, with greater
that cetacean and pinniped milks are unusually rich in fats and pro- albedo and greater reflection of radiation, has not been upheld by
teins, and polar bears too produce a milk richer than that of other the evidence. There is now extensive documentation of the thinning
Carnivora (see Table 15.13). Hence Weddell seal pups, receiving and break-up of ice sheets. In Antarctica several ice shelves have
milk with 60% fat content, can double their weight in the first been monitored carefully and show marked disintegration and
10 days after birth. retreat of the ice front (Fig. 16.47), while in Greenland ice thinning
has also been reported. Since many polar invertebrates appear to

69°00′S Hariot Glacier
1989

1966

69°15′S 1974
1989

MBt.alfour Fleming Glacier

PrGolsapceiecrt 0 10 km Fig. 16.47 Documented ice-sheet thinning in part of
67°00′W Antarctica since 1966. (Reprinted from Nature 350,
69°30′S 68°00′W Doake, C.S.M. & Vaughan, D.G., copyright 1991,
with permission from Macmillan Magazines
Limited.)

EXTREME TERRESTRIAL HABITATS 663

have upper lethal temperatures rather close to their current max- 16.4 High-altitude habitats
imum microclimate temperatures, there may be casualties from
overheating. Life at altitude in many ways presents a special case of low-
temperature habitat, where height above sea level parallels the
Ozone depletion is currently a phenomenon very much centered effects of latitudinal distance from the equator. However, there are
on the polar zones, with polar stratospheric clouds implicated in the also additional problems relating to temperature, water availability,
reactions with atmospheric halogens (chlorine and bromine) that respiration, and pressure, so these habitats are given a section of
lead to ozone destruction. The seasonal Antarctic ozone “hole” is their own here.
still expanding every year, and some annual thinning in the Arctic is
also documented. The ozone-depleted air has on occasions moved 16.4.1 Montane habitats
out to lie over the southern tips of Australia and South America, and
routinely affects the Antarctic continent and fringes. The expected Occurrence
effects of increased frequencies of skin cancers, and of cataracts,
will certainly be most likely in the polar mammals and birds, with Mountains occur in all continents (Fig. 16.48), and in a wide range
penguins perhaps most profoundly at risk. of forms, both as long mountain chains and as relatively isolated
peaks. The process of orogenesis (mountain building) is primarily
All of these problems can be accentuated by increased predation related to plate tectonic movements, with the land mass rising up
risks for weakened animals faced by introduced predators; feral where two plates collide and forming a mountain chain along the
mice in the sub-Antarctic are already a problem for insects. Hence perimeter of one plate. This may be either at the edge of a continent
in some ways these cold terrestrial environments are every bit as where a submerged plate undergoes subduction below a land mass,
“fragile” as the tropical forests and temperate wetlands that are as with the Andes in South America, or it may be in the center of a
more common areas of concern, but as yet they have received much continent formed from two land masses abutting on each other, as
less research effort. with the Ural mountains between Europe and Asia, or the Himalayas
between Asia and India. However, every mountain range is unique,
Fig. 16.48 The world’s mountain ranges. since the processes underlying orogenesis are very complex.

Tropic of Cancer

Equator

Tropic of
Capricorn

664 CHAPTER 16

Table 16.6 Characteristics of mountain ranges. ample is the isolated peak of Mt Kilimanjaro in Tanzania, almost on
the equator yet with snow and glaciers at the summit all year round
Mountain range Highest peak Latitude even in blazing midday sunshine. Other tropical mountain ranges
(m (ft)) 45 – 47°N may be extremely arid, with the northern Andes having exception-
35°S–7°N ally low-humidity air since the precipitation has been shed from air
Alps Blanc rising up the west-facing slopes, giving a rain-shadow effect. These
Andes 4807 (15,771) 34–42°N dry mountain peaks are again always profoundly cold by night;
Antarctica Ojos del Salado 30 – 33°N many animals living there must show expanded thermal tolerances.
Appalachians 7034 (23,241) 28 –38°S In more temperate latitudes, mountain ranges may show a lesser
Atlas Vinson Massif 42– 43°N diurnal temperature range but a very drastic seasonal variation, so
Australian Alps/ 5140 (16,863) 5 –15°N that temperate mountain ranges such as the Alps and Rockies have
Mitchell 28 –35°N an extremely variable snowline.
Great Dividing Range 2037 (6684) 30– 42°N
Caucasians Toubkal 5°S–3°N Aside from elevation, mountains also may pose challenges in
Ethiopian plateau 4165 (13,664) 42°N terms of geological instability, with periodic fracturing, quaking, or
Himalayas Kosciusko 35 – 62°N volcanic emissions. While potentially lethal for local populations in
Iran/Turkish plateau 2230 (7316) 35– 40°N the short term, such effects may in the longer run produce increased
Kenyan plateau Elbrus 36 –39°N diversity (by separating subpopulations on isolated peaks or plateaus,
Pyrenees 5642 (18,510) 43– 45°S leading to potential allopatric speciation), or in the case of vulcan-
Rockies Ras Dashen 53 – 68°N ism to increased local soil fertility and biotic productivity.
Sierra Madre 4620 (15,157)
Sierra Nevada Everest Montane vegetation
Southern Alps (NZ) 8848 (29,028)
Urals Ararat (Büyük Agri) Vegetational patterns at altitude parallel those with latitude, but
5165 (16,945) may show the same sequences compressed into a much smaller
Kilimanjaro linear dimension (Fig. 16.49a). In ascending from the lower slopes
5895 (19,340) one may pass from deciduous forest and chaparral or grassland into
Pico de Aneto coniferous forest, above which is a distinct treeline; above that again
3404 (11,168) there may be regions of shrubby vegetation or ericaceous plants,
Elbert sages, and junipers, with some thinning grass, then bare rock with
4399 (14,431) lichens. The snowline in winter descends downwards through these
Citlaltepetl successive tiers of vegetation.
5699 (18,697)
Whitney But the actual vegetation on any particular mountain range varies
4418 (14,495) with continent and latitude (Fig. 16.49b), so that it is very hard to
Cook generalize beyond this. In addition, mountain ranges have often
3764 (12,346) acted as refugia and as centers of isolation at different times in their
Narodnaya history, so that many of them have unique combinations of flora.
1894 (6213)
Montane fauna
Furthermore, every existing mountain range is of a different age,
some still rising and forming, others the result of hundreds of The upper lichen zones of mountains have an invertebrate fauna
millions of years of fracturing and erosion since they first formed, largely restricted to the soil layers and including springtails, mites,
thus giving a vast range of different types of formations. Some key and nematodes. Spiders, particularly from the genus Pardosa, occur
characteristics of major mountain ranges are given in Table 16.6. in most mountain ranges, subsisting partly on windblown insect
fauna such as aphids; some insects also occur as residents (up to
Being areas of marked recent geological upheaval, younger about 6000 m in the Himalayas). In these upper rocky areas, where
montane areas also tend to suffer from other geological phenomena there is patchy vegetation there is also a range of relatively large and
such as earthquakes and vulcanism. The Andes, for example, are quite specialized vertebrates, particularly camelids, with the bac-
part of the Pacific “ring of fire”, with numerous active volcanoes. trian camel occurring in the Himalayas, the dromedary in central
Mountainous areas may also be sufficiently elevated to be frozen, Asia, and the llama, alpaca, guanaco, and vicuña in South American
thus giving rise to glaciers, and the scouring effects of recent or mountain ranges. There are also various sheep and goats, including
current glaciations are often very obvious. the alpine ibex, mouflon, and chamoix, the Himalayan goral, tahr,
and markhor, and the Rocky Mountain bighorn. Amongst the crags
From a biological point of view, several of these geological factors there may be resident raptorial birds (eagles, etc.) and a range of
have an important impact. Elevation in itself is perhaps the most passing migrant birds. Just a little lower down, where the soil is
obvious, with effects on temperature, pressure, and oxygen avail- deeper and vegetation more prolific, there is a wide diversity of
ability. In mountain ranges daily average temperatures are reduced burrowing rodents, providing prey for the raptors. Where there are
by about 1°C for every 150 m of altitude. This effect is roughly sim- lakes within the mountain ranges, particularly in the long chain of
ilar at all latitudes, so that even tropical mountain ranges sitting
astride the equator can be snow-covered (see Plate 9f, between
pp. 386 and 387). They are therefore profoundly cold at night even
though highly irradiated by day, and these diurnal cycles of extreme
heat and cold are accentuated during the dry season. A classic ex-

Tropical Temperate Boreal

6000 Altitude (m) Nival Nival Nival
5000 Alpine Alpine
4000 Afro-alpine belt Subalpine Subalpine
3000 Montane
2000 Ericaceous belt East
1000 Bamboo belt Submontane Moss/lichen
Pine
0 Montane Aspen
(a) forest belt Juniper
Natural grassland Sage
and cultivated zone

Altitude (m) West Alpine
4000 Pine forest
Pine and hemlock
3500 Cedar and fir forest
Transition brush
3000 Oak forest
Pine Chaparral

Altitude (m) 2500 Tree-groundsel
Fir Rock hyrax
Giant heath Fig. 16.49 Patterns of floral change with altitude in
2000 Leopard different mountain ranges. (a) Schematic zonation.
Bamboo (b) Patterns in the Sierra Nevada (above) and in
1500 East Africa (below).
Cedar Duiker
Tree fern
1000 Forest buffalo
Oak Acacia tree

500 Elephant

0

Alpine
3650

Heath
3000

Bamboo

2275
Rain forest

1650
Savanna

(b)

666 CHAPTER 16

the Andes, quite a range of waterfowl also occurs, especially geese Table 16.7 Altitudinal limits for various vertebrates.
and coots but also including flamingos.
Taxon Altitude (m) Location
Further down the mountains faunal diversity inevitably increases
and largely parallels the fauna of the equivalent latitudinal belt, with Fish 2800 Alps
a particularly strong representation of insects, such as grasshoppers, Trout 3800 Andes
and some pollinators, such as bees, butterflies, and flies. Amphibians Trout 4700 Asia
and reptiles become rather common, each species often having a Nemachilus
quite substantial altitudinal range. Rodents are again common, as 3000 Alps
are various large deer and antelope (elk, pronghorn, taruga, klip- Amphibians 4500 Andes
springer, etc.) in dense bush and forests, and very bulky animals Salamander 5000 Himalayas
such as the yak in plateau areas of Asia. Thus many taxa of animals Eleutherodactylus
have surprisingly high altitudinal limits (Table 16.7). Toad 3400 Rockies
4000 Kilimanjaro
To make the point that every mountain range is different, an Reptiles 4900 Andes
example of the faunal distribution up a tropical mountain is shown Lizard 5500 Himalayas
in Fig. 16.49b. Here hyrax are a speciality in the upper slopes, with Skink
leopards making homes in isolated crags and only descending at Iguanid 4000 – 6500 Rockies
night to feed; lower down the typical African bush fauna appears. Lizard 5000 – 6000 Himalayas
8800 + Himalayas
It is generally found that species diversity decreases with altitude, Birds
and that species ranges increase with altitude. The habitats thus Several 4000 Rockies
become dominated by relatively few, relatively specialist, species Lammergeier 4500 + Andes, Himalayas
extending over broad elevational bands. An example of elevation Barheaded goose 4800 –5400 Andes
ranges for bats in the Andes is shown in Fig. 16.50. 5000 Andes
Mammals 5800 Asia
16.4.2 Thermal problems Deer mouse 6000 Andes
Human (permanent)
The main environmental effect of altitude, as far as animals are con- Llama, alpaca
cerned, is the declining temperature. However, on most mountains Chinchilla
there is in addition a particularly stark contrast between conditions Yak
in sun (since the radiative load is very high) and in the shade, and Taruca deer
often a stark contrast between day and night. Thermal problems can
also be greatly magnified by high winds. cannot empty their guts and are bound to be full of INAs, so that
they are particularly vulnerable to bodily freezing.
Animals in mountain ranges may therefore have to exhibit a high
thermal tolerance, to avoid freezing by night, and to cope with over- Heliothermy: basking, sun–shade shuttling, and color
heating and desiccation by day. In tropical mountains the change
between the two conditions may be extremely sudden at sunrise and Amongst ectotherms, the insects, lizards, and snakes use basking
sunset, with no time to “prepare” on a daily basis. To make matters and shuttling heliothermy to a marked degree. There have been
worse, since smaller animals are active and feeding by day they classic studies on an Andean lizard species, Liolaemus multiformis,
living at 4000 m, which emerges from its burrow at dawn (0700 h)
with an air temperature of only −5°C and basks on heaps of vegeta-
tion that insulate it from the ice, warming up to a Tb of 35°C within

3500
3000

Elevational range (m) 2500
2000

1500

1000

500

Fig. 16.50 Elevational ranges of 129 bat species in the

0 Andes; species that occur at a higher mean altitude
10 20 30 40 50 60 70 80 90 100 110 120 130 (solid circle) also have substantially greater

Bat species altitudinal ranges. (From Patterson et al. 1996.)

EXTREME TERRESTRIAL HABITATS 667

Temperature (°C) 40 Cloacal temperature Use of vegetation and microclimate

30 Because of the combination of freezing and desiccation dangers
referred to above, many montane animals from the tropics cannot
20 be either particularly cold-hardy or particularly desiccation resist-
Air temperature ant, and there is a strong tendency to use behavioral rather than
physiological techniques to survive. Hiding in crevices and under
10 rocks, and seeking shelter within vegetation, are almost ubiquitous
strategies amongst invertebrates. Thus, for example, insects
0 sampled from above 4000 m on Mt Kenya showed almost no special
adaptations to low temperature, but instead sheltered in the rosettes
07:00 08:00 09:00 10:00 11:00 of large Senecio plants and in other dry flower heads. The predomin-
Time of day ance of large rosette plants in these habitats may be particularly
important in providing stable microclimates amongst the bulk of
Fig. 16.51 Basking in a Peruvian mountain lizard allows cloacal temperature to decaying older leaves.
rise sharply after dawn and then be maintained at a steady 35–38°C, well above
air temperature. (Adapted from Pearson 1954.) Certain insects are particularly adept at exploiting the sharp
temperature gradients around mountain vegetation. One example
2 h (Fig. 16.51). However, life at altitude complicates the issue of is the checkerspot butterfly, Euphydryas gillettii, in the mountains
thermal balance and patterns are not straightforward. Within the of Wyoming, USA, which preferentially lays its eggs on the
genus Liolaemus there is no clear association between thermal toler- southeast-facing leaves of certain honeysuckles, to gain maximum
ance and elevation, because varying body masses affect thermal warming from the early morning sun. Eggs laid in such sites mature
inertia; with mass factored out, high-elevation species heat more more quickly than those from other zones of the plant, and so are
slowly. High-altitude Andean frogs have a broader thermal toler- more likely to produce caterpillars that will have fed enough to
ance than congeners from neighboring lowlands, and greater survive when the early montane winter sets in.
aerobic metabolic scopes at low temperatures. The lizard Sceloporus
variabilis achieves a mean Tb of only 28.9°C at 1000 m in Mexico, Microhabitat selection certainly also matters for vertebrates, but
whereas the same species at 45 m can achieve 32.4°C, despite the two the physical nature of the terrain at high elevations may limit the
populations having similar metabolic rates. Another closely related options for these larger animals. For example, the microclimate
lizard, S. jarrovii, is winter-active in mountains, and it can darken choices are relatively similar for the Andean and lowland frogs men-
rapidly when cold, with the melanophores directly responding to tioned above, although the times of day (and air temperatures) at
melanophore-stimulating hormone. Skin samples show a differing which each kind of habitat is sought out do vary markedly.
dose–response curve to this hormone at different temperatures, and
at 35°C the darkening response is dramatically reduced compared Burrowing and huddling
with lower temperatures. Pigment cell sensitivity thus appears to
be acclimated at the cellular level, to allow appropriate thermo- Burrowing in general serves as a way of avoiding very cold temper-
regulatory responses. atures for montane animals. The Andean lizard Liolaemus spends
on average 82% of its time in deep burrows, with 15% basking and
Postural thermoregulation is also very obvious in montane fauna. crouching on warm surfaces and just 2–3% actively foraging or
Basking and ground-hugging is common in ectothermic montane interacting with other animals. Deer mice in Wyoming mountains
butterflies such as Colias species, and crouching postures side-on to similarly use burrows to avoid freezing; with night temperatures of
the sun are conspicuous in montane grasshoppers such as Melanoplus −15°C, the burrow never falls below 0°C. Note that this deer mouse
sanguinipes, which can raise Tb up to 20°C above ambient. These is the same species that can be found in the Nevada desert further
high-altitude grasshoppers often exhibit higher resting metabolic south in the USA, where, as we saw, the burrows have the opposite
rates than their low-altitude congeners, which may compensate role of providing a buffer against overheating.
for lower temperatures and shorter seasons. Amongst endotherms,
the Andean guanacos bask with their flanks and axillary regions Montane animals also frequently combine the benefits of bur-
exposed to the sun, but adopt curled up postures where these rows and aggregations. The alpine marmot (Marmota marmota)
“thermal windows” are shut off towards sunset, achieving a max- overwinters in large underground nests, containing 5–8 animals of
imum 22% reduction in thermal window heat loss. They then bed the same family (whereas its close relative the woodchuck does not
down in groups, with their hindquarters into the wind, these postural live at altitude, and hibernates singly). The alpine marmot under-
changes together giving a 67% energy saving. goes torpor with a Tb of only 7– 8°C for periods of about 2 weeks,
interspersed with short arousals when Tb rises to normal levels for a
For many montane animals there are indications that the day or so. Within the nest all the individuals are synchronized, and
metabolic rate rises and the critical thermal maximum decreases, huddling occurs both during torpor and during the high Tb phases.
inter- and intraspecifically, with increasing altitude. When one individual begins to arouse, some of its body heat is
transferred to the other marmots, helping them to warm passively.
The first one to be fully aroused also grooms its nest mates and
covers them with extra nest material to aid their warming. The
marmot burrows are commonly around 12°C internally in the fall,

668 CHAPTER 16

but this has dropped close to 0°C by early spring. When burrow 0 Pelophila borealis
temperatures fall below 5°C, the marmots raise their metabolic rate –10 Calathus melanocephalus
somewhat, but because of the burrow this is only required for rather Patrobus septentrionis
less than half the total period of torpor. The more animals there are
in the burrow, the longer it takes for the burrow temperature to fall Supercooling points (°C)
to 5°C, giving a real benefit to “social hibernation”.

Even in the larger mountain mammals a gregarious habit is com-
mon, with sheep and goats living in small herds and huddling
together at night and in stormy weather.

Insulation, heat distribution, and metabolic rate –20 Snow cover

Montane mammals show some interesting adaptations of furs. The J J A S O N D J F MA M
duck-billed platypus, Ornithorhynchus anatinus, lives in mountain Month
streams in eastern Australia and may dive for prolonged periods in
water close to freezing point. It has one of the most effective fur Fig. 16.52 Seasonal variation in supercooling point in three species of alpine
insulations known, with a dense underfur and flattened guard hairs ground beetles. (From Sømme 1995.)
to trap air, combined with countercurrent heat exchangers at the
base of its tail and all four limbs. Oreamnos americanus, a wild goat other habitats, levels of protection against freezing tend to show
from the Rocky Mountains, has evolved the same strategy as we seasonality; Fig. 16.52 shows the strongly seasonal variation in
met earlier in the polar bear, with a rather coarse pelt of hollow hairs supercooling points for alpine beetles.
that appears white (and presumably it gets the same advantages).
The large camelids, deer, and antelope from mountain areas are also One of the more spectacular examples of freezing tolerance is
famous for the depth and quality of their pelage. Many are used as the New Zealand weta (Hemideina maori), a very large montane
providers of high-quality wools (e.g. chinchillas, alpaca, and cash- grasshopper that survives in the frozen state for much of the winter,
mere goats). The individual hairs may be very long, most spectacu- and which can be seen freezing and thawing on a daily basis in
larly in the wild yak where the rather coarse fur almost reaches the spring and fall. The weta may have more than 80% of its body
ground. During the short summer periods, when these animals water converted into ice, promoted by an ice-nucleating protein,
might risk overheating, blood can be shunted to the less insulated though the intracellular contents remain unfrozen through osmotic
extremities to dissipate excess heat. dehydration effects and a build-up of proline. A few cases of freeze
tolerance in species from tropical mountains have also been re-
In several invertebrates, notably insects, mass-specific metabolic corded, including beetles from Mt Kenya, Meridacris grasshoppers
rates tend to increase with elevation, and it has been argued that this from the northern Andes, and Agrotis caterpillars from Mauna Loa
is an adaptation to accelerate development in species that remain on Hawaii.
annual (see below). However, in the grasshopper genus Xanthippes,
population differences in mass explained most of the effects (high-
altitude grasshoppers were smaller), and when mass was factored
out little effect of elevation remained. In heterothermic bees Tb and
warm-up rate increase with altitude, although it is unclear whether
this results from decreased thermal conductance or higher mass-
specific heat-generation rate.

Coping with cold and freezing 16.4.3 Dehydration and water balance

Small ectotherms in mountains may have real problems with Animals suffer an increased tendency to dehydrate at altitude. At
achieving activity in continuously cold conditions. In insects this is low ambient temperatures the water vapor content of the ambient
sometimes circumvented by a degree of endothermy, as for example air is reduced, and any animal with a Tb above Ta will lose water very
in the rainbeetles (Plecoma) of the Sierra Nevada of the USA, which quickly in its warm exhaled saturated breath. Furthermore the dif-
achieve a Tb of 35°C even in air temperatures around freezing. fusion constant for all gases, including water vapor, increases with
Bumble-bees in the Himalayas and Andes achieve similar feats. altitude. Increased wind speeds may add to the dehydrating effect.
Where there is standing water or snow, larger animals, including
Many small animals from seasonal temperate mountains have most of the vertebrates, may have little problem, but small inverte-
classic physiological adaptations to achieve cold-hardiness in winter, brates are more at risk.
with both freeze tolerance and freeze intolerance exhibited. Smaller
species (mites, springtails, etc.) tend to be freeze intolerant, voiding Invertebrates from mountains may therefore have relatively high
their guts to eliminate nucleating agents and accumulating glycerol dehydration tolerance. For example, tenebrionid beetles from
or other polyols or sugars. Larger invertebrates tend to be freeze exposed habitats on the slopes of Mt Teide (Tenerife, 2000–2500 m)
tolerant, accumulating both nucleating agents and cryoprotectants, can survive at least 40 days at 5% RH, with only 15–30% weight loss,
and surviving repeated freezing of their extracellular fluids. As in matching or outdoing some more xeric lowland species for rates

EXTREME TERRESTRIAL HABITATS 669

Alpine Carabidae Table 16.8 Altitude and pressure effects in humans.

0.5 Atlas Mts lowlands — East Africa Altitude (m) Atmospheric Ambient Alveolar Alveolar
0.2 Pico del Teide East pressure
Andes Mts (kPa) P O2 P O2 P CO2
Norway (kPa) (kPa) (kPa)

Rate of weight loss (mg h–1) * Carabidae from arid 0 101 21.1 13.8 5.3
3100
4340 71 14.6 8.9 4.8
5300
Africa 5500 62 12.8 6.0 –
6200
6000 –7000 Ceiling for unacclimated humans
8500
lowlands — 8848 Highest human habitation
9200
0.1 Alpine 12,300 46 9.7 5.3 3.2
0.05 Tenebrionidae 14,460
arid 15,400 Ceiling for acclimated humans
Pico del Teide 20,000
* from Human breathing possible for a few hours

Tenebrionidae 33 6.9 4.0 1.5

30 6.3 2.8 –

19 3.9 1.1 –

Ceiling for humans with pure oxygen supply

0.02 * 12 2.4 0.1 ~0

6 1.3 0 0

0.01 50 100 500
10 Fresh weight (mg)

Fig. 16.53 Rates of water loss (cutaneous evaporative water loss, CEWL) in 16.4.4 Pressure and respiration
montane beetles compared with those from arid lowlands (measured at similar
temperature and humidity). There is a lowered evaporative water loss (EWL) in Another important effect of altitude is the change in barometric
tenebrionids from Pico del Teide (Tenerife), but for carabids (living in the litter pressure, which dramatically alters the partial pressures of gases
layer) there is little effect except in the relatively exposed Norwegian beetles. in the atmosphere. The relationship between altitude and pressure
(From Sømme 1995.) is exponential, pressure decreasing by 50% for every 5500 m of ele-
vation. Thus at the top of Mt Everest (8848 m above sea level) the
of cuticular evaporative water loss (CEWL). Likewise grasshoppers barometric pressure is only 250 Torr or 33 kPa, about one-third of
(Melanoplus) from montane populations also show lower water the sea-level value, with Po2 at 6.9 kPa.
loss rates, and the amount and melting point of cuticular lipids are
correspondingly higher. However, in groups such as carabid beetles The additional physiological problems of altitude are therefore
that normally live within the litter layer the montane species are mainly respiratory, due to low pressure and low oxygen. This is
no more desiccation resistant than similar lowland species; only a unlikely to be a significant problem for animals in high-altitude
few species that survive in rather exposed zones above the treeline ponds and streams, and indeed the amphibious African crab
in Norway have lowered CEWL values (Fig. 16.53). In addition to Potamonautes warreni shows little specialization in ponds at 1400 m
cuticular adaptations, there may be excretory adaptations to min- elevation. Nor is it a substantial problem for terrestrial arthropods
imize water loss in invertebrates. Montane tenebrionids normally using a tracheal respiratory system, which is rarely at the limits of its
have a cryptonephridial system, and the gut lumen (and therefore capacity to supply oxygen. But for vertebrates with lungs it repres-
the urine/feces) may reach 2500–2750 mOsm. However respiratory ents an additional constraint on performance, and especially for the
adaptations to reduce water loss are not clearly documented, so that maintenance of a high BMR in endotherms. Table 16.8 shows the
although Melanoplus grasshoppers use discontinuous ventilation effects of altitude on partial pressures of gases for a human.
at times, this behavior shows no good relationship with altitude or
water loss rates. For nonadapted birds and mammals, hyperventilation is the
normal response, in an attempt to maintain alveolar Po2, but arterial
For endotherms the issues of water balance are somewhat more oxygen levels inevitably decline, and for humans loss of conscious-
complicated. Many mammals are reported to have lower total body ness results at about 50% arterial oxygen concentrations, normally
water values at altitude, and in humans this effect can be marked occurring at around 7000 m above sea level. Hyperventilation also
(29 kg in Andean populations compared with 39 kg in weight- and tends to lead to reduced alveolar Po2, which in turn inhibits respira-
age-matched lowland humans). High-altitude populations can also tion for terrestrial vertebrates (see Chapter 7), giving an automatic
clear a drinking-water load much more quickly, mainly because brake on the acclimatory response. This can be partly overcome
the collecting ducts of the kidney become relatively insensitive to by excreting excess carbonate at the kidneys leading to metabolic
the hormone arginine vasopressin. It is still unclear whether other acidosis and thus an improved central chemoreceptor response
aspects of water loss rates are altered in mammals. Careful analysis to increase the respiratory rate. The need to oxygenate the tissues
of deer mice water loss rates with altitude show a clear increase, but conflicts sharply with the need for acid–base homeostasis. Inorganic
this was an indirect effect, with mass and metabolic rate as con- phosphate and 2, 3-diphosphoglycerate in the red blood cells play
founding variables. Differences in the thermal environment are some role in changing the hemoglobin affinity to assist in this
probably the main cause of higher overall water-flux rates in small balance, overriding the Bohr shift (Fig. 16.54). Nevertheless both
mammals at higher altitude. arterial blood concentrations and blood acidity are reduced, which
may lead firstly to mild cerebral edema and secondly to ever-
increasing pulmonary edoma as the pulmonary capillaries constrict
in some parts of the lung leading to increased pulmonary pressure

670 CHAPTER 16 Descent Ascent Descent

Ascent

29P50 (Torr) 20
27 DPG (µmol (gHb)−1)
25 16

(a) 12 Fig. 16.54 (a) Acclimatory changes in hemoglobin
affinity in humans at altitude (4510 m) for 5 days,
012 34 567 89 (b) 012 34 567 89 and (b) the associated change in erythrocyte
Time (days) Time (days) diphosphoglycerate (DPG) concentrations.
(Adapted from Bouverot 1985.)

and patchy leakage of fluid into the alveoli, leading to crackly animals) have high-affinity hemoglobin, albeit less spectacularly
breathing as a symptom of the “altitude sickness” experienced by than in the four montane species (llama, guanaco, alpaca, and
humans. vicuña) suggests that the latter explanation is more likely. However
a comparison of carnivores from high altitude in Peru shows P50
For resident adapted animals, the respiratory and circulatory sys- values of 31.1 Torr (puma) and 18.5 Torr (fox) compared with 36.3
tems become modified. In vertebrates this means that enhanced and 26.2 Torr, respectively, in the same genus or species from sea
lung volume, and extra pigment in the blood (increased hema- level, suggesting that in this group the change in respiratory pig-
tocrit) with high-affinity properties, are the commonest responses. ment affinity and structure occurred after invasion of the montane
Enhanced lung volume is hard to prove in endemic species, but is habitat. The same is true for geese, where the high-altitude migrators
readily seen in comparisons within species, even in humans, where (the barheaded goose in Asia and the Andean goose) have specially
high altitude natives have larger barrel-shaped chest with larger modified pigment relative to close lowland relatives. In every case,
lungs, and may also have larger hearts, allowing exertion levels that the changed affinity can be traced to just one or a few amino acid
can never be matched by incoming humans however long they stay substitutions within the protein, and for the two geese species the
and attempt to acclimate. An increased hematocrit is useful during point mutations are quite distinct, confirming their separate evolu-
acclimation, but is rare in permanent residents such as camelids, tionary origins.
since it also increases blood viscosity. High-affinity hemoglobin (at
normal concentration) is a better response in permanently resident A high-altitude rodent from China, the pika, reveals further cir-
mammals and birds, with the oxygen dissociation curve well to the culatory adaptations, having reduced pulmonary vasoconstriction
left. This is particularly apparent in camelids (Fig. 16.55); but do the responses with a larger right ventricle giving high pulmonary perfu-
camelids have this characteristic due to residence at high altitude sion; in this species again there is no increase in hematocrit. Com-
over hundreds of generations, or have they come to inhabit high parisons of the circulatory systems of high-altitude birds (Andean
altitudes because they were already endowed with suitable hemo- coots) show further circulatory changes. Capillarity is increased in
globin? The fact that the two camel species (essentially lowland muscles, and mean muscle fiber diameter is decreased. These changes
appear to be sufficient to allow regulated energy production in
Oxygen partial pressure (kPa) 16 muscles without increases in enzymatic activity, since oxidative
4 8 12 enzyme function shows no significant differences from sea-level coots.

100 Birds’ eggs also have a particular respiratory problem at altitude,
the shell needing larger than usual pores to compensate for reduced
80 rates of gas exchange and therefore incurring rapid EWL. Most
birds that nest at altitude must compensate by providing more
protected nest holes with a humid microclimate.

Saturation (%)60 16.4.5 Life cycles

40 As with polar species, montane invertebrates often have extended
Other mammals life cycles, needing two or more seasons to complete a cycle that in
Vicuña related lowland congeners would take only 1 year. Carabid beetles
from the Austrian Alps routinely take 2–3 years; even at the relat-
20 Llama ively limited heights of Snowdonia in Wales, carabids seem to be
biennial, whereas their lowland conspecifics are annual. Wolf spiders
0 20 40 60 80 100 120 of the genus Pardosa have a 2-year cycle above the timberline in
Oxygen partial pressure (mmHg) the Rockies, whereas species below the timberline always complete
the cycle in one season; the same applies for high-altitude Pardosa
Fig. 16.55 Oxygen dissociation curves and lowered P50 values in high-altitude from Norway (3 years) and from Austria (2–3 years). Similar effects
llama and vicuña compared with sea-level mammals. (Data from Hall et al. have been reported in mites, springtails, moths, and crane flies.
1936.) Diapausing stages may contribute to the lengthened cycle, and as

EXTREME TERRESTRIAL HABITATS 671

in other extreme habitats this phase is often triggered by temper- The overall pattern of life on mountain slopes is likely to change
ature rather than by photoperiod, allowing greater phenotypic markedly in response to continued global warming (Fig. 16.56). An
plasticity. However, there is also evidence that on reaching adult- analysis of likely changes in vegetation distribution on the east and
hood high-altitude populations undergo more rapid senescence. west slopes of the Cascade Range in USA (Fig. 16.56b) shows the
In Melanoplus grasshoppers montane populations aged and died eastern faces lose much of their interesting alpine upper zones and
more quickly than lowland populations when both were kept in a become dominated by sagebrush scrub, while the west loses alpine,
common equable environment, perhaps due to selection on their hemlock, and fir habitats and gains further oak savanna.
reproductive schedules.
16.5 Aerial habitats
An alternative strategy at somewhat lower elevations, or where
microclimatic variation can be exploited to speed up development, Aerial life is in some senses a special case of life at altitude, where
is to curtail the life cycle somewhat so that it can be fitted into the animal has usually generated the altitude by its own activity.
one season. A Rocky Mountain grasshopper, Aeropedellus, has one This “altitude” may be very limited in small insects, but can exceed
fewer nymphal stage than normal, and many insects at similar eleva- that of the highest mountains for some birds, who are able to fly at
tions are rather smaller as adults than in lowland populations. But heights greater than those achieved by human mountaineers using
patterns of change with altitude are not simple. In lizards, growth accessory oxygen (see Table 16.7). All of these animals may there-
rates and reproductive potentials can either increase or decrease fore have altitude-related problems as described above, relating to
with elevation, depending on rather subtle balances of behavioral temperature, water balance, pressure, and respiration; but in addi-
adjustments and local climate patterns. tion they have to solve the more mechanical problems of keeping a
low body weight and good buoyancy, of having appropriately shaped
In mammals, the most conspicuous adaptation is that of aerodynamic surfaces and, of course, of fueling. The mechanical
extremely precocial young, which on high mountain slopes can and physiological problems often become coupled, since flying
move around and look after themselves almost from the first day entails substantial power output, potentially producing unusually
after birth. Birds appear to show an alternative pattern of increased high heat loads and compounding the problems of water balance by
biparental care in montane species (linked with less sexual dimor- increasing convective and evaporative cooling and/or increasing
phism and relatively drabber males). This may be associated with metabolic water production. In flying animals, temperature, water
another problem for many high-altitude species, that of attracting a balance, and respiratory problems are particularly closely tied
mate for reproductive purposes. Data on this issue are limited, but together.
at least in Andean frogs there is evidence that the more montane
species show less energetically demanding vocal behaviors. Many organisms live continually in the air for short periods,
often in dispersive phases, and often involuntarily. A great many
16.4.6 Other problems and adaptations in mountains more use flight and other kinds of airborne locomotion in short
bursts, for prey capture, escape from predators, or competition for
A major problem in high mountain crags is that of locomotion, and acquisition of mates. Just a few insects and some birds (e.g.
and of keeping a grip and maintaining balance on unstable difficult swifts) stay aloft for extended periods, and could be said to lead truly
terrain that is often very windswept. For the large mammals that aerial lives. It is worth remembering that most animals fly; the
make a living in these habitats, some show careful slow gaits, picking majority of insects of course, but also most birds (of which there are
their way amongst rocks, while others have a bouncing jumping twice as many species as there are of mammals) and even about
locomotion achieved at amazing speeds. The latter group have one-fourth of all mammals (the bats). Remember that though flight
major adaptations, particularly of the feet, to give this sure- is energetically expensive, it is also very efficient in terms of cost per
footedness. The bighorn sheep of the Rockies have soft elastic pads unit distance traveled.
in their feet that absorb the shock of impacts and provide an effect-
ive grip on slippery rock. Flight, whether of short or long duration, needs particularly
high-energy foods such as nectar, fruit, or very good quality flesh,
Communication across craggy mountain expanses may be diffi- especially in the form of fish for the birds that spend long periods
cult, with many obstructions to long-range visual signals, so that aloft gliding and flying over the sea. Very few leaf-eating herbivores
auditory communication has become particularly common in are good fliers, since the diet is too poor and the gut needs to be too
amphibians, rodents, and the larger mammals. Honking and large. Fueling within the body has to be critically adjusted to keep
barking sounds that carry well in thinner cool air are used to com- the wing musculature adequately supplied. In insects, proline and
municate between and among the herds in larger mammals, and to lipids are used, while in vertebrate fliers glycogen stores remain the
signal danger among marmots and other rodents. primary source of blood glucose. However, small passerine migrat-
ory species have particularly high levels of plasma triglycerides, and
Some higher-altitude populations may be among the most sus- this may be an adaptive system of fuel supply.
ceptible to potential global climatic change. Most obviously, they
almost by definition occur in isolated small populations, relatively Wing muscle design also varies according to lifestyle and time
close to the edge in terms of local extinction. More specifically, ana- spent aloft. Birds that fly only in short bursts have predominantly
lyses of locomotor performance and stamina in a widespread North white anaerobic muscle fibers in their flight muscles, while pro-
American lizard Urosaurus ornatus, across a range of habitats, indic- longed fliers have predominantly red aerobic fibers in the main
ate that the high-elevation populations in ponderosa pine forests pectoralis (downstroke) muscles. Flying birds have the highest
may be the most at risk, lacking an ability to modify their geographic
distribution on an appropriate timescale.

672 CHAPTER 16

Current climate Nival/ +3.5°C/ + 10% precipitation Nival/
polar desert change scenario polar desert
Alpine wet tundra
Alpine wet tundra Subalpine moist forest
Subalpine moist
Montane steppe
forest
Subalpine dry scrub Lower montane thorn
steppe
Montane steppe
Pre-montane thorn woodland
Montane desert scrub

Lower montane thorn steppe
Pre-montane thorn woodland

(a) Eastern slopes Western slopes
80 Alpine and forest zones 120
60
40 Alpine and forest zones
20 100
0
20 80
40
60 Area in vegetation zones (%) 60
80 Area in vegetation zones (%)
100 40

(b) 20

0

20

Savanna and steppe 40 Savanna and grassland
zones zones

Current +2.5°C +5.0°C 60 +2.5˚C +5.0˚C
Climate scenario Current Climate scenario

Alpine and forest zones: Savanna and steppe zones: Alpine and forest zones: Savanna and grassland zones:
Juniper savanna Cold snow zone Oak savanna
Cold snow zone Sagebrush steppe Alpine Grassland
Alpine Mountain hemlock
Mountain hemlock Silver fir
Abies grandis Western hemlock
Ponderosa pine Douglas fir

Fig. 16.56 Effects of global warming on ecosystems at altitude. (a) A warming of flight is 8–12 times that of the resting metabolic rate, reflecting
3.5°C is predicted to move floral zones upwards and severely reduce the high a much higher factorial scope than is found in exercising mammals
alpine communities in general. (b) Predictions for the east and west faces of a of similar size. In bats especially, there is considerably respiratory
northern hemisphere mountain range, for two different levels of warming. specialization to give fast uptake and transfer of oxygen: a thin
(a, Adapted from Beniston 1994.) blood–gas barrier, a vast alveolar surface, and a large lung capillary
volume. The first two features are also present in birds, with the
mass-specific energy turnover, and the highest core body temper- addition of a small and rigid lung aided by cross-current in the
atures, of any animals. The design features of the smallest humming- parabronchi (see Fig 7.11).
birds, which allow this power output, were considered in Chapter 6.
Respiratory cycles are often coupled to wingbeat frequency in
Because they are generally small, birds cannot store large amounts flying animals, with thoracic musculature (in both insects and birds)
of energy and may have fewer options for patterns of energy alloca- generating both effects and so giving a saving on muscular effort.
tion than any other vertebrates. Their power output in sustained The insect tracheal system is probably always adequate to cope with

EXTREME TERRESTRIAL HABITATS 673

supplying oxygen fast enough, but for vertebrates it is a different Bradshaw, D.S. (1986) Ecophysiology of Desert Reptiles. Academic Press,
story, particularly when flying at any height. At very high altitudes, Sydney.
where the partial pressure of oxygen is low, the driving force for dif-
fusion of oxygen across the pulmonary surfaces is very low, and here Carey, C., Florant, G.L., Wunder, B.A. & Horowitz, B. (1993) Life in the Cold:
only the cross-current blood flow system of the parabronchial bird Ecological, Physiological and Molecular Mechanisms. Westview Press,
lung will suffice, by insuring that partially depleted air continually Boulder, CO.
encounters new deoxygenated blood. Hence high flying is only
possible for birds, and is never seen in bats. Hadley, N.F. (1994) Water Relations of Terrestrial Arthropods. Academic
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The water balance problems of aerial animals are rather poorly
understood. Flapping flight in birds certainly increases respiratory Heller, H.C., Musacchia, X.J. & Wang, L.C.H. (eds) (1986) Living in the Cold:
water loss and may also increase cutaneous losses leading to rather Physiological and Biochemical Adaptations. Elsevier, New York.
rapid dehydration. However, all flying birds appear to be excellent
plasma-volume regulators, even when undergoing substantial Hochachka, P.W. & Guppy, M. (1987) Metabolic Arrest and the Control of
dehydration, an ability that in mammals tends only to occur in desert Biological Time. Harvard University Press, Cambridge, MA.
species. It appears that this goes with an ability to tolerate high heat
loads during flight. In insects, small species appear to suffer net Lee, R.E. & Denlinger, D.L. (1991) Insects at Low Temperature. Chapman &
water loss in flight, which may constrain their flight duration and Hall, New York.
require modified dietary choices (e.g. more dilute nectar for bees).
But large insect species, for example bees of more than 200 mg, Louw, G.N. (1993) Physiological Animal Ecology. Longman Scientific &
appear to generate more metabolic water than they can readily Technical, Harlow.
cope with due to their exceptionally high metabolic rates, and they
have been observed jettisoning excess water while in flight, both Louw, G.N. & Seely, M.K. (1982) Ecology of Desert Organisms. Longman,
by loss of saliva or crop fluid from the mouth and by copious dilute London.
urination.
Reviews and scientific papers
Finally, it should be noted that flying is an expensive business, Addo-Bediako, A., Chown, S.L. & Gaston, K.J. (2001) Revisiting water
with costs ranging from 50 to 120 W kg−1 in birds and bats, and up
to 300 W kg−1 in insects. There may therefore be design trade-offs loss in insects: a large scale view. Journal of Insect Physiology 47, 1377–
between flight apparatus and other organ systems. For example, in 1388.
territorial insect species where flight determines mating success, Ancel, A., Visser, H., Handrich, Y., Masman, D. & LeMaho, Y. (1997) Energy
such as in the dragonfly Plathemis, extra investment in flight muscle saving in huddling penguins. Nature 385, 304 –305.
may mean reduced gut tissues and fat reserves in the males, and per- Badyaev, A.V. (1997) Altitudinal variation in sexual dimorphism: a new
haps reduced longevity. pattern and alternative hypotheses. Behavioural Ecology 8, 675–690.
Baker, M.A. (1982) Brain cooling in endotherms in heat and exercise.
16.6 Conclusions Annual Review of Physiology 44, 85 –96.
Bale, J.S. (1993) Classes of insect cold hardiness. Functional Ecology 7,
Extreme environments pose a series of linked problems for their 751–753.
inhabitants, and some of these problems are rather similar whether Block, W. (1995) Insects and freezing. Science Progress 78, 349–372.
we are looking at deserts, polar regions, or mountains. Not only are Butterfield, J. (1996) Carabid life cycle strategies and climate change; a study
the problems similar, but the convergence of adaptation between on an altitude transect. Ecological Entomology 21, 9 –16.
quite different groups is striking. Animals living at these extremes Caceres, C.E. (1997) Dormancy in invertebrates. Invertebrate Biology 116,
have repeatedly acquired the same kinds of solutions: from behavior 371–383.
(use of burrows and other refugia, and gregariousness) through to Cerda, X., Retana, J. & Cros, S. (1998) Critical thermal limits in Mediter-
features at the gross morphological scale (overall size and shape, and ranean ant species: trade off between mortality risk and foraging perform-
the reduction or elaboration of appendages) down to physiological ance. Functional Ecology 12, 45 –55.
systems (peripheral countercurrent exchangers, altered insulation, Christian, K.A. & Morton, S.R. (1992) Extreme thermophilia in a
changes in metabolic rate, and periods of hypometabolism) and the central Australian ant Melophorus bagoti. Physiological Zoology 65,
fine details of biochemical endowments (altered membrane and 885 –905.
enzyme properties, and the use of osmolytes that protect against Convey, P. (1996). Overwintering strategies of terrestrial invertebrates in
freezing and desiccation damage). Convergent evolution is extremely Antarcticaathe significance of flexibility in extreme seasonal environments.
commonplace where there are only limited possible solutions to European Journal of Entomology 93, 489 –505.
common physical problems. Danks, H.V. (1992) Long life cycles in insects. Canadian Entomology 124,
167–187.
FURTHER READING DeLamo, D.A, Sanborn, A.F., Carrsco, C.D. & Scott, D.J. (1998) Daily activ-
ity and behavioural thermoregulation of the guanaco (Lama guanicoe) in
Books winter. Canadian Journal of Zoology 76, 1388 –1393.
Bouverot, P. (1985) Adaptations to Altitude-Hypoxia in Vertebrates. Duman, J.G. (2001) Antifreeze and ice nucleator proteins in terrestrial
arthropods. Annual Review of Physiology 63, 327–357.
Springer-Verlag, Berlin. Elkhawad, A.O. (1992) Selective brain cooling in desert animals: the camel
(Camelus dromedarius). Comparative Biochemistry & Physiology A 101,
195 –201.
Faraci, F.M. (1991) Adaptations to hypoxia in birdsahow to fly high. Annual
Review of Physiology 53, 59 –70.
Fletcher, G.L., Hew, C.L. & Davies, P.L. (2001) Antifreeze proteins of teleost
fish. Annual Review of Physiology 63, 359 –390.
Florant, G.L. (1998) Lipid metabolism in hibernators: the importance of
essential fatty acids. American Zoologist 38, 331–340.
Gaede, K. & Knülle, W. (1997) On the mechanism of water vapour sorption
from unsaturated atmospheres by ticks. Journal of Experimental Biology
200, 1491–1498.

674 CHAPTER 16

Gibbs, A.G., Louie, A.K. & Ayala, J.A. (1998) Effects of temperature on cuticu- (1969) Temperature regulation and respiration in the ostrich. Condor 71,
lar lipids and water balance in a desert Drosophila: is thermal acclimation 341–352.
beneficial? Journal of Experimental Biology 201, 71– 80. Schmidt-Nielsen, K., Schroter, R.C. & Shkolnik, A. (1981) Desaturation of
exhaled air in camels. Proceedings of the Royal Society of London B 211,
Haim, A. & Izhaki, I. (1995) Comparative physiology of thermoregulation in 305 –319.
rodents: adaptations to arid and mesic environments. Journal of Arid Sherbrooke, W.C., Castrucci, A.M. de L. & Hadley, M.E. (1994) Temper-
Environments 31, 431– 440. ature effects on in vitro skin darkening in the mountain spiny lizard
Sceloporus jarrovii: a thermoregulatory adaptation? Physiological Zoology
Hainsworth, F.R. (1995) Optimal body temperatures with shuttlingadesert 67, 659 – 672.
antelope ground-squirrels. Animal Behaviour 49, 107–116. Sinclair, B.J., Vernon, P., Klok, C.J. & Chown, S.L. (2003) Insects at low
temperatures: an ecological perspective. Trends in Research in Ecology &
Henen, B.T. (1997) Seasonal and annual energy budgets of female desert Evolution 18, 257–262.
tortoises (Gopherus agassizii). Ecology 78, 283 –296. Sinclair, B.J. & Wharton, D.A. (1997) Avoidance of intracellular freezing by
the New Zealand alpine weta Hemideina maori (Orthoptera; Stenopelma-
Jenni-Eiermann, S. & Lukas, J. (1992) High plasma triglyceride levels in tidae). Journal of Insect Physiology 43, 621– 625.
small birds during migratory flight: a new pathway for fuel supply during Stone, G.N. & Purvis, A. (1992) Warm-up rates during arousal from torpor
endurance locomotion at very high mass-specific metabolic rates? Physio- in heterothermic mammalsaphysiological correlates and a comparison
logical Zoology 65, 112–123. with heterothermic insects. Journal of Comparative Physiology B 162,
284 –295.
Klok, C.J. & Chown, S.L. (1997) Critical thermal limits, temperature toler- Storey, K.B. (1997) Metabolic regulation in mammalian hibernation:
ance and water balance of a sub-Antarctic caterpillar Pringleophora enzyme and protein adaptations. Comparative Biochemistry & Physiology
marioni. Journal of Insect Physiology 43, 685 – 694. A 118, 1115 –1124.
Storey, K.B. & Storey, J.M. (1990) Metabolic rate depression and biochem-
Kuhnen, G. (1997) Selective brain cooling reduces respiratory water loss ical adaptation in anaerobiosis, hibernation and estivation. Quarterly
during heat stress. Comparative Biochemistry & Physiology A 118, 891–895. Review of Biology 65, 145 –174.
Storey, K.B. & Storey, J.M. (1996) Natural freezing survival in animals.
Machin, J. & O’Donnell, M.J. (1991) Rectal complex ion activities and Annual Review of Ecology & Systematics 27, 365 –386.
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parisons with tenebrionids. Journal of Insect Physiology 37, 829 – 837. environments. Annual Review of Entomology 43, 85–106.
Tatar, M., Gray, D.W. & Carey, J.R. (1997) Altitudinal variation for senes-
Maina, J.N. (2000) What it takes to fly: the structural and functional respir- cence in Melanoplus grasshoppers. Oecologia 111, 357–364.
atory refinements in birds and bats. Journal of Experimental Biology 203, Tracy, R.L. & Walsberg, G.E. (2000) Prevalence of cutaneous evaporation in
3045 –3064. Merriam’s kangaroo rat and its adaptive variation at the subspecific level.
Journal of Experimental Biology 203, 773 –781.
Nagy, K.A. & Gruchacz, M.J. (1994) Seasonal water and energy metabolism Wagner, P.D. (2000) Reduced cardiac output at altitudeamechanisms and
of the desert-dwelling kangaroo rat (Dipodomys merriami). Physiological significance. Respiratory Physiology 120, 1–11.
Zoology 67, 1461–1478. Walsberg, G.E., Weaver, T. & Wolf, B.O. (1997) Seasonal adjustment of solar
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69, 1481–1501. the physiology and behaviour of Namib Desert tenebrionid beetles.
Evolution 50, 1231–1237.
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on Land (ed. P. Dejours, L. Bolis, C.R. Taylor & E.R. Weibel), pp. 155–179. camelus. Physiological Zoology 56, 568 –579.
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Schmidt-Nielsen, K., Kanwisher, J., Lasiewski, R.C., Cohn, J.E. & Bretz, W.L.

17 Parasitic Habitats

17.1 Introduction happened many times. Here we deal mainly with parasites living on
other animals, though of course many land animals are notionally
A great many animals live in an intimate association with another “parasitic” on plants.
organism, either on its outer surface or within its body; these “com-
mensals” range in their effect on the host from harmful parasites Parasites are known in most of the common phyla of animals
to beneficial symbionts (see Box 17.1), although here we are con- (Table 17.1), but certain groups are extremely rich in parasitic
cerned primarily with parasites having an intimate and negative species, particularly the tapeworms, flukes, acanthocephalans, and
effect on their host. Living in or on other organisms is phylogenet- nematodes (collectively often termed helminths), and the insects.
ically extremely widespread in the Metazoa, and it is clear that Nematodes are extraordinarily abundant and highly speciose, while
invasions of the body surfaces and the interiors of other species have the insect group contains huge numbers of species (especially para-
sitic wasps and flies) that develop as larvae inside other insects or

Box 17.1 Interactions between species over evolutionary time gradually change the relationship in ways that
benefit themselves.
It is traditional to view interactions between species in terms of positive
and negative impacts for each partner, resulting in an “interaction grid” On such a matrix, parasitism is usually classified as a contramensal-
as follows: ism; the parasite benefits and the host is harmed.

Species 1 Note, however, that the boundaries between parasitism and predation
become rather difficult, and in effect there is a continuum of kinds of
+ve 0 −ve relationship. Predators kill and eat many items of prey that are usually
+ve Mutualism smaller than they are; parasites do not normally kill their single much
Species 2 0 Commensalism Contramensalism larger host but eat it (or its resources) while it lives. A biting fly, or a
−ve Neutralism Amensalism vampire bat, that alights on a larger animal and sucks its blood is normally
Competition seen as predatory (but sometimes as parasitic, especially if it transmits
disease); a fly that punctures the skin to feed and then lays eggs in the
However, the terminology is often confused in existing literature, wound is more clearly a parasitic species. The term parasitism therefore
particularly in relation to the terms “commensalism” and “symbiosis”. needs to be reserved for associations that not only have a negative
Commensalism is often used in a wider sense than is shown in the matrix impact on the host but that also involve a relatively lengthy association
above, to include all kinds of situations where two species live together between the two species (so excluding the “hit-and-run” biting flies).
(usually one on or within the surfaces of another). Symbiosis is some-
times used as a catch-all term for species living and interacting together, There still remain problems with many arthropod “parasites” (com-
but is perhaps better reserved for a more restricted usage where two monly wasps and flies) where one or more eggs are laid on a host
species are both benefitting from an interaction, making symbiosis (usually a larval insect, not dissimilar in size from its attacker) by the
synonymous with mutualism. adult female. The resulting offspring hatch and feed on the host, which
is usually immobilized by their presence but still alive (hence the relation
Thus zooxanthellae within corals are an example of mutualism or sym- is parasitic) but which dies when they mature into adults and leave the
biosis, where both plant and animal benefit; bromeliad plants that live on carcass (hence the outcome is effectively predation). The term “para-
a tree trunk but take nothing from the tree are true commensals; and sitoid” is commonly used for these intermediate kinds of relationship.
herbivory and carnivory are both “contramensalisms”. But the boundar-
ies are not always clear-cut, and in almost every case both partners may For our purposes, the parasitoids are living for most of their life in an
internal enclosed environment created by the host and with physiolo-
gical problems like those of a parasite rather than those of a predator;
therefore we will include them in this chapter without further distinguish-
ing them from “true” parasites.

676 CHAPTER 17

Animal group Importance as parasites Table 17.1 Occurrence of parasite members in
animal groups.
Poriferans (sponges) A few “ectoparasitic”, boring into shells, etc.
Cnidarians (sea anemones, hydroids, etc.) A few ectoparasites on fish, etc.
Ctenophores (comb-jellies) Very few
Platyhelminths (tapeworms and flukes) All groups (except most turbellarians) are ecto- and

Nemertines endoparasites on invertebrate and vertebrate hosts
Rotifers A few parasitic/symbiotic? in other invertebrates
Nematodes (roundworms, filarial worms) A few ectoparasites
Huge numbers of endoparasites in invertebrate and vertebrate
Nematomorphs (horsehair worms)
Acanthocephalans (spiny-headed worms) hosts
Molluscs All endoparasitic in arthropods as larvae
All endoparasitic in vertebrate guts
Annelids Some larvae are parasitic on fish; a few adult ectoparasites

Insects and endoparasites
Leeches are ectoparasitic/predators; a few polychaetes
Crustaceans
are parasitic
Arachnids (spiders, mites, etc.) Very numerous ectoparasites (e.g. lice, fleas, tsetse flies,
Chordates
mosquitoes); also parasitoids on other insects (e.g.
ichneumon wasps, flies); some larvae endoparasitic in
vertebrates (e.g. bot flies)
Uncommon; some barnacles on crabs, some copepods
and branchiurans mostly on fish or on other crustaceans,
pentastomids in vertebrate lungs
Mites and ticks are ectoparasites
Some jawless fish are ectoparasites/predators

inside plants. From consideration of these two groups alone, which this chapter deals with the physiology of host defenses and the bio-
dominate the animal kingdom numerically, it is probably fair to chemical, physiological, and behavioral tricks used by parasites to
conclude that most animal species are parasites. cope with these.

This chapter surveys the departures from a free-living physiology There are other ways in which a biotic environment is unusual.
that are associated with a range of types of parasitism. There are two Animals normally control their own metabolic resource allocation
main aspects to cover. Firstly, being a parasite involves coping with using hormones as control agents, making “decisions” on alloca-
the abiotic conditions to be found when living in or on a particular tions to growth and to reproduction, eventually undergoing pro-
part of the host. For many parasites, homeostatic mechanisms gramed senescence followed inevitably by death. But many parasites
within the host provide the parasite with energy and nutrients, regu- are not passive bystanders in the control of host resource allocation,
late temperature and water balance, and supply the dissolved gases but instead actively reroute resources to favor their own develop-
for aerobic respiratory exchange while removing metabolic wastes. ment, by releasing hormones and neuromodulators that operate
In this sense, the parasitic life is physiologically “easy” most of the directly on host receptors. Effects include prevention of host repro-
time. However, some parts of the host environment (e.g. the acidic duction, alteration of host size, induction of entirely new tissues for
or anoxic parts of the gut) are less suitable for normal life; thus the parasite’s benefit, and considerable changes to host longevity.
parasites may show adaptations to unusual pH, redox potential,
dissolved gas levels, and so on. Some of these adaptations parallel To be successful a parasite must also reproduce or be trans-
features found in free-living organisms that occupy similarly extreme mitted within its host’s lifetime, posing a further set of physiological
environmentsafor example, some of the adaptations found in hurdles to be overcome, and mortality of propagules is often high.
gut-inhabiting nematodes and platyhelminths are similar to those Parasites show many adaptations that improve transmission
found in metazoans inhabiting anoxic muds. between hosts, including methods to synchronize parasite and host
reproduction, and manipulation of host behaviors. These mech-
However, being a parasite also involves interactions with a host, anisms operate through intimate chemical interactions between the
which constitutes a biotic environment, and which creates a unique parasite and host, giving an added dimension to parasite environ-
set of problems. Most obviously, the host commonly seeks to evict mental physiology.
the parasite, and is therefore an aggressive environment that “fights
back”; and just as hosts are part of the parasite environment, so Clearly, many of the more dramatic metabolic adaptations in the
parasites are an ancient part of the host environment. Many hosts environmental physiology of endoparasites are responses to a host
have developed a range of defenses against parasite attack, and these environment that is both hostile and capable of coevolutionary
in turn have led to an equally diverse array of parasite counter- responses. Indeed host and parasite genomes may become intim-
measures. Whereas physiological solutions to a given abiotic envir- ately linked, and recent evidence indicates convergent changes in a
onmental challenge should have long-term selective value in that range of parasite genomes, including reduced genome size and
environment, the same cannot be said of the host–parasite arms lowered G + C content, while genes for surface proteins or cell wall
race, which is an ongoing evolutionary struggle with no predefined constituents divergently multiply. It may be that the parasites should
optimum or endpoint. Defense and counterdefense are therefore not really be seen as having “invaded” hostile environments in an
a dominant part of the biology of many parasites, and a large part of evolutionary sense, but as having “created” them by driving the evo-
lution of the hosts’ protective and immune systems. Certainly these

PARASITIC HABITATS 677

evolutionary interactions are a major part of what makes parasite 17.2.2 Living in respiratory passages
environmental physiology unique.
Many parasites inhabit the buccal cavities or respiratory chambers
17.2 Parasite environments of larger animals; most notable are the great range of flukes and
leeches found in the gills and buccal cavities of marine and fresh-
The environment of parasitic organisms is unusual in consisting of water crustaceans and fish. These locations are still essentially
two components: ectoparasitic, though less exposed to some aspects of the external
1 The macrohabitat in which the host organism lives. conditions. Many parasites have taken this route further, and inhabit
2 The microhabitat, resulting from modification to the free-living deeper respiratory passages as endoparasites. These environments
environment brought about by living in or on a particular region of are moist enough to allow essentially aquatic taxa to survive; for
the host. example, the lungs of terrestrial vertebrates support crustaceans
(e.g. pentastomids in snakes and birds) and platyhelminths (e.g. the
The importance of these two components in determining the human lung fluke). Parasites derived from terrestrial ancestors have
environment experienced by a parasite varies enormously across the also invaded respiratory passageways, for example the mites whose
spectrum of host–parasite interactions, differing between parasite infestation of the tracheae of bees causes the disease varroa, and the
species and between stages in the same parasite life cycle. At one maggots of the nostril fly, Oestrus ovis, which live within the nasal
extreme, some parasites living on the external surface of their host passages of sheep and goats. Here most aspects of the parasite’s
(termed ectoparasites) may experience much the same environ- physical environment (such as temperature, levels of respiratory
ment as their host, and so require similar physiological tolerances gases, and water content) are dominated by the host, and physiolo-
and adaptations to free-living organisms in the same habitat. At the gical problems are relatively limited. The entry and exit of eggs
other extreme, parasites living within host tissues (termed endo- or infective larval stages is also uncomplicated, via the respiratory
parasites) commonly experience a relatively stable but often highly openings. A dramatic example of this is provided by the larvae of the
unusual internal microhabitat, and they may have their thermal, nostril fly, which when mature migrate towards the nostril openings
osmotic, respiratory, and nutritional needs met entirely by the host. and are expelled into the environment in an explosive sneeze!
The term “endoparasite” covers a wide range of different niches However, this also points to a major drawback of life in respiratory
within a host’s body (especially if the host is a vertebrate), and dif- passages; many hosts, and especially vertebrates, have defenses such
ferences between these niches have major consequences for the as coughing and sneezing that serve to eject parasites.
environmental physiology of parasites. In addition to the ectopara-
sitic environment on the skin, we therefore need to consider three Many of the parasites in respiratory passages feed by penetrat-
major categories of endoparasitic nicheathe respiratory passages, ing the wall of the host’s body to feed on blood. They then become
gut, and bloodain what follows. vulnerable to attack by the various blood-mediated host defenses
discussed below, and their environment is best regarded as some-
17.2.1 Living on the skin what intermediate between respiratory and blood-based.

For parasites in aquatic environments there is little “microclimatic” 17.2.3 Living in the gut
amelioration around the surfaces of the host animal, whereas for
terrestrial ectoparasites, especially on birds and mammals, the envir- Parasites inhabiting the gut are surrounded by host food material,
onment close to the host skin may be much less thermally variable which provides nutrition for many of them (particularly cestode
and much less desiccating than the macrohabitat. Skin ectoparasites tapeworms). The gut lining is also richly vascularized, providing
on a land vertebrate may need only fairly narrow thermal tolerances a further food source for those gut parasites that penetrate the gut
and many will have relatively little problem with water balance. This wall and feed on blood (nematodes and some trematode flukes)
will be especially true if the parasite is “plugged in” permanently or or tissue fluids (acanthocephalan worms). Entry via the mouth is
intermittently to the capillaries or tissues of its host, as with many easily achieved, and the exit of eggs or infective larval stages is
ticks and fleas, and thus endowed with a freely available water supply. also uncomplicated, via the anus or possibly via the mouth if the
parasite can move itself or its propagules upwards against the gut
The physiological tolerance of particular groups of skin parasites movements.
may mean that they are capable of living in some environments and
not others. This is again seen most clearly when comparing terres- However, there are severe problems as well. The gut of most
trial and aquatic habitats. For example, while platyhelminth flukes potential hosts is a relatively anoxic environment, especially in its
are major ectoparasites of vertebrates in marine habitats, they are far lower reaches, and many gut parasites are therefore at least facul-
less abundant and speciose in terrestrial hosts, presumably being tatively capable of anaerobic respiration. Also, gut parasites are
unable to cope with the desiccation associated with a terrestrial exposed to the digestive processes of the host, including extremes of
environment given their permeable outer surfaces (see Chapter 5). pH, high levels of activity of a range of enzymes, and the mechanical
Some monogeneans survive in terrestrial habitats by generally action of peristalsis. Conditions are most extreme in the stomach,
avoiding the most exposed outer surface of the host, and limiting with a very low pH, abundant proteolytic enzymes, and a high turn-
any free-living phase in their life cycle to periods when the host is in over of the stomach lining making attachment difficult; relatively
water. A good example of this is the common fluke Polystoma, few metazoan parasites survive here. At a given location in the gut,
which as an adult inhabits the bladder of frogs. conditions may also change dramatically and cyclically during the
processing of a single host meal. Species feeding on blood may be

678 CHAPTER 17

attacked by blood-borne host defenses, and some host defenses are borne (humoral) and cell-mediated responses, as well as some more
also known to reach nonblood feeders in the gut lumen. Further- widespread defensive systems.
more, the gut again has ways of physically removing parasites at
either end, by vomiting or by the copious fecal emissions (diarrhoea) The tapeworm Hymenolepis diminuta provides the best studied
induced by some parasitic infections. example of adult migration between microenvironments within the
host gut. The adults show a daily (circadian) migration in response
17.2.4 Living in tissues and blood to the position of food along the gut. When the host’s stomach is
full after feeding, the scolex (“head” region) of the worm is found
Host tissues include not only the muscles, body cavity, and organs within the intestine close to its exit from the stomach (the pyloric
of the host, but also host circulatory systems containing cells (e.g. sphincter). With the passage of food into the intestine, the worm
blood and lymph). In some ways, these constitute ideal parasite shifts back down the intestine, and finally moves forward again to
habitats: as long as the parasite tissues have similar general require- await the next host meal. An adaptive explanation for this change
ments to the host tissues, they are provided with nutrients and in position is that the cestode is using the balance between the sur-
oxygen, and waste products and carbon dioxide are removed for rounding host gut contents and the physiological environment to
them. In other ways, inhabiting host tissues is the most demanding achieve adequate absorption of nutrients. Indeed there is evidence
of all parasitic habitats. Firstly, although tissue parasites are pro- that some parasites adjust their position in the host’s gut when the
tected from physical removal, they are exposed to the full range of host expects to be fed, even if the host does not actually feed. This
host defenses based on host recognition of nonself tissue (described occurs in the digenean fluke Bunoderina encoliae, which inhabits
below). Such exposure has given rise to a spectacular diversity of the rectum of sticklebacks, and it suggests that parasites can detect
parasite countermeasures, including the exploitation of a number stimuli more subtle than the mere presence/absence of gut contents.
of specific parts of the host’s bodyaimmunologically privileged
sitesawhere host defenses are reduced. Second, there is often no It is also important to realize that parasites (particularly endopar-
direct aperture in the host’s tissues through which the parasite can asites) may move between very different environments during their
infect the host or release eggs or larvae. Tissue-inhabiting parasites life cycle. This is well illustrated by the life stages of the digenean
thus tend to have complex life cycles and infective strategies. Eggs or fluke Schistosoma mansoni (Fig. 17.1), which causes the disease
larvae may escape by release into the gut or lungs (thus encounter- bilharzia in humans. Schistosomes generally live as adults in the
ing, albeit briefly, the problems already outlined for such areas), or blood system of vertebrates, and adults of S. mansoni prefer the fine
may be transmitted by a blood-feeding vector such as a mosquito. mesenteric blood vessels surrounding the human gut. Schistosome
Entry into a second host may involve boring into host tissues by eggs are spiny, and with the help of the host’s immune system (see
larvae, boring out of the host’s gut after being swallowed, or being section 17.7) make their way out of the host’s body with the feces
injected by blood-sucking insect vectors. or urine. The eggs hatch into free-swimming ciliated miracidium
larvae, which locate and penetrate a freshwater snail as the second
17.2.5 Microenvironments in space and time host organism. The miracidium larvae give rise to a different type
of larva, the sporocyst. These reproduce asexually in the snail, pro-
A feature of parasites inhabiting each of these habitat types is that ducing first a second generation of sporocysts and then a third larval
the region of the host body they exploit is extremely specific (e.g. a type, the cercaria. The cercariae leave the snail and swim actively
particular part of the respiratory tract, or of the gut, or a particular until they encounter human skin; they then bore through the skin
set of blood vessels). Characteristics of internal host environments and shed their ciliated larval epidermis, metamorphosing very
that confer this specificity not only include general aspects such as rapidly into a smaller version of the adult worm, called a schisto-
pH, salt concentrations, and levels of oxygen and carbon dioxide, somula. These immature adults migrate to the blood supply, and
but many more intimate fluctuations in host physiology. Recogni- travel in it until they reach the hepatic portal vein. This life cycle
tion of these is important in many aspects of parasite biology, rang- thus involves two distinct dispersive free-living freshwater stages,
ing from parasite migration within the host to the timing of parasite which must cope with the vagaries and variability of freshwater
reproduction. bodies (see Chapter 13), and also must cope with abrupt changes
in their external environment as they penetrate the tissues of their
Host physiology may alter on a variety of temporal scales. Changes next host. There are also two stages that develop inside host tissues,
may be unidirectional and long term (such as those associated with but the two hosts are extremely disjunct taxonomically, differing
sexual maturation), or medium term and cyclic (such as the changes in such basic variables as body temperature and levels of dissolved
in levels of mammalian reproductive hormones in the blood, or gases and metabolites, and also in the types and magnitudes of
changes in levels of insect molting hormones), or operate on even defenses they are able to mount against invading organisms. The
shorter timescales (such as changes in the chemical composition of different environments encountered by the life stages of S. mansoni
the gut associated with the processing of a meal, or changes in the have been inevitably selected for stage-specific physiological adapta-
levels of metabolites associated with host activity–sleep cycles), and tions; successful completion of the life cycle requires appropriate
these short-term changes can be particularly important in synchro- sense organs at each stage to detect which environment the current
nizing the release of infective stages in some parasites (e.g. the life-cycle stage is in. These sensory inputs must be linked to switches
release of nematode filariae into the blood). In addition, many hosts able to trigger the expression of genes relevant to each particular
are able to deploy mechanisms that have evolved specifically to environment. This example shows that the modifications to the
impede parasites, including a wide range of relatively specific blood- environmental physiology of a free-living organismaeven a relat-
ively “simple” platyhelminthamay be extremely complex.

PARASITIC HABITATS 679

(e)

Via heart
to liver

4–10 days of Adult worms in liver.
development Permanent pairing begins

in lungs about the 26th day

Via heart In mammal Pairs enter hepatic
to lungs portal system
Some eggs
Schistosomulum enters return to Eggs laid in (a)
lymphatics mesenteric vessels
liver, causing
Cercaria penetrates granulomas Eggs tear through
mammal skin into intestine.

In water Excreted in feces
Emergence of cercariae begins
about 15 days after infection.
Continues up to 3–4 months

Eggs fully embryonated

Cercariae formed Numerous daughter In water
sporocysts
Ciliated miracidium
In snail hatches. Must enter
(d)
snail within 24 h

Penetrates
snail tissue

(b)

(c)

Fig. 17.1 The life cycle of the human blood fluke, Schistosoma mansoni. Enlarged A feature of any complex life cycle is that the behavior and envir-
life-cycle stages are: (a) a fertilized egg, (b) a miracidium larva, (c) alternative onmental physiology of any one life cycle stage may limit the distri-
snail hosts, (d) a cercaria larva, and (e) a pair of adult flukes, with the female lying bution of the parasite. Thus while adult Schistosoma can probably
in a groove in the male. (Adapted from Trager 1986.) survive in human beings anywhere, they also require freshwater
habitats containing the snail intermediate host. Furthermore, snail
and human hosts must be abundant enough for the larvae involved

680 CHAPTER 17

Hosts Parasites
1
A

B2

C3

D4

E5

A1

B2

C3

D4

(a) E5
Pocket gophers
O. hispidus Chewing lice Fig. 17.2 (a) Alternative patterns of speciation
O. underwoodi G. chapini in parasites and their hosts, with host–parasite
O. cavator G. setzeri relationships indicated by dashed lines. In the upper
O. cherriei G. panamensis example, speciation of host-specific parasites exactly
O. heterodus G. cherriei tracks speciation of hosts. Such parallel evolution
G. costaricensis results in Fahrenholz’s rule: i.e. taxonomically
Z. trichopus G. trichopi related hosts have taxonomically related parasites.
P. bulleri The lower example shows a case in which host and
C. castanops G. nadleri nonspecific parasite phylogenies do not match. (b)
C. merriami G. expansus A clear example of parallel evolution, demonstrated
G. busarius (b) between pocket gophers (rodents of the family
G. geomydis Geomyidae) and their chewing lice (order
G. busarius (a) Mallophaga, family Trichodectidae). Gophers:
G. breviceps G. oklahomensis O, Orthogeomys; Z, Zygogeomys; P, Pappogeomys;
G. personatus G. ewingi C, Cratogeomys; G, Geomys; T, Thomomys. Lice:
T. bottae G, Geomydoecus; T, Thomomydoecus. (a, Reprinted
T. talpoides G. texanus from International Journal for Parasitology 23, Page,
(b) G. actuosi R.D.M., Parasites, phylogeny and cospeciation,
pp. 499–506, copyright 1993, with permission from
G. perotensis Elsevier Science; b, from Hafner & Page 1995.)

G. thomomyus

T. minor
T. barbarae

to find them in their very limited lifetimesaa matter of hours in hawaiiensis, which is an exception to the monogenean generaliza-
each case. Considerations of this kind mean that many parasites tion made above, being able to infect 24 fish species distributed in a
have a limited distribution even in regions where they are generally range of families but all living in the same coral reef habitat. The
endemic. study of the relative importance of parasite–host relationships and
external macroenvironments in determining speciation patterns in
17.2.6 Parasite environment and parasite speciation parasites is very much in its early stages, though, because the sam-
pling of host species for their parasite faunas is still very incomplete.
The importance of host microenvironments in the evolutionary
radiation of parasite groups is encapsulated in what has become 17.3 Basic parasite physiology
known as Fahrenholz’s rule, which states that the evolutionary radi-
ations of parasites tend to parallel those of their hosts (Fig. 17.2). 17.3.1 Ionic and osmotic adaptation, and water balance
Parasite groups that show this pattern tend to be highly adapted to
their host environment and to infect only a small diversity of host In general, parasites are either bathed in, or are taking in fairly
species; for example, 78% of monogenean parasites of fish and 70% continuously, a fluid that is already being regulated by their host. In
of parasitic copepod crustaceans are restricted to a single host spe- this sense they have fewer problems with osmotic physiology than
cies. However, not all parasite groups follow Fahrenholz’s rule, and almost any other kind of animal. Once inside the host many of them
some parasitic taxa are characteristic of a given habitat rather than a are highly permeable, are fairly intolerant of water loss (because
group of closely related hosts; a good example is the fluke Benedenia

PARASITIC HABITATS 681

they never experience it), and have weak or absent kidney function. absent from hosts in warm marine areas, preferring cool temperate
However, it must always be remembered that the larval or transmis- seas; and it is found near the surface at cooler high latitudes but in
sion phases may have very different problems, surviving outside the deeper waters at lower latitudes.
host in what may be very different osmotic conditions. Endoparasitic
nematodes that infect insect larvae are known to remain within the For terrestrial ectoparasites, temperature balance is also usually
host cadaver for variable times dependent on the external humidity; fairly easy, as they exist mainly within the stable boundary layer
at low relative humidity (RH) they may stay within the corpse for up created around a reasonably sized host (only during transmission
to 50 days rather than emerge and risk desiccation. Other nematode between hosts are cooler temperatures potentially encountered,
parasites adopt the cryptobiotic response (see Chapter 14) when so that egg or larval stage may need greater cold tolerance or even
exposed to desiccation during transmission. freeze tolerance). Ectoparasites are therefore common on land
vertebrates, and especially on endothermic hosts where the trapped,
Many aquatic ectoparasites are surprisingly sensitive to variation still air within fur or feathers may be at a rather constant tem-
in the salinity of the environment inhabited by their host, and perature (close to the host’s body temperature, Tb), and at a high
monogenean and trematode platyhelminths are generally rare in humidity. Thus an ectoparasite here may need a rather high but
low-salinity environments. Where the host is better able to tolerate narrow-band thermal tolerance, and can use enzymes and mem-
variation in salinity than its ectoparasite, the ectoparasite may be branes with rather limited acclimatory ranges. In cold climates,
absent from part of the host’s range; this applies for the mono- ectoparasites tend to congregate in the warmest places: the “armpit”
genean fluke Benedenia melleni, which has a lower tolerance of high or “groin” regions of mammals, or beneath the wings on birds. On
salinity than its fish hosts. marine mammals they may be fairly evenly dispersed in the aquatic
phase, but tend to accumulate on the tail flipper when seals and
Terrestrial ectoparasites may have very little amelioration of walruses haul out to give birth, this being the warmest spot and used
water balance or ionic problems across their external surfaces relat- for basking; for example, the lice on elephant-seal flippers stay at
ive to a free-living animal in the same environment, but they do 27–34°C throughout a diurnal cycle.
have the advantage of being plugged in to a reliable regulated fluid
source. Some species with terrestrial hosts may have the option of For endoparasites, problems are again effectively handed over to
excreting into the host (as in the tick shown in Fig. 5.23) rather than the host’s regulatory systems for large parts of the life cycle. But
to the outside world. Some endoparasites of desert ectotherms may many endoparasite life cycles involve transitions between different
face significant problems, however; the monogenean Pseudodip- thermal environments. This is particularly true for those life cycles
lorchis inhabits the bladder of the spadefoot toad Scaphiopus (see (such as the infection of human hosts by schistosome cercariae, or
section 16.2.2) and must therefore survive greatly increased osmotic the injection of nematode filaria larvae into mammalian blood by an
concentrations for many months at a time. insect vector) where a free-swimming larva enters an endothermic
host. Such abrupt changes in thermal environment can be very
Endoparasites are probably usually in osmotic balance with their damaging (as discussed in Chapter 8), and parasites make extensive
animal host’s tissues, though this is rarely studied. For any host of use of heat shock proteins (HSPs) to protect their metabolism. HSP
reasonable size, whether in sea water, fresh water, or on land, this manufacture can occupy a major proportion of a parasite’s meta-
will give the parasite a stable habitat. In land and freshwater animals, bolism during such transitions; in adult schistosomes, production of
and in marine vertebrates, a stable osmotic concentration of 100– HSP-70 represents more than 1% of the total adult protein produc-
400 mOsm is likely, while in marine invertebrates the concentration tion, and levels are higher again in the postinvasion schistosomula
is around 1000 mOsm. The interesting experiences will come for larva. The transmission stages of vertebrate endoparasites may also
parasites on migratory aquatic hosts, for example eels, salmon, and need much broader thermal tolerance; nematode parasites have a
crabs such as Eriocheir that move between seas and rivers. Little is marked degree of cold tolerance that is also susceptible to rapid
known of such parasites, but it is very likely that the host does most selection. They have also been shown to change their membrane
of the regulatory work and the parasite conforms with the resulting lipid saturation in similar fashion to other ectotherms exposed to
osmotic concentration of the host tissues. colder conditions. Most nematodes that exploit insect hosts also
have a suite of inducible HSPs that can protect them from excess
One interesting example of host habitat effects on parasite heat (e.g. in a heated decomposing corpse until conditions are
physiology is provided by some endoparasitic wasps that develop favorable for leaving). There are indications that nematode para-
inside larvae of species of fruit fly (Drosophila). These fruit flies live sites of vertebrate hosts living in extremely arid and hot conditions,
in fermenting fruit, and particular species differ in their tolerance such as those of the dromedary of the Sahel, have rather specialist
of the ethanol generated by fermentation in this habitat. Parallel suites of enzymes with reduced isozymic variation compared with
adaptations are found in the parasitic wasps: strains and species that nematodes from more mesic hosts.
attack Drosophila in alcohol-rich habitats show greater tolerance of
ethanol. While intricate temperature regulation may not be a notable
feature of parasitic adaptation, sensitivity to temperature certainly
17.3.2 Thermal adaptation is. For many parasites that develop in or on endothermic hosts, tem-
perature is a major cue for larval penetration of the host, or for egg
Small aquatic ectoparasites effectively experience the thermal hatching within the host. For example, schistosome cercariae move
vagaries of the macrohabitat, since water is usually well stirred and up a temperature gradient when locating human skin, and fleas
of quite high thermal conductivity. Thus temperature may be locate new hosts by moving towards warmth. Hatching of a range
important in constraining the environment occupied by these kinds of eggs, including taeniid tapeworms, is triggered by temperature.
of parasite. For example, the trematode fluke Derogenes varicus is

682 CHAPTER 17

Nematodes that have snails as intermediate hosts have an unusually producing bladder, but with the posterior segments of the flea con-
high developmental temperature threshold, and this probably helps taining a narrow airway that penetrates the host’s skin through a
to insure that larvae remain in their first instar while the snail under- small pore.
goes winter hibernation, the first instar being more cold resistant
than later larvae. In general, a very wide range of parasites associated Endoparasites
with endothermic hosts show high sensitivity to temperature gradi-
ents as infective stages. All endoparasites need the physiological scope to cope with the
particular levels of oxygen and CO2 (and the associated pH) of
While parasites may show adaptation to high body temperat- their niche within the host. However, in any one particular spot
ures in endotherms (37–41°C), a range of host organisms react to these conditions should be relatively constant, so in some sense
infection by producing short bursts of exceptionally high body the adaptation is not too difficult. Some parasitic sites, such as
temperatureagenerally termed fever (see Chapter 8). Fever in the bloodstream and lungs, are unambiguously aerobic, while the
vertebrate endotherms is induced in response to chemicals termed lumen of the small intestine and the bile duct may have consistent
pyrogens, which can be produced either by parasitic organisms but extremely low oxygen tensions. The hemoglobin of the fly
(exogenous pyrogens) or by host blood cells (endogenous pyro- Gasterophilus can even, apparently, take up O2 from the stomach
gens). In mammals both operate, as endogenous pyrogens are contents of the horse it lives in, having a P50 of only 0.003 kPa.
produced by leucocytes in response to exogenous pyrogens, and Parasitic worms such as the nematode Ascaris lumbricoides or the
they act directly on the hypothalamic temperature control center to fluke Fasciola hepatica are oxygen conformers, i.e. the rate of oxygen
elevate the setpoint about which temperature is regulated. Some uptake varies with the partial pressure.
ectothermic animals (including some caterpillars and some lizards)
also react to infection by elevating their body temperature. In But the greatest physiological problem by far is usually that
these cases elevation is usually achieved by a change in behaviora respiration must necessarily be anaerobic, particularly in the large
increased basking duration, and altered posture to increase the intestine.
surface over which heat is absorbed. In these ectothermic cases,
fever has a demonstrated advantage in conferring protection from relative use of anaerobic respiration
bacterial infections, but in endotherms the role of fever is less clear. In a number of ways, respiration in parasites inhabiting relatively
High temperatures may slow infections down, but can also cause anaerobic habitats (such as the lower gut of vertebrates) parallels
harm or even death to the host. pathways seen in free-living metazoans inhabiting environments
such as anoxic surface muds in aquatic habitats, and the pathways
Temperature also has marked effects on parasite–host interac- must often have been inherited from free-living ancestors. Indeed,
tions, altering relative levels of susceptibility, latency, and virulence; parasites sometimes show metabolic pathways that seem unsuited
the net effects are rarely linear and there can be complex outcomes to their habitat in the host. For example, anaerobic respiration is
at the population level. common in adult nematodes and platyhelminths, and is found even
in species inhabiting relatively aerobic habitats, such as the blood of
17.3.3 Respiratory adaptation vertebrates. Use of relatively inefficient anaerobic metabolism even
where oxygen is available suggests that the efficient exploitation of
Ectoparasites high-energy metabolites has not been important in these species.
Perhaps this is because these materials are so abundant in the host
In general, ectoparasites exchange gas with the macroenvironment, environment that parasites can “afford” to be wasteful. In explain-
whether water or air, and show little specialization. However, some ing the metabolic pathways used for energy generation by parasites,
aquatic ectoparasites show a range of behavioral responses when we therefore need to separate genuine adaptations to selective pres-
exposed to hypoxia by the behavior of their host. For example, sures from ancestral mechanisms characteristic of particular taxa
Entobdella soleae, a monogenean ectoparasite of the sole, shows that may have little or nothing to do with a parasitic way of life.
increased body undulations to maintain movement of water over Remember also that the use of entirely anaerobic respiration does
the body surface through which gas exchange takes place. Similarly not necessarily mean that a particular species can thrive in the total
fish lice increase the ventilatory movements of their pleopods absence of oxygen. Schistosomes, for example, largely respire anaer-
(modified abdominal limbs). Parasites that occupy the outer respir- obically as adults, but require a certain minimal level of oxygen to
atory passages of their hosts are supplied with oxygen by the host’s carry out the synthetic reactions associated with the manufacture of
ventilatory currents (e.g. flies living in the nasal passages of rumin- egg shells. In the total absence of oxygen, adult schistosomes survive
ants, or marine leeches in the branchial cavities of fish). well but cannot reproduce.

Some tissue endoparasites are able to be “ectoparasitic” in terms Aerobic respiration is now known to occur at a low level in
of respiration, reaching the exterior for gas exchange by causing many adult parasites formerly thought to rely entirely on anaerobic
lesions in the host body wall. For example, the larvae of many respiration. While the activity of the aerobic respiration pathways is
tachinid flies have posterior spiracles armed with hooks that they limited, the far greater yield of ATP per glucose molecule generated
use to penetrate either the skin of their host, or an air sac or major aerobically means that even low activity can make a significant con-
tracheal airway. The host responds by forming a funnel of wound tribution to the parasite’s energy budget. In the filarial nematode
tissue around the parasitoid larva’s spiracles, providing permanent Litomosoides carinii, adults pass only 2% of their carbon through
access to gas exchange with the exterior. The jigger flea has a similar aerobic respiration, and 98% is fermented; yet starting with 100 mol
trick, the adult living beneath the skin as little more than an egg-

PARASITIC HABITATS 683

of glucose, the energy yield of the 98 mol processed via fermentation There are two other important differences relating to parasite
is 196 mol of ATP, and the 2 mol of glucose respired aerobically anaerobiosis compared with free-living versions. Firstly, for para-
generate 72 mol of ATP, or 27% of total energy storage. sites it is a semipermanent state, not an emergency measure until
oxygen returns. Thus helminths do not accumulate anaerobic end-
The large intestinal nematode Ascaris lumbricoides exhibits trans- products for later resynthesis into glycogen. Secondly, in parasitic
itions in energy metabolism during its life cycle that are character- helminths anaerobic metabolism persists even if some oxygen is
istic of a number of parasites. The eggs leave the host with feces, and available, and the anaerobic pathways are not inherently inhibited
survive in the soil. Larval development within the egg is aerobic, by the presence of oxygen.
with a high activity of enzymes involved in the Krebs cycle. After
ingestion of the egg, a second-instar larva emerges within the host’s In general, anaerobic parasitic helminths can be divided, on the
gut. It burrows through the gut mucosa to enter the bloodstream, basis of their end-products, into two groups:
reaching the liver 2–3 days after infection, where it molts into a 1 Those that rely essentially on glycolysis alone and produce lactate
third-instar larva. This then switches to anaerobic metabolism as it or some other reduced derivative of pyruvate as end-products of
migrates via the heart to the lungs, reaching them after 7–9 days. carbohydrate breakdown (“homolactic” fermentation).
The larva then moves up the trachea and is swallowed, reaching the 2 Those that go beyond glycolysis to fix carbon dioxide and have
intestine again after 8–10 days where it molts into a fourth instar what is often referred to as an “Ascaris-type metabolism”.
before finally reaching adulthood. Both the fourth-instar larva and
the adult can continue their development in the complete absence In parasitic helminths where carbohydrate is broken down glyco-
of oxygen. lytically, the amount of lactate varies from 30% under aerobic
conditions to 80% under anaerobic conditions. Acetate and acetoin,
In Schistosoma, the transition from aerobic respiration in the the other end-products, are produced by the decarboxylation of
cercaria to anaerobic metabolism in the schistosomula (see Figs 17.1 pyruvate via the pyruvate dehydrogenase complex. In the acantho-
and 17.8) is very abrupt. When a cercaria penetrates human skin cephalan Moniliformis, the main end-product is ethanol, with small
there are two rapid morphological changes: the propulsive tail is amounts of lactate, succinate, and volatile fatty acids. These para-
lost, and the outer layer of cuticle (the glycocalyx) surrounding the sitic helminths do not produce alanine, octopine, alanopine, etc. as
remaining anterior part of the body is shed. The loss of the glyco- anaerobic end-products, unlike free-living anaerobic invertebrates.
calyx results in a massive increase of the permeability of the parasite
epidermis to host metabolites, some of which are thought to be the Ascaris adults illustrate the alternative anaerobic energy-generation
cause of the metabolic shift from aerobiosis to anaerobiosis. The key mechanism that is also found in other (unrelated) gut parasites,
host metabolite may be serotonin (5-hydroxytryptamine, 5-HT), such as the tapeworm Hymenolepis, as well as in some free-living
which among other effects it has in vertebrates, activates the enzyme invertebrates. Glycolysis terminates with phosphoenolpyruvate
adenyl cyclase and promotes the formation of cAMP. This has a (PEP), rather than pyruvate, and the enzyme PEP carboxykinase then
direct effect on respiration through its ability to activate a number converts the 3-carbon PEP to a 4-carbon product, oxaloacetate, a
of enzymes involved in glycolysis. step that generates 1 ATP. The enzyme malate dehydrogenase is
then used to reduce oxaloacetate to malate. In the process, the
In other parasites, shifts between mechanisms may be gradual NADH formed in glycolysis is oxidized to NAD+, maintaining the
rather than abrupt. In large parasitic worms, mitochondria with NADH/NAD+ balance.
cristae on the inner membrane are concentrated in outer tissues,
while mitochondria in deeper tissues lack cristae. Cristate mito- The malate produced enters the mitochondrion, and rather than
chondria generally indicate aerobic respiration, and the absence of entering the normal Krebs cycle it acts as the substrate for two other
cristae usually indicates anaerobiosis, leading to the conclusion that linked pathways. These pathways together are termed malate dis-
deeper tissues predominantly use anaerobic respiration. This has mutation; malate is reduced in one series of reactions, and oxidized
been explained as the result of limited diffusion of oxygen into the in the other. In the oxidation route it is converted to pyruvate and
tissues of larger parasites. It may also explain in part the general shift CO2, while in the reduction route it is converted to fumarate and
from aerobic to anaerobic respiration through the life cycle of para- then succinate (Fig. 17.3). These two reactions are coupled in that
sitic platyhelminths, being an effect of increasing size as well as of the oxidation route generates NADH from NAD, and this NADH
changes in habitat. is then responsible for the reduction of malate in the second route.
As in normal aerobic respiration, the NADH generated is the raw
anaerobic pathways material for an electron transport system. The cytochrome involved
Respiration involves the oxidative breakdown of a small organic in the anaerobic electron transfer system (cytochrome b558) is differ-
molecule, and this is most typically glucose, but raw materials can ent to those used in the usual aerobic chain (cytochromes a, a3, b, c,
include amino acids, glycerol, or fatty acids (see Chapter 6). It seems and c1), and the terminal electron acceptor is fumarate rather than
that parasites have an almost complete dependency on carbohy- oxygen. The cytochrome and fumarate reductase enzyme make up a
drate (either as glycogen or exogenous glucose) as their sole energy complex that is the major component of adult Ascaris mitochon-
source. In adult helminths there is no active β-oxidation sequence, dria, and rhodoquinone is used as an electron carrier, rather than
so there is no catabolism of fatty acids, and amino acid catabolism is the ubiquinone characteristic of the aerobic electron transfer chain
very limited. Similarly, there is no evidence of the cofermentation of (see Chapter 6). The redox potential of ubiquinone is more positive
amino acids and carbohydrate or of fatty acids and carbohydrate; (+113 mV) than that of the fumarate/succinate couple (+33 mV),
this is found in the free-living larvae of some endoparasites, but is such that electron transfer to fumarate would not be favored. In
absent from the adults. contrast, the redox potential of rhodoquinone is strongly negative
(−63 mV), favoring electron transfer to fumarate. In Ascaris and

684 CHAPTER 17 Mitochondrion

Cytoplasm (?) ATP 2-Methylbutyrate
Glucose ADP 2-Methylvalerate

NAD+ NADH + [H] Propionate
Acetate
PEP
(?) ATP GTP (?)
CO2 ADP
CoA
− [H] GDP

Oxaloacetate Pyruvate Succinate
NADH NAD+ ATP
NADH ADP Fig. 17.3 The malate dismutation reaction in the
mitochondria of the nematode Ascaris lumbricoides.
NAD+ Fumarate Note the principal stage resulting in ATP generation
(between fumarate and succinate), together with
Malate Malate three other possible ATP- or GTP-generating stages
(marked with ?). PEP, phosphoenolpyruvate.
Mitochondrial (Adapted from Trager 1986.)
outer membrane

many other parasites the fumarate, succinate, and pyruvate are usu- 3 Oxaloacetate is rapidly metabolized by the enzyme malate dehy-
ally further metabolized to propionate, acetate, and volatile fatty drogenase, favoring further CO2 fixation by the PEP carboxykinase.
acids such as 2-methylvalerate and 2-methylbutyrate.
Similar transitions in energy metabolism between life-cycle stages
Energy is thought to be stored in ATP at several stages in the dis- are seen in other parasites. Schistosoma mansoni has two free-living
mutation reaction. The best known ATP generation point is during larval stages, the miracidium that locates the snail intermediate
the electron transfer chain in the reduction route. The enzyme host, and the cercaria that penetrates the human host. Cercariae are
fumarate reductase, which converts fumarate to succinate, is definitely aerobic, and miracidia are probably so, but the adults rely
coupled to an electron transfer system in the mitochondrial inner to a large extent on anaerobic respiration, even in the presence of
membrane, phosphorylating ADP to ATP. This is the major known oxygen. In contrast to the metabolic pathways used by adult Ascaris,
energy storage reaction in Ascaris. Three other possible stages at schistosome adults generate lactic acid in much the same way as
which ATP is generated are also indicated in Fig. 17.3. The endpoint anaerobically functioning invertebrates described in Chapter 6,
of the metabolism of malate is the fatty acid 2-methylbutyrate. In yielding only two molecules of ATP per molecule of glucose. The
contrast to the 36–38 ATP molecules generated from a single glucose same energy-storage system is also important in filarial nematodes.
molecule in traditional aerobic metabolism, the Ascaris mechan- Thus across parasites as a whole, a range of end-products of anaer-
ism generates between three (two in glycolysis, one additionally obic glycolysis are found, most yielding only 2 ATP per molecule
in the mitochondrion) and five (if the additional ATP-generation of glucose (Table 17.2).
steps in the mitochondrion actually occur).
17.3.4 Feeding
This pathway is unusual in the role played by PEP carboxykinase,
which differs radically from its usual role in animals. In mammals Parasite feeding strategies can be broadly divided into two very
this enzyme is present in the liver, and is involved in the manu- different types:
facture of glucose from lactic acid (gluconeogenesis; see Chapter 6). 1 Parasites feeding on host tissues and fluids via the mouth. This
In contrast to the carbon fixation seen in Ascaris, in mammals the category includes those feeding on blood or hemolymph, and on
enzyme catalyzes the same reaction but in the opposite direction! In host exudates such as mucus on the skin.
effect the animal is using the second span of the tricarboxylic acid 2 Parasites absorbing nutrients from host body fluids or gut con-
cycle, from succinate to oxaloacetate, but operating in the reverse tents, across their body wall.
direction. It has what has been described as a partial, reversed tricar-
boxylic acid cycle. How is this reversal achieved? Three aspects of Feeding via the mouth
the situation in Ascaris favor this kind of CO2 fixation:
1 Levels of the substrate PEP are far higher in Ascaris tissues than Where the parasite takes in food via the mouth, it is possible for the
they are in mammalian tissues; pyruvate kinase, which normally parasite’s body to be enclosed in a cuticle or sheath that is metabolic-
breaks PEP down, is present only in very low concentrations in ally relatively inactive, conferring protection against attack by host
Ascaris. immune responses or digestive enzymes. Most nematodes, for
2 Ascaris PEP carboxykinase has a seven-fold higher Km (i.e. lower example, feed via the mouth and have metabolically inactive cuticles
affinity) for oxaloacetate than for PEP.

PARASITIC HABITATS 685

Table 17.2 Pathways used in parasite anaerobic Respiration type End-product mol ATP generated Organism
respiration. per mol glucose
Aerobic CO2, H2O Almost all aerobes
Anaerobic Lactic acid 36 Very common; e.g. Schistosoma
2
Anaerobic Ethanol mansoni, filarial nematodes
Anaerobic Alanine 2 Some helminths
Anaerobic Acetate + succinate 2 Many invertebrates
Anaerobic Acetate + propionate 3.7 Many helminths
Anaerobic Acetate + propionate, 5.4 Many helminths
2–5 Some nematodes, e.g.
methylbutyrate,
methylvalerate Ascaris lumbricoides,
Hymenolepis diminuta

that are thick and multilayered. The same is true of many blood- Direct absorption across cuticles
feeding ectoparasites, whose outer body layers must protect them
from conditions in the external environment. The mouthparts of all Where direct absorption occurs, the outer tissues of the parasite
blood feeders need to be modified for attachment and/or suction are typically highly metabolically active, and experience rapid fluxes
(Fig. 17.4). of nutrients, ions, and water; it is not possible for the parasite to
isolate itself from the host by a barrier layer. Direct absorption of
To generalize, the main problems for this group, and hence the host nutrients across the body wall is found in a wide diversity of
principal feeding adaptations found in members of this group, are parasites, particularly among the platyhelminths. It is also found
three-fold: in acanthocephalan worms, in the first larval stage of some insect
1 coping with large volumes of fluid. endoparasitoids, and in a small number of highly specialized
2 Coping with the metabolic breakdown products of blood (par- nematodes.
ticularly iron).
3 Coping with possible blood-borne infective agents such as Parasitic platyhelminth teguments consist of several layers
bacteria. (Fig. 17.5a,b). The outer layer is composed of syncytial living tissue,
the nuclei lying more centrally within the animal below layers of cir-
Many parasites from a diversity of animal groups feed on blood, cular and longitudinal muscle. The outer surface of the tegument is
including platyhelminths (monogeneans and trematodes), nema- covered in a thin glycocalyx of mucopolysaccharides and glycopro-
todes, leeches, crustacean fish-lice, arachnids such as ticks, and teins. This layer has a net negative charge, and is able to bind both
insects such as lice, fleas, mosquitoes, and tsetse flies. Problems may inorganic and organic charged molecules, including host enzymes.
result from very intermittent meals of large volume; adaptations These may then be used to digest surrounding food material, which
are best known in leeches and in biting insects, where in both is absorbed by the parasite. The surface area of the tegument is
cases diuretic elimination of water is initiated by hormones (often enlarged (by up to 10 times) by microvilli (called microtriches in the
triggered by body-wall stretch receptors) to promote very rapid case of cestodes), which are particularly well developed in cestode
fluid loss after a meal. Initial blood digestion occurs in response tapeworms (Fig. 17.5b) and are presumably adaptations for large-
to enzymes released by pharyngeal or “salivary” glands. Homogene- scale secretion and absorption across the tegument. The outer sur-
ous acellular products of this digestion, including hemoglobin, are face of acanthocephalan worms also has an enlarged surface area
usually digested intracellularly. Iron is discarded back into the gut (Fig. 17.5c), in this case through high densities of surface pores,
lumen by exocytosis and shed with the normal feces, or in the case of which lead to blind-ending spaces (“crypts”), enlarging the surface
schistosomes iron-rich waste products are voided by regurgitation area by about 60-fold. The nematodes that absorb nutrients across
(flukes usually have a blind-ending gut, with no anus). To cope with their body wall lack the usual thick and nonabsorptive cuticle, and
the third problem, it is known that antibacterial peptides are upreg- develop microvilli all over their surface, through which it is assumed
ulated in response to ingestion of a blood meal in the blood-feeding nutrient absorption takes place.
fly Stomoxys calcitrans, and such a system may be widespread.
The major physiological adaptations in nutrition are associated
Some parasites with normal guts and mouths that could feed on with digestion and absorption of host material, both inside and
blood or other tissues nevertheless use the skin as an uptake sur- often also immediately outside the parasite’s body, while protecting
face for key nutrients. For example, the monogenean Diclidophora the same tissues from attack by host defenses. Cestodes and acan-
merlangi feeds mainly on blood, but supplements its diet by the thocephalans especially are in competition with their hosts for
absorption of amino acids through its outer tegument. nutrients in the gut lumen. If they are to compete successfully for
these, their ability to bind and absorb nutrients must be at least as
Most parasites can use their metabolic pathways to synthesize the good as or better than the host’s. Adult cestodes, for example, are
majority of the amino acids they require, often by the described able to absorb all detectable glucose from their surrounding
routes relating to carbon dioxide fixation, and most can synthesize medium, indicating a very high-affinity (low Km) active uptake for
pyrimidines; but few if any can manufacture the purine ring, which this compound.
must be obtained from the host. Salvage pathways therefore exist in
many parasites to allow recycling of certain host molecules from the Living in the gut clearly has real hazards, and gut parasites show a
blood before they are broken down in normal catabolic paths.