686 CHAPTER 17
(a) (b)
Antennule Spine
Antenna Eye
Maxillule
Maxilla Compound Labrum
eye epipharynx
First
thoracic limb Maxillary Food channel
palp Hypopharynx
Salivary duct
Labium Mandible
Antenna
Maxilla
Maxilla Labrum
epipharynx
Abdomen Mandible
Hypopharynx
Labella
(c) (d)
Fig. 17.4 Mouthparts of blood-feeding parasites. (a) The proboscis of an spread out of their natural alignment; to the right are the components in their
acanthocephalan worm. (b) The spiny head collar of the nematode Gnathostoma, functioning arrangement. (a, From Matthews 1998, photograph courtesy of H.
with the mouth at the center. (c) Ventral view of a crustacean fish louse, where Melhorn; b, from Matthews 1998, photograph courtesy of L. Gibbons, CAB
the enlarged maxillules (limbs modified for feeding) hold the parasite to the fish’s International; c, adapted from Kaestner 1980; d, from Brusca & Brusca 1990.)
skin by suction. (d) Piercing mouthparts of a mosquito, with the components
Digenea Microtriches PARASITIC HABITATS 687
Outer body surface
Mitochondrion Cestoda
Pinocytotic Basement Vacuole
vesicle membrane
Circular Syncytial
Mitochondria muscle zone
Spine
Longitudinal Cytoplasmic
Basement muscle extension
membrane
Main body of Nucleus
Circular tegumental cell Mitochondrion
muscle
Longitudinal (b) Striped
muscle Pore layer
Mitochondria
Nucleus
(a)
Acanthocephala
Crypt Felt-fiber
Fiber layer
Lacunar Radial
canal layer
Fig. 17.5 Highly modified cuticles in gut parasites: (a) tegument of a digenean (c)
fluke, (b) tegument of a cestode tapeworm, and (c) cuticle of an acanthocephalan
worm, showing internal crypts. (Adapted from Matthews 1998.)
variety of tricks to enhance their own competitive success. Many gut sitoids may disrupt host absorption of materials from the hemo-
parasites coat themselves in mucus, which is a good ion-binding lymph, which increases resource availability for themselves.
matrix, to limit the effects of extreme pH in the host gut. Some
intestinal parasites inhibit digestive activity of the hosts and indir- Many parasites secrete enzymes associated with feeding. A
ectly inhibit vitamin and blood-sugar metabolism. For example, number of gut-inhabiting parasites are able to reduce the risk of
the tapeworm Diphyllobothrium latum has very high affinity for digestion by their host by releasing “antienzymes”acompounds that
vitamin B12, and can cause deficiency disease (pernicious anaemia) neutralize the host enzymes. Survival may also be augmented by the
in humans. In the nematode Nippostrongylus, adults secrete large tolerance of high levels of toxic compounds, as illustrated by tape-
quantities of acetylcholinesterase from their excretory pore, perhaps worms in the guts of rabbits. Rabbit bile contains very high levels of
to produce local inhibition of peristaltic activity in the host gut deoxycholic acid: 36 mg ml−1, in comparison with 1.77 mg ml−1
(which will also help prevent them being dislodged). Insect para- in dog bile. Rabbit gut parasites that live below the point where the
bile duct enters the intestine are able to cope with this level of
688 CHAPTER 17
deoxycholic acid, while larvae of the dog tapeworm, Echinococcus some show daily migrations in the host blood system that enable
granulosus (which lives in a similar position in dogs), are destroyed them to make use of blood-feeding insect vectors. Third, and most
by the bile acid concentrations found in rabbits. elegantly, parasites that reach their definitive host by moving up a
food chain are sometimes able to manipulate the behavior of their
17.4 Reproduction and transmission intermediate host such that they are more likely to be eaten.
17.4.1 Goals and challenges of transmission 17.4.2 Movement between hosts
All hosts have a finite lifetime, and the long-term survival of para- Reinfection requires that a suitable host is located, and usually a
sites requires the transmission of infective stages from one host to specific part of the host’s body. In cases where the parasite habitat
another. In marine and freshwater environments, transmission is essentially external, the movement of individual adults or larvae
between hosts can take place, as we have seen, via ciliated free-living through the medium may be possible. In marine ectoparasitic platy-
larval stages or (in the case of ectoparasites in particular) by direct helminths such as flukes, the detection and settling of larvae on
adult migration. In many cases larval dispersal is passive, without host external surfaces is analogous to detection of settling sites by
direct attraction to the hosts, although larvae may concentrate in the planktonic larvae of many other marine organisms. In many
areas more often visited by the host. An example is larval concentra- endoparasites, the situation is rather more complicated. Reinfection
tion in surface waters at times when intermediate hosts feed. involves not only the release of eggs or larvae from adults that
may be located deep within host tissues, but also the subsequent
The situation is quite different in terrestrial habitats. Adult re-entering of hosts. This is achieved via the mouth and digestive
tapeworms, nematodes, and other parasitic worms, though able to tract, or via the host’s skin. In the latter case, location of the adult
locomote and survive in very moist terrestrial habitats, are unable to site in the host usually also involves highly complex larval migra-
survive outside the host in drier environments. Movement from one tion through the host’s body.
host to another thus cannot be direct. However, direct transmission
is often possible for ectoparasites with a more recent terrestrial free- The physiological tolerances of particular parasite groups have a
living ancestry, such as biting flies, fleas, or ticks. Endoparasites are major bearing on the infection routes possible for free-living adults
generally unable to survive as adults in terrestrial habitats and rely or larvae. Adults and larvae of many parasites can survive in aquatic
on resistant eggs and/or larvae released from the host to achieve environments but are less tolerant of terrestrial ones. In platy-
infection of further hosts. One parasitic strategy is to produce long- helminth parasites in particular, infection by free-living life stages
lived, desiccation-resistant eggs that are released into the environ- tends to take place only when the host is aquatic or is a terrestrial
ment in large numbers and are taken up by the same host species animal that intermittently comes to water (as in the life cycle of
(usually via the mouth). The host occupied by the adult parasite Schistosoma). Some platyhelminth adults can survive for short
(usually termed the definitive host) may be extremely patchily dis- periods outside the host, even in terrestrial environments. For
tributed in the environment, making the possibility of direct infec- example, adults of cestode tapeworms release their eggs packed into
tion of another host very low. Some parasites have evolved life cycles reproductive segments called proglottids. These leave the host with
that exploit an intermediate host species, usually one that is more the feces and can survive and disperse eggs for a while outside the
abundant in the larval environment than the definitive host. Many host. Even large proglottids, however, probably do not disperse far.
parasitic life cycles include asexual reproduction by larvae in the Nematodes are better able to survive in free-living terrestrial envir-
intermediate host, increasing the probability that at least one larva onments, and several serious parasites of humans have larvae that
will successfully reach either a further intermediate host or the spend time in the soil. In the case of the nematode hookworms
definitive host. In many life cycles, the intermediate host is a prey Necator americanus and Ancyclostoma duodenale, the parasite life
item for the next intermediate host or the definitive host, so that cycles include free-living larval stages that actually feed on bacteria
the limited ability of the parasite to move between hosts is vastly in the soil (Fig. 17.6). Dispersal by larvae in terrestrial environments
enhanced by the ability of a predator to detect and locomote towards can also be achieved if they are collected from one host and deliv-
its prey. The same advantage applies for parasites transmitted by ered to another without exposure to the external environment. A
vectors. For endoparasites such as tapeworms that infect terrestrial number of parasites (particularly nematodes) survive by being
hosts, complex life cycles of this type can be seen as a necessary con- spread via blood-feeding vectors, notably insects and ticks. Parasite
sequence of the limited ability of the parasite to survive and loco- larvae enter the vector as it feeds from one host, and (sometimes
mote on land. What a blood-feeding tsetse fly (Glossina morsitans) after intermediate larval stages) enter the next host as the vector
can achieve by flying between two cattle, a tapeworm must achieve feeds again.
by apparently tortuous and indirect means.
The alternative to free-swimming larvae or adults is the use of
Parasite environmental physiology shows adaptations associated eggs or larvae that are protected from environmental conditions
with several steps in the transmission process. Firstly, there are para- by egg shells or other structures. Parasite eggs leave the host either
site traits associated with different methods of movement between through a natural aperture (most often with host feces), or through
hosts. These include adaptations to particular environments, and a hole in the host’s body wall induced by the parasite, as in the
the dramatic changes that often take place when moving from one nematode commonly known as the guinea worm, Dracunculus
to the other. Secondly, a number of parasites have evolved mechan- medinensis, or the jigger flea, Tunga penetrans. Once released, these
isms allowing reproductive synchronization with their host, and resistant stages are unable to locomote themselves, but there is a
probability that if they survive long enough they may encounter
PARASITIC HABITATS 689
In human Via trachea and pharynx to intestine,
about 2 days after infection
Via lymphatics
and heart to lungs Molt to
stage IV
in lungs
Final molt
to adult stage
Infective stage III Adult and attach
filariform larva to intestinal wall and
penetrates skin mature (about 5 days
after infection)
Can survive only
a few days
Stage III larvae are Eggs passed
negatively geotropic. with feces
Respond to warmth
Rhabditiform larvae
feed on bacteria
Fig. 17.6 Life cycle of the hookworm nematode Molt twice in Eggs hatch in
Necator americanus. (From Trager 1986.) about 5 days about 2 days
In soil
another host. Sometimes the larva is dispersive for a while, but plex and permanent attachments to the host. This is the case with
forms a resistant cyst before reaching the limits of its environmental many monogeneans that grow into the tissues of fish gills.
tolerance. Here the liver fluke Fasciola hepatica is a good example;
its life cycle is similar to that of Schistosoma, except that the cercaria Free-swimming larvae are found in many parasitic groups, par-
larvae do not actively bore through the skin of their definitive host ticularly the platyhelminths. The longevity, and sensory and loco-
(a ruminant mammal). Instead, they form resistant cysts on grass motory abilities, of platyhelminth larvae are relatively limited, and
leaves, and rely on the ruminants to eat them. Dispersive stages of this without the direct inoculation of another host by a vector, only a
type typically maintain a very low metabolic rate, are very desicca- tiny proportion reach the next host in the life cycle. Host location by
tion resistant, and able to survive unfavorable osmotic conditions free-swimming larvae involves two general steps. First, responses to
for long periods. Eggs of the gut nematode Ascaris possess a lipid general stimuli such as light or gravity allow the larvae to concen-
layer inside the egg shell that is extremely impermeable to both trate in regions of the environment where contact with the next host
water loss from the egg and entry of other chemicals from the exter- has a better than random probability. For example, larvae of flukes
nal environment. In some nematodes, the dispersive stage is a larva that attack bottom-living fish tend to stay near the bottom, while
that resists desiccation rather differently, by retaining the cuticle of a species attacking surface-swimming fish are positively phototropic
previous molt as an extra layer around the worm. These adaptations and maintain themselves in upper water layers. Second, responses
clearly parallel those seen in other essentially aquatic Metazoaasuch to characteristic host cues stimulate egg hatching, larval orientation,
as rotifers, tardigrades, and many free-living nematodesathat dis- and attachment behaviors. Thus in the monogenean Entobdella
perse through terrestrial environments using a cryptobiotic stage soleae, the sole fluke, which parasitizes a bottom-living fish, eggs
(see Chapter 14) between phases in aquatic habitats. hatch in response to urea in the mucus of the host’s skin, and detec-
tion of this cue stimulates the release of a proteolytic hatching fluid
Infection by free-living adults or larvae and emergence of the larva. The larvae show a diurnal rhythm in
their hatching activity, which peaks during the middle of the day
In aquatic ectoparasites, dispersal by free-swimming adults is when their hosts are lying inactive and accessible. Having located a
possible. The adult must already be able to tolerate conditions host, the larvae use adhesive glandular secretions to maintain contact
experienced in the external environment, and needs only to be able until the main attachment organ (the hook-bearing opisthaptor)
to release its attachment to one host and then locate another. This is can be applied to the fish’s skin.
certainly possible for some monogenean flukes, but is probably
impossible for many species that, though ectoparasitic, form com- The situation becomes more complex in endoparasites, many of
which have complex life cycles. The miracidium larvae of schis-
tosomes (see Fig. 17.1) locate the intermediate snail host, and the
690 CHAPTER 17
Carapace of Y-shaped cuticular Incipient
cyprid rod in base of antennule kentrogon
Invasion cell Naupliar eye
Antennules 10 min
0 min
Gill filament
of host
(a) (b)
Kentrogon
Invasion
cell
15 min Antennular 25 min
article 2
100 µm
(c) (d)
Anterior Fig. 17.7 Rapid body reorganization during
cuticular shield host infection in the rhizocephalan barnacle
Lernaeodiscus porcellanae. (a–d) The free-swimming
cyprid larva locates and settles on the gills of its host,
a crab, attaching by secretions from a large cement
gland. Within 25 min the cyprid larval body is
1h Cement 10 h 15 h extensively reorganized, forming a sac-like structure
termed the kentrogon. Then the carapace of the
Invasion Injection cyprid is shed. (e) The kentrogon develops a stylet,
cell stylet and injects a specialized “invasion cell” into the crab
(e) between 40 and 60 h after attachment; this divides to
20 h 40 h Injection provide a network of parasite tissues, more similar
stylet 60 h to a fungus in structure than to a typical crustacean.
(Adapted from Brusca & Brusca 1990.)
cercaria larvae re-enter the definitive host. There is a dramatic and place help to soften the outer layers of the host’s skin. Once the larva
rapid reorganization of the larval body on entering a host from the has gained entry into a small break in the host’s skin, proteolytic
free-living aquatic environment. In the case of the schistosome trans- secretions break down the host cells and allow the larva to move
itions a motile outer layer (ciliated in the miracidium, and smooth inwards. Then the larva undergoes a dramatic transformation into
with a muscular swimming tail attached in the cercaria) is rapidly the next larval stage, the schistosomula; the free-swimming cuticle
shed to leave a new outer layer. An even more extreme example is and tail are shed (Fig. 17.8c), leaving the highly specialized absorp-
shown in Fig. 17.7 for Lernaeodiscus porcellanae, a rhizocephalan tive outer covering (tegument) characteristic of the adult. While the
barnacle that is parasitic on crabs. body wall of the cercaria was relatively impermeable, though prob-
ably with salt uptake regions to maintain larval metabolism in the
In life cycles involving more than one host, stage-specific host hyposmotic freshwater environment, the new tegument is a perme-
location behaviors and recognition cues must be used. Larval recog- able surface through which all metabolic exchange with the host takes
nition of the host is normally only effective over short distances, and place for the rest of the parasite’s life. An important early function of
for schistosomes it involves movement up a temperature gradient, the tegument is the rapid acquisition of host surface antigens, ren-
and response to lipids characteristic of the host skin. Once contact is dering the parasite invisible to the host immune system (see below).
made, the cercaria uses secretions from two specialized acetabular
glands whose ducts open into an anterior sucker (Fig. 17.8). Secre- Infection by free-living larvae in nonaquatic terrestrial environ-
tions from these glands are sticky, and while holding the larva in ments is less common. In the nematode parasites of mammals that
PARASITIC HABITATS 691
Postacetabular glands
Preacetabular glands
Gland ducts
(a)
(b)
Fig. 17.8 Penetration of human skin by a cercaria (c) (d)
larva of Schistosoma: (a) enlargement of anterior
portion of a cercaria, showing glands and ducts;
(b) adhesion to, and penetration of, the skin surface;
(c) shedding of the larval tail; (d) migration of the
metamorphosed schistosomula larva into deeper
tissues and then to the human’s circulation.
(Adapted from Matthews 1998.)
have free-living larvae surviving and feeding in the soil, infection of nematode Wuchereria bancrofti. The vector exploited by the parasite
a host is preceded by a molt to a nonfeeding stage, which must locate varies geographically, and parasites emerge in the peripheral circu-
a host within a few days. Host location is brought about by negative lation at the right time for their local vector. Thus numbers of
geotropism (keeping the larvae at the soil surface) and by rapid move- Wuchereria microfilariae just beneath the skin peak during the night
ment towards a source of warmth. Once contact is made, the filariae in regions where the main vectors are night-biting Culex and
of the nematode hookworm Necator americanus also bore through Anopheles species, and during the day where the main vector is the
the skin of their vertebrate host, using proteolytic secretions from day-biting Aedes. The parasites must detect some stimulus in the
their esophageal glands to break down host cells in their path. host metabolic cycle that has a daily rhythm, and experimental
confirmation of this comes from studies of Wuchereria filarial
Vector-mediated parasites migrations in people working night shifts, with biorhythms 12 h out
of phase in comparison with the normal human cycle, who show
In a sense, parasites utilizing vectors avoid some of the problems filarial migrations that are 12 h out of phase with filariae in people
associated with entering the external environment. They do not working day shifts (unfortunately for the parasites, this results in
need sense organs to find the next host, since the vector does that for larval presence in the peripheral host blood system at a time when
them, and they are not exposed to the risks of desiccation. However, their mosquito vectors are not active).
they encounter other challenges. First, the larvae must reach a part
of their host in which they become accessible to their vector. For In addition to getting the timing right, vector-borne parasites
parasites occupying internal tissues, this requires migration towards must also be present in the blood in an area of the body favored by
the host body surface in the peripheral circulation. Although this their vector. Onchocerca is another nematode parasite of humans,
brings the parasites to within reach of the mouthparts of blood- being the agent of the disease river blindness. It is transmitted by
sucking vectors, traveling in the bloodstream may expose the para- several species of biting blackflies that show species-specific prefer-
site larvae to intensified host defense. A partial solution to this ences for biting particular parts of human hosts. Thus the nematode
problem is for the parasite to show a very brief and precisely timed larvae aggregate in the legs in regions where their vector prefer-
diurnal migration between the deeper tissues and the blood vessels entially bites legs, and in the upper body when this region of the host
just beneath the skin, as observed for the microfilariae of the is preferred. This clearly requires very specific larval detection ofa
and response toahost stimuli.
692 CHAPTER 17
% of population 30 Paramucosal species Luminal species
0
30 T. uncinata T. numidica Fig. 17.9 Distribution of nematode species of the
0 T. microstoma T. macrolaimus genus Tachygonetria in the intestine of the Greek
30 T. robusta T. dentata tortoise. The eight species are divided into two
0 T. stylosa T. conica groups: (a) those living close to the gut wall
(paramucosal) and (b) those inhabiting the lumen
30 (b) of the gut. For each group, the distribution of the
0 parasites along the intestine is shown from left to
30 right. (Adapted from Schad 1963.)
(a)
A second set of challenges involves parasite responses to the the emergence of larvae can be divided into two types. First, some
environments present in the vector. Vector-transmitted parasites stimuli indicate that the infective stage has passed unsuitable
are initially swallowed into the gut of the vector, and thence move to regions of the gut; thus the emergence of several intestinal parasites
the blood and on into the tissues. Survival requires parasite resist- is initiated by low pH, characteristic of the host stomach, although
ance to host digestive processes, and defenses in host tissues, which hatching does not progress further until more favorable conditions
are extensive even in invertebrates (see below). Eventually (some- are reached. Second, some stimuli indicate more directly that the
times after intermediate larval stages) the larvae reach the vector’s egg or larva has reached the right part of the gut for hatching or
salivary glands or proboscis, and are reinjected into another host. metamorphosis. For example, the increase in temperature asso-
This requires the parasite to cope with three very different vector ciated with entry into an endothermic host provides a very simple
environments, often within a very short timeframe. trigger for a few parasites. Alternatively, conditions in the host gut
may stimulate secretion of enzymes by the egg or larva, leading
Reinfection via the gut to rupturing of the egg/cyst wall. Ascaris eggs hatch in response to a
critical concentration of CO2, an appropriate pH (slightly alkaline;
Infection via the gut typically involves eggs or encysted larvae that see Fig. 17.11) and a high temperature (close to 37°C). Within the
emerge in response to the conditions in a certain part of the host gut. eggs, larvae release lipase and chitinase, and the lipid-rich inner
Protective coats around the egg or larva, coupled with relatively layer of the egg shell increases in permeability. The enzymes diffuse
specific hatching or excysting stimuli, allow the parasite to reach the through and dissolve a small area, through which the larva emerges.
appropriate part of the host gut without being digested on the way. As another option, digestive enzymes present in the host gut
Protective coats include egg shells, cysts formed by larvae, and larval may break down the egg/cyst wall; here examples are provided by
sheaths in some nematodes. They also include cases where the larva hatching of the eggs of tapeworms, and excystment of digeneans
is surrounded by tissue laid down by an intermediate host. In the and cestodes. Host enzymes remove the outer layers of the egg or
tapeworm Taenia solium, the cysticercus larvae are surrounded by cyst, and then bile causes changes in the permeability of the remain-
cysts of pig tissue in the muscles, and emergence is triggered when ing membranes.
the flesh of the pig is consumed and then digested by the human
definitive host. 17.5 Parasite sensory abilities
A wide range of stimuli are known to trigger emergence from It is usually suggested that in comparison with their free-living relat-
eggs or cysts in the gut. Generally, stimuli in invertebrate hosts ives, many parasites have reduced sense organsaparticularly those
are less specific than those in vertebrates, even where these are both associated with stimuli absent from the interior of a host’s body,
present in the same parasite life cycle. For reasons that are not such as light. This is true of some parasites, such as the rhizocephalan
always obvious, gut parasites usually occupy a relatively specific barnacle Sacculina. This parasite, which in the adult stage looks
position in the host’s alimentary canal (Fig. 17.9). This may repres- nothing like a barnacle and quite like a mushroom, forms a network
ent the region of the gut in which resistance to host defenses and of tissue within the body of its crab host, extending externally as a
levels of nutrient acquisition are optimum for a given parasite. formless mass of tissue beneath the crab’s abdomen. Unlike the free-
Host guts show characteristic gradients in chemical and physical living barnacles from which it is derived, the adult Sacculina lacks
conditions along their lengths (Fig. 17.10), and there may be triggers obvious sense organs.
corresponding to particular combinations of conditions that allow
parasites to emerge at the correct position. Conditions required for
PARASITIC HABITATS 693
120 2000 8 300
7 250
100 Electrolyte (mEq) Chloride 1800 6 200 Osmotic pressure (mOsm)
Sodium 1600 5 150
80 1400 4 100
Water (ml) 3 50
60 Water 1200 pH 2 0
1000 1 9 10
40 0
800 pH
20 012 mOsm
600 (b) Stomach
0 4 5 6 78
0 400
(a) 200
1 23 4 567 8 0 12 3
9 10 Intestine
Distance along intestine
30
Glucose (mg per 100 g body wt 30 min 25 0
after feeding 1 g in 2.5 ml water)
Bile salt concentration (mOsm) 25 Glucose –20 Oxidation/reduction potential (mV)
20 Eh –40
20
–60
15 15 –80
–100
10
10 –120
5 5 –140
–160
0 0 –180
Liver 1 2 3 4 5 6 7 8 9 10 123456 78
bile
(c) Distance along intestine (d) Distance along intestine
Fig. 17.10 Gradients in conditions along the mammalian gut, for: (a) water and It could be that parasites infect hosts at random, but die in the
salts; (b) pH and osmotic pressure; (c) bile salts; and (d) glucose and redox “wrong” hosts, or in the wrong part of the right hostagenerating
potential (Eh). (From Matthews 1998.) specificity without sensory selection of hosts by the parasite. Altern-
atively, parasites could possess sense organs allowing specific selec-
However, to extend the example of Sacculina over all parasites tion and rejection of alternative hosts and sites. Site recognition
may be unwise. Many parasites are able to successfully locate hosts could in part be attributed to a small number of highly specific
as larvae, and furthermore to locate amazingly specific microhabitats recognition cues, perhaps mediated by recognition of specific host
within their hosts. Within the human blood system, young larvae cell types at a molecular level. Detailed studies are now revealing
of Schistosoma are able to recognize and congregate in the hepatic that parasite sense organs and nervous systems are far more com-
portal vein, while other flukes are able to migrate to a wide diversity plex than previously appreciated. Superficially simple endoparasites
of highly specific sites in other parts of the body, including the brain, such as trematodes and nematodes have highly complex sensory
heart, and bladder. systems. As an example, adults of the marine aspidogastrid fluke
Lobatosoma manteri have a probable total of 20,000–40,000 sur-
% Hatch 80 face sensory receptors of at least 14 different types. Such a complex
70 sensory system may be required to monitor the physiology of the
60 6.5 7 7.5 8 host, and to prevent overexploitation leading to host death (and so
50 pH parasite death).
40
30 The ability of parasites to find such specific locations in their
20 hosts suggests an ability (across a range of parasite species) to detect
10 extremely precise combinations of pH, osmotic concentration,
0 oxygen tension, patterns of fluid pressure in water currents, and
temperature. In addition, the exploitation of different habitats
6 through the life cycle also implies that different subsets of receptors
or activation thresholds for given behaviors are present in different
Fig. 17.11 The pH sensitivity of hatching by eggs of the gut nematode Ascaris life-cycle stages. Remember also that parasite behaviors are often
lumbricoides. (From Matthews 1998.) very flexible, and able to take into account variations in the para-
site’s environment. Thus the adults of a number of intestinal worms
are able to adjust their location in the gut in response to the digestive
694 CHAPTER 17
cycle of their host, while others adjust their spatial patterning in the for the parasite. The scale of the manipulation can range from a
host in response to whether it is well fed or fasting. These alterations small area of host tissue immediately around the parasite to re-
of position again suggest a sophisticated ability to detect and organization of the host’s entire body. The mechanism of parasite
respond to changes in environmental stimuli. modification is rarely known, but in at least some cases it is through
active secretion of chemical signals.
17.6 Parasite regulation of host physiology
17.6.1 Modification of host tissue growth
Parasite manipulation of the way hosts invest their resources is
widespread, and is thought to result in greater resource availability On the most local scale, parasites may modify the physiology and
development of individual cells. The nematode Trichinella spiralis
Fig. 17.12 Galls formed by cynipid gall-wasps. (a) Longitudinal section through is able to transform individual cells in the muscles of its pig host:
a gall induced on a rose, showing the larva (La) in its hollow cell (LC), and the secretory/excretory products of the worm transform muscle cells
surrounding plant tissue layers on which the larva feeds (C, outer plant tissues; into nurse cells, probably through direct modulation of host
NT, nutritive tissue; PNT, parenchymatous nutritive tissue; VT, vascular tissue genomic expression.
supplying the gall). (b–f ) Examples of galls induced on oak trees by gall-wasps:
(b) Neuroterus quercus baccarum, (c) Andricus aestivalis, (d) A. quercus tozae, Some of the clearest examples of parasite control of host tissue dif-
(e) A. coronatus, (f ) A. tomentosa. (a, From Brooks & Shorthouse 1998.) ferentiation come from insects that form galls in plants (Fig. 17.12).
Galls are plant tissues induced by another organism, providing that
(b) (c)
(e)
(a) (d) (f)
PARASITIC HABITATS 695
organism with food and a measure of physical protection (see hormone (see Chapter 10), causing infected mice to reach a spectacu-
Chapter 15). Typically, galls consist of nutritive inner tissues, on lar size.
which the galling organisms feed, and outer tissues that are often
hardened. The gall-forming organism is often able to induce the Some parasites are also able to prevent molting in their host, for
plant to produce abnormal cell types and structures, and to direct example in crabs infected by Sacculina. Suppression of molting is
resources such as nitrogen preferentially to the gall tissues. A group required because the parasite has external parts that disrupt the
of small wasps (commonly termed gall-wasps, in the hymenopteran usual form of its host’s exoskeleton, and an attempt to molt would
family Cynipidae) induce the most structurally complex and diverse probably kill both host and parasite. In other cases, the suppression
galls known. At the center of the gall is a layer of endosperm-like of host molting maintains feeding and growth by a particular host
tissue on which the gall-wasp larva browses. A series of outer tissue life-cycle stage attacked by the parasite, so enhancing parasite
layers give the gall of each species a characteristic form, and show a growth.
wide diversity across gall-wasp species, including layers of woody or
spongy tissue, complex air spaces within the gall, and surface coats The clearest examples of this type of host manipulation are to
of sticky resins, hairs, or spines. It is thought that these outer tissues be found among insect parasitoids, representing a special case of
protect the gall-former from attack by insect parasites and verte- parasitism in which the parasite always kills the host. Idiobiont
brate predators. In addition to physical protection, gall tissues are parasitoids kill or paralyze their host at the time of egg laying, and no
often rich in toxic secondary plant compounds (see Chapter 15). further host growth takes place. Koinobiont parasitoids represent
Some oak-feeding gall-wasps are even able to induce oak tissues to a more subtle strategy in which the parasite allows the host to con-
secrete a sucrose-rich nectar, attracting ants to the surface of the tinue to develop after egg laying; parasitoid larvae avoid damaging
gall, which further protects the gall-wasp from insect enemies. organs essential to host survival and growth, and may also mani-
pulate the host’s endocrine physiology, nutritional biochemistry,
17.6.2 Modification of host reproduction and life cycles and/or behavior. The eggs or larvae of koinobiont parasitoids typ-
ically delay their own development until the host reaches a large
Rather than initiating the development of novel tissues, parasites size, and may also prolong the life cycle of the host, both strategies
may prolong existing phases of the host’s life cycle to favor their own resulting in greater resource availability for the growing parasite.
development. One way of diverting resources into parasite growth is For example, the parasitoid Cotesia congregatus is able to prevent the
to suppress sexual maturation of the host, such that host resources larva of its caterpillar host Manduca sexta (the tobacco hornworm)
are never directed into eggs or sperm. This occurs in chaetognaths from metamorphosing into a pupa, and can induce up to six extra
and snails infected with trematode larvae, and in crabs infected by host larval instars. Metamorphosis of the host is usually brought
Sacculina. In the snail case, trematode larvae interfere with the about by a drop in the levels of juvenile hormone and an increase in
endocrine control of host development, by causing the host snail’s the level of ecdysone in the host’s hemolymph. Parasitoid larvae are
central nervous system to manufacture a protein (“schistosomin”) able to prevent the drop in levels of juvenile hormone, and some
that interferes with several of the snail’s usual hormones involved in may also block the conversion of inactive ecdysone into the active
the control of egg development. A vertebrate example is given by 20-hydroxyecdysone. However, it is worth noting that delay in para-
tapeworm larvae that suppress sexual behavior and egg maturation sitoid development as the host grows may come with a cost; most
in many fish, probably by preventing the production of the host’s koinobiont insect parasitoids are endoparasites, and they are thus
gonadotropic hormones. exposed to host defenses for rather longer.
Sometimes the parasite does not completely inhibit reproduc- Synchronization between host and parasite life cycles is also
tion, but inhibits or delays it. For example, male hamsters infected an option that many parasites exploit, insuring that parasite young
by schistosomes show decreased testosterone levels and so reduced are produced at the same time as host young. Molting in insect
investment in male behavior and secondary sexual characters. The parasitoids appears to occur in response to host titers of juvenile
change is thought to be under parasite control, through release of hormone and ecdysone. More spectacularly, rabbit fleas time their
chemicals termed opioid peptides. These have many effects on host own reproduction by sensing the changes in circulating hormones
behavior and immune responses, and in the hamster suppress in their pregnant female host’s blood.
immune defenses as well as altering host investment in reproductive
effort. Some parasites can directly inhibit mating ability via mor- 17.6.3 Parasite manipulation of host behavior
phological or behavioral effects; one example occurs in the schisto-
some bilharzia parasites infecting freshwater snails, where a Many host behaviors have direct impacts on parasites, ranging from
parasite-derived neuropeptide directly inhibits development of the obvious examples such as grooming behavior, coughing, sneezing,
host snail’s copulatory organ. or vomiting, to less obvious cases such as predator avoidance. It is in
the interests of parasites to increase the probability of host behaviors
Another parasite-induced effect is host gigantism, sometimes that benefit the parasite, and to suppress those which do not. Host
associated with host castration. Again, the suggestion is that such a behaviors result from the interactions of stimulus detection and
manipulation of resource investment by the host results in greater assimilation systems (sense organs and central nervous system),
resource availability for the parasite. Host gigantism in response to communication mechanisms (nervous and endocrine systems), and
infection is best known for cestode larvae of the genus Spirometra, effector mechanisms (muscles). A number of cases are known in
whose larvae live in mice. The larvae secrete a hormone (“plerocer- which parasites interfere with one or more of these components
coid growth factor”) that mimics the effects of pituitary growth (though it has recently been argued that the associated evidence is
not always particularly strong). In the best known cases, much of the
696 CHAPTER 17
Polymorphus paradoxus Polymorphus marilis
Infested
amphipods
Mallard Vegetation
Infested
amphipods
Uninfested amphipods Scaup Fig. 17.13 Behavioral manipulations by parasites:
(a) (b) the interactions of duck predators and gammarid
amphipod crustaceans infested by different species
of acanthocephalan worms (Polymorphus). One
species causes gammarids to stay at the surface
where they are eaten by dabblers such as mallard (a),
while another causes them to swim at depths where
divers such as scaup eat them (b).
manipulation is achieved by chemical interventions, and thus repres- (a highly unusual behavior for a worker bumble-bee), providing the
ents components of the environmental physiology of the parasite. fly larva with a protected location in which to pupate.
Parasite-induced host behaviors can be divided into three types: 17.7 Biotic interactions: host–parasite conflicts
1 Behaviors that help maintain the parasite in the host. An example
is provided by the behavior of portunid sand crabs infected with 17.7.1 Host defenses
Sacculina (similar to the parasite in Fig. 17.7), which show increased
cleaning behavior, tending the parasite as if it were a crab egg mass Host defense mechanisms and parasite responses have presumably
stored in the same location. This behavior is shown even by male been evolving since one species first invaded another, hundreds of
crabs, which do not usually carry egg masses. millions of years ago. Thus parasites are part of the host environ-
2 Behaviors that increase the probability of parasite transmission. ment, requiring the evolution of defense mechanisms. Similarly, as
For example, healthy individuals of the estuarine snail Ilyanassa soon as hosts begin to evolve defenses, there is strong selection on
obsoleta avoid being exposed by tidal flow. In contrast, individuals parasites to evolve countermeasures. Defenses and countermeas-
infected with the trematode Gynaecotyla adunca follow high tides ures thus both fall into the category of environmental physiology.
and become stranded on beaches and sandbars, increasing the prob- This is particularly true for endoparasites, although several host
ability that larvae will reach the semiterrestrial crustaceans that are defense mechanisms are able to reach ectoparasites on the outer
the next host. In the acanthocephalan worm Polymorphus para- body surface.
doxus, for which surface-feeding ducks are the definitive host and
the freshwater amphipod Gammarus is an intermediate host, the It is a common misconception that host defenses are essentially
parasite alters the amphipod behavior from benthic scavenging well limited to vertebrates, but this is certainly not the case. It is now
away from ducks to a suicidal pattern of skimming along the surface known that a number of host defense systems are widespread phylo-
and clinging to surface weed (Fig. 17.13a), where ducks readily eat genetically, and probably of very ancient origin (Fig. 17.14 and
them. The related parasite P. marilis causes the gammarids to swim Table 17.3), while others appear to be limited to vertebrates. As well
in the lower waters of the pond, insuring that they are picked up by as withstanding host defenses, some parasites have evolved mech-
a different required host, in this case diving ducks such as scaup anisms that directly suppress host defenses, or utilize them in their
(Fig. 17.13b). Polymorphus is thought to alter Gammarus behavior own development. The control of host immune responses involves
by somehow interfering with 5-HT metabolism. the complex interplay of a variety of chemical messages, including
3 Behaviors that favor parasite survival after host death. Insect para- hormones that influence host behavior; the secretions of some
sitoids may pupate within or on their dead host, and a number of parasites, perhaps primarily aimed at suppression of host immune
species manipulate the host so that before it dies it reaches a location responses, thus also modify host behaviors to the benefit of the
suitable for pupal survival. For example, conopid flies that parasitize parasite.
bumble-bees insure that just before death the bee burrows into soil
PARASITIC HABITATS 697
123456 1 2 3 4? 5 6 from nonself cells. Recognition normally takes place in response to
Vertebrates complex glycoproteins, termed antigens, present on the surface of
Arthropods cell membranes. A primitive recognition system in all animal cells is
(insects, crustaceans) mediated by a number of proteins, including agglutinins, cecropins,
and lectins, in tissue fluids such as the blood. A second recognition
1 2 3 4? 5 6? 1 2 3? 4 5 6 system results from detection of nonself antigens by a range of
receptors on the surface of host white blood cells (found in inverte-
Tunicates Annelids brates as well as vertebrates; see Table 7.8). Vertebrates possess an
(sea squirts) (segmented worms) additional highly complex self-recognition system, involving cell
surface markers of the major histocompatibility complex (MHC).
1 2 3 4? 5 6? 1 2? 3? 4? 5 6* This involves incorporation into host cell membranes of gene prod-
Echinoderms ucts coded for by two groups of polymorphic lociaMHC class 1
Molluscs (on all adult cells) and MHC class 2 (on a subset of adult cells). The
(starfish, sea urchins) (snails, mussels, presence of these surface markers gives cells a highly characteristic
signature recognized by host defenses. Either the presence of other
Deuterostomes octopuses) surface antigens or the absence of the correct MHC signature can
lead to attack by host defense systems.
Ancestral coelomate Protostomes
Once tissues have been recognized as foreign, hosts may mount
12 3 4 5 6 an immune response against them. Such a response can take several
forms, broadly divided into those involving blood and other cells
Nemertines (cell-mediated responses), and those relying on the presence of
(ribbon worms) compounds existing freely in host blood and tissue fluids (humoral
responses). The initial reaction to foreign tissue is often a local
1 2 3? 4 5 6 1 2? 3? 4? 5 6 swelling of host tissue, and local aggregation of host defensive cells.
Coelenterates This defensive effort is achieved through signaling between host
(corals, jellyfish) Platyhelminthes cells; avoidance of host defenses by parasites can therefore be
(flatworms) brought about by manipulating these signals.
1 2 3? 4 5 6
Sponges Acoelomates Signaling between host cells during the immune response
Ancestral Both vertebrates and invertebrates possess tissues, particularly white
metazoan blood cells, whose primary function is the control of the behavior
and production of particular types of host defensive cell. In ver-
Plants 123456 tebrates this control includes instructions for the manufacture of
Protozoans highly specific defensive antibodies by host cells that never actually
confront parasites directly. On a more local scale, signals between
Immunocytes Alloimmunity Soluble factors cells dictate the type of response mounted in the immediate vicinity
1 of a particular parasite. Communication is achieved via cell surface
2 Allograft rejection Natural receptors to specific messenger molecules, and differential stimula-
Probable 5 activity tion of sets of receptors can produce very different responses by the
absence same host cell. The most important chemical signals can broadly be
Alloimmune memory 6 Inducible divided into two types: cytokines and hormones. The known diver-
3 and specificity factors sity of these signals is far higher in vertebrates than in invertebrates.
4 Mixed “leucocyte” cytokines
reactivity These are polypeptides released by a variety of activated immune
and nonimmune cells (including endocrine glands), regulating host
? Insufficient data * Limited defenses in both invertebrates and vertebrates. There are four basic
response sets of cytokines (Table 17.4), with a range of effects summarized in
Fig. 17.15. They are best studied in vertebrates, but at least three
Fig. 17.14 Phylogenetic patterns in immune-type responses and defense systems types are already known in invertebrates, and the invertebrate inter-
in the Metazoa. Cells attacking nonself tissues (immunocytes) are ubiquitous, leukin IL-1 shows a marked diversity of functions: (i) stimulation of
while more complex cellular immune responses and humoral responses (natural phagocytosis and proliferation in white blood cells; (ii) promotion
and inducible soluble factors) have a more limited distribution. See also Table of leucocyte aggregation leading to encapsulation of nonself tissue;
17.3. (From Roitt et al. 1998.) (iii) cytotoxicity to some cell types; and (iv) induction of increased
vascular permeability allowing greater accessibility of nonself tissue
There are a number of defense systems that parasites have to to host defenses.
withstand, and what follows is a very brief review of the environ-
mental physiology of host defense.
Distinguishing “self ” from “nonself ”, and the initiation of defense
Defense in an organism relies on the ability to distinguish self cells
698 CHAPTER 17
Evolutionary step or selection pressure Immunological implications Table 17.3 Evolution of the immune system.
(Adapted from Rowley & Ratcliffe 1988.)
Single-celled animals Recognition and discrimination
Multicellularity (including colonial forms) Histocompatibility system, recognition, and short-
term memory
Mesoderm and circulatory system, nutrition and
defense as separate functions Freely circulating and more diverse blood cell types,
cellular immunity, and erythrocytes
Cancer and viral infections associated with
increasing complexity and longevity Immunosurveillance of own cells for those that are
infected or cancerous
Ancestral protovertebrates
Lower vertebrates: increased size, longer lifespan, Increased recognition and discriminatory powers?
True lymphocytes, lymphoid tissue, and antibody
and reduced reproductive potential compared
with invertebrates production (lgM), longer term memory
Emergence onto land, exposure to irradiation, and
development of high-pressure blood vascular Bone marrow, additional antibody classes,
systems T- and B-lymphocytes, lymphoid organs with
Amniotes (reptiles, birds, mammals) with loss of increased complexity
free-living larval form
Advanced differentiation of immunocompetent cells
Endothermy provides a more favorable allowing increased diversity and efficiency of
environment for pathogens immune system
Viviparity with maternal–fetal interactions Increased efficiency of immune system, integrated
cellular and humoral responses, germinal centers
in secondary lymphoid organs, lymph nodes
Additional fine-tuning of immune system to avoid
rejection by mother
Table 17.4 Types of cytokines in animals. Secondly, there are induced, adaptive defenses (also termed
“specific” or “anticipatory”). These defenses are more specific to
Type Functions particular parasites, and include those with a “memory” that confer
enhanced protection of the host after an initial exposure to the
Interferons Defense of the body against viruses parasite.
Interleukins (17 different types) Directing other cells to divide or
The division between these types is in part taxonomic. A range
Colony-stimulating factors differentiate of nonspecific systems are common to all Metazoa, while long-
Up- or downregulation of cellular processes term memory in the immune system and the manufacture of highly
Tumor necrosis factors a and b, Division and differentiation of bone marrow, antigen-specific antibodies (immunoglobulins) are known only in
and transforming growth factor vertebrates.
hence levels of specific white blood cell
types nonspecific immunity
Mediating inflammation and Both cell-mediated and humoral nonspecific immunity systems are
cytotoxic responses widespread in both invertebrates and vertebrates. Cell-mediated
defenses include three reactions mediated by host cellsaphagocytosis,
other chemical mediators of immune responses natural killer (NK) cells, and encapsulationawhich may be ubi-
Vertebrate white blood cells possess surface receptors for many quitous in the Metazoa. All are mediated by white blood cells
hormones, neuropeptides, and neurotransmitters, including ster- (leucocytes; see Fig. 17.16), which may have their evolutionary roots
oids, epinephrine and norepinephrine, enkephalins, endorphins, and in the phagocytic cells responsible for intracellular digestion and
others. Corticosteroids, endorphins, and enkephalins are of par- transport of food in basal metazoans. Phagocytosis occurs in inver-
ticular importance for parasite environmental physiology because tebrates and vertebrates alike, when phagocytes move towards and
they suppress host immune responses. Cytokine- and hormone- engulf invading material, which is digested intracellularly. NK cells
mediated systems can interact in complex ways; for example, inter- are large granular white blood cells that recognize and destroy non-
leukins from blood cells can elevate or depress the production of self cells by releasing cytotoxins, possibly pore-forming proteins
corticosteroids, while interleukins from pituitary and adrenal that become incorporated in the membrane of the nonself cell so
glands affect the numbers and activities of white blood cells. that it either swells and explodes through osmotic inflow of water,
or ceases to function as a result of metabolite leakage. The third pro-
Defense systems cess of encapsulation involves surrounding nonself material with
tightly adhering layers of host cells. Parasites may be killed when
The defenses mobilized following the detection of nonself tissue walled in by encapsulation; or this may be merely the first stage in a
can be broadly divided into two types. Firstly, there are nonspecific, sequence of cell-mediated host responses resulting in the destruc-
innate immune defenses (also termed “natural”, “nonadaptive”, tion of the parasite, including the action of lysosomal enzymes such
and “nonanticipatory”). These tend to occur in response to a broad as peroxidases and lysozymes. The cell-mediated defenses of inver-
spectrum of parasites, with relatively general defensive properties. tebrates are now known to involve a wide diversity of cell types
The defenses have little or no “memory”, so prior exposure to a para- (Table 17.5).
site does not result in a more effective defense next time the host is
attacked.
PARASITIC HABITATS 699
IL-2, IL-2R, B
proliferation,
differentiation Plasma cells
Antibody Proliferation of
specialized phagocytes
T Interleukin production
(mesangial cells)
release in the kidney
Platelets Platelet IL-6
formation
Skin-forming cells
Growth
Platelet-forming cells Bone tissue
(megakaryocytes) control
in bone marrow
Acute phase Hepatocytes
response in liver
Formation and C-reactive
regulation of protein etc.
bone turnover
Osteoclasts
(a)
Cytokines
B Antigen Th Cytokines Tc LGL
presentation
Activation Cytotoxicity
Fig. 17.15 (a) The range of effects of a cytokine, APC
interleukin-6 (IL-6). (b) An example of the role
of cytokines in mediating interactions between Antibody Intracellular Virally infected
populations of white blood cells: here, between T- production organisms in cells and some
helper cells (Th), B-cells (B), cytotoxic T-cells (Tc), macrophages
and large granular lymphocytes (LGL). Th-cells are (b) tumor cells
stimulated by antigen-presenting cells (APC) and
B-cells to produce cytokines; macrophages are
activated to kill intracellular microorganisms; and
Tc-cells and LGLs recognize and kill target cells.
See text for more details. (From Roitt et al. 1998.)
Humoral defenses include toxins that are permanently present short-term memory in humoral immunity (up to several weeks) has
in the tissues of some metazoans as defenses against predators and been demonstrated in molluscs and insects.
parasites alike. These occur in many sponges and tunicates, and in
those herbivorous insects that store toxic secondary plant com- adaptive immunity
pounds in their tissues (see Chapter 15). More generally, humoral Adaptive immunity involves the development of highly specific host
defenses common to vertebrates and invertebrates include proteins responses to particular parasite antigens. This is coupled with an
that adhere to and aggregate foreign material (e.g. agglutinins and ability of the host immune system to maintain a small population of
lectins), antibacterial peptides (e.g. tachyplesins and defensins), and cells specific to a given parasite antigen even when the infection is
relatively broad-spectrum digestive enzymes (lysozymes). Although cleared. This immunological “memory” allows later reinfections to
many of these broad-spectrum humoral defenses are described as be met with a rapid and highly specific defensive response.
principally “antibacterial”, some confer effective protection against
metazoan parasites. Humoral defenses can be rapidly elevated in As far as is known, such adaptive immunity is only present in
response to invasion (termed an “induced response”), but the dura- vertebrates, and it represents a major breakthrough in controlling
tion of response is generally only a few days. Agglutinins may show parasites. If rats are infected with the nematode Nippostrongylus
some specificity to markers on particular types of invading cell, and brasiliensis, nematode larvae reach the gut and mature, beginning to
release eggs about 5 days after infection. Egg production reaches a
700 CHAPTER 17
Leucocytes (white blood cells) Other
Lymphocytes Phagocytes Auxillary cells
Large
granular Mononuclear
Cell B-cell T-cell lymphocyte phagocyte Neutrophil Eosinophil Basophil Mast cell Platelets Tissue cells
B T LGL
Soluble Antibodies Cytokines Complement Inflammatory Interferons
mediators mediators Cytokines
Fig. 17.16 Summary of the main cell types involved in the immune system, The specific leucocyte membrane receptors and antibodies
the majority belonging to one of the classes of white blood cells (leucocytes). involved contain a common structural motif, the immunoglobulin
(From Roitt et al. 1998.) domain. In vertebrates there is a wide diversity of similar genes with
this motif, almost certainly derived by multiple gene duplication
peak about 9 days after infection, and then decreases rapidly. After events and sequence divergence from a single ancestral gene. Several
21 days, all the adult worms have been expelled from the intestine. cell types are involved:
But if these exposed rats are then reinoculated with infective nema- 1 Mononuclear phagocytes (“monocytes”). A range of different
tode larvae, very few adult worms reach maturity, and infections are forms of these cells exists in different vertebrate tissues (Fig. 17.17),
cleared in 10 days rather than 21.
Table 17.5 Cells and tissues of invertebrate immune systems. Brain
(From Roitt et al. 1998.) Microglial cells
Cells/tissues Role(s) in immunity/physiology Lung Splenic
Alveolar Macrophages
Mucus, cuticle, shells, tests, and/or Physicochemical barriers to invasion macrophages Kidney
gut barrier Mesangial
Mediate cellular and many of the Liver phagocytes
Five groups of free and sessile humoral defense reactions Kupffer cells
white blood cells Synovial
Progenitor cells May act as stem cells for other cell types Blood A-cells
Phagocytic cells Phagocytosis, encapsulation, clotting, Monocytes
Hemostatic cells wound healing, and killing Lymph node
Plasma gelation and clotting by cell Resident and
Nutritive cells recirculating
aggregation; nonself recognition, macrophages
Pigmented cells lysozyme, and agglutinin production
Encapsulation reactions and wound Stem cell
Fixed cells such as pericardial cells, healing? Nutritive role? Precursors in
nephrocytes, or pore cells, etc. Role in defense (if any) unknown; bone marrow
respiratory function
Hemopoietic organs—well Pinocytose colloids and small Fig. 17.17 Distribution of different types of phagocytic cells (collectively termed
organized in some invertebrates particulates; synthesize lysozyme mononuclear phagocytes, or monocytes) in vertebrates. These are manufactured
(pericardial cells) and other in the bone marrow, and pass out of the blood to form a range of tissue-specific
Fat body (insects), midgut, and antimicrobial factors? morphs. (From Roitt et al. 1998.)
sinus lining cells (molluscs, Hemopoiesis and phagocytosis;
crustaceans) synthesize antimicrobial factors in a
few animals
Synthesize immune proteins and
agglutinins (fat body), phagocytosis
(midgut cells), clearance of foreign
particles
PARASITIC HABITATS 701
including mammalian monocytes, which become tissue macro- N
phages. They recognize particular portions of antigen molecules, N
and if these are not compatible with the MHC signature of host cells,
then the structure bearing them is attacked. In addition to their C C
phagocytic ability, macrophages can destroy other cells by secreting C Heavy chain C
a range of toxic compounds. Cytotoxicity can be through the release
of proteolytic and other cytolytic enzymes, or through the release Light chain
of toxic compounds termed “reactive oxygen intermediates” and
“reactive nitrogen intermediates”. Oxygen intermediates are formed N
by enzymes that reduce oxygen to the superoxide anion, OO−. This
in turn can give rise to toxic hydrogen peroxide and hydroxyl rad- N
icals. Monocytes in the blood use peroxidase to create more toxic
bleach-like oxidants. Nitrogen intermediates are formed by the Fig. 17.18 The basic structure of immunoglobulins. The Y-shaped molecule
enzyme nitric acid synthase, which combines oxygen with nitrogen consists of two identical light polypeptide chains and two identical heavy
from the amino acid arginine to produce toxic nitric oxide. Under polypeptide chains linked together by disulfide bonds (dark green). N is the
certain conditions, nitrogen intermediates and oxygen intermedi- amino terminal and C the carboxy terminal of the chains. The variable regions
ates may interact to produce even more toxic peroxynitrites. These are at the N-terminal ends of the heavy and light chains. (From Roitt et al. 1998.)
compounds are all highly oxidizing, and their application in defense
is sometimes termed the “oxidative burst”; it can destroy multi- 1 IgM. This is the first immunoglobulin secreted in response to
cellular parasites such as nematode microfilaria larvae and the infection. It is a five-molecule polymer that stimulates phagocytosis
cercariae of schistosomes. and also binds cells bearing the correct antigen together. It is
2 Neutrophils. These are the most common type of leucocyte in the secreted across the wall of the intestine, and is thus active against gut
blood, and are shorter lived as after ingesting the target material parasites.
they die. Neutrophils are able to mount cytotoxic responses using 2 IgG. After 4–5 days, IgM is replaced by IgG, which plays a major
toxic proteins and reactive O2/N2 intermediates, against targets role in activating cytotoxicity by macrophages, neutrophils, and
labeled with antibodies. This defense is also effective against various eosinophils. It also activates a complex cascade of reactions termed
metazoan parasites. the complement system. This consists of at least eight factors
3 Eosinophils. These are a specialized group of leucocytes that can that interact to result in a membrane attack complex, forming pores
recognize and damage large extracellular parasites. Although capable in bacterial cell walls. Complement components also attract
of phagocytosis, they function principally by cytotoxic responses. macrophages, enhance phagocytosis, and increase local vascular
4 Lymphocytes. These are wholly responsible for the specific permeability.
recognition of parasite antigens, central to adaptive immunity. There 3 IgA. This is secreted in body fluids such as tears, saliva, and milk,
are two types, derived from bone marrow stem cells: T-cells develop and boosts the immunity of young infants. It is also secreted into the
in the thymus gland, while B-cells develop in the bone marrow in gut, and is resistant to enzymatic attack.
mammals. Both B- and T-cells accumulate in the lymph nodes and 4 IgE. This is bound to cells termed mast cells. In response to anti-
spleen, from where they respond to parasite antigens in the blood. gens and cytokine messages from activated T-cells, it causes the
T-cells exist in two types with different surface markers; T-helper mast cells to release chemicals including histamines into the sur-
(Th) cells and cytotoxic T (Tc) cells. Tc-cells are involved mainly in rounding tissues and stimulates cytotoxicity by macrophages and
recognizing antigens resulting from intracellular parasites, and eosinophils. The histamines cause direct damage to parasites, or
killing infected cells, while Th-cells are more important in responses disrupt the usual parasite microhabitat by tissue inflammation, or
to multicellular parasites. Th-cells divide to produce a clonal popu- increase exposure of the parasite to other attacking agents as a result
lation of antigen-specific cells, which then release cytokines to of increased vascular permeability. Mast cells and IgE are important
activate other cells in the immune system (see Fig. 17.15b). B-cells in defense against helminth infections, particularly for worms
also possess highly specific antigen-recognition abilities, and once that live in contact with the gut lining. Activated mast cells cause
activated they manufacture and release large quantities of antibody. shedding of the intestinal epithelium, aiding removal of the worm.
antibodies and complement Antibodies are able to reach parasites in a wide diversity of
Immunoglobulin (Ig) antibodies are proteins composed of four locations in or on the host. While tissue and gut parasites are most
peptidesatwo heavy (≈ 400 amino acids) and two light (≈ 200 amino obviously exposed to attack, parasites on the body surface can also
acids) chains (Fig. 17.18) bound together to give a Y-shaped struc- be reached if they feed on blood. Fish produce antibodies in
ture. The arms of the Y contain highly variable regions on both the response to attack by ectoparasitic monogenean flukes, targeting
heavy and light chains, and this is the part of the immunoglobulin them either via the blood they ingest or via the mucus on the fish
involved in binding to a specific antigen. The base of the Y has a
more constant amino acid sequence characteristic of particular
immunoglobulin types, and is the part of the molecule recognized
by host cells. In mammals, antibody molecules can be divided into
four types, with characteristically different roles in host defense.
702 CHAPTER 17
skin. Mammals produce antibodies to anticoagulants in the saliva of cells. In vertebrates such sites include the eye lens (occupied by lar-
arthropod blood feeders such as ticks, leading to infiltration of the vae of some digenean fish flukes) and parts of the central nervous
bite site by mast cells. Ticks attempting to feed from immune hosts system. In insects certain sites (including nerve ganglia, salivary
may fail to engorge, fail to molt normally, or die of desiccation. glands, gonads, muscle fibers, and the fat body) show far lower risks
of encapsulation than others, and these too are exploited by para-
Coordination of host defenses sites. Life-cycle stages that migrate through host tissues are more at
risk from host immune defenses than those inhabiting the gut
In parasites with complex life cycles, each host provides a different lumen, and it is possible that exploitation of the gut as an adult site
defensive environment, and a single parasite species may be attacked may represent avoidance of host immune responses.
by several of the immune responses described above. Often particu-
lar components of the immune system are of differing importance After parasites enter the host, the speed with which they reach
in different tissues, and where parasite larvae migrate through the immunologically privileged sites may be crucial to their survival.
host they may be exposed to a sequence of defenses. This can be The larvae of some endoparasitic tachinid flies hatch in the gut of
illustrated by the diversity of defenses brought to bear by the human their insect host where they are relatively safe from host defenses;
immune system on the larvae of Schistosoma mansoni. Attacks they then migrate rapidly from the gut wall towards the anterior
are directed against the larval tegument, whose antigens induce nervous system of their host, a protected site. On the way they initi-
Th-lymphocytes to initiate production of IgG and IgE antibodies by ate a vigorous encapsulation response from their host, and only the
B-cells. The antibodies bind to the larval tegument. Direct humoral most rapidly moving are able to reach safe sites in the nervous sys-
attack on the worm is carried out by the complement system, both tem. Tachinids also illustrate the fact that safe sites are sometimes
alone and in concert with worm-bound antibodies. The cytokine, exploited only for a while immediately after the parasite enters the
interferon, secreted by Th-lymphocytes, activates macrophages, host. After a period, generation of more effective defenses by the
which in turn secrete another cytokine, tumor necrosis factor. This tachinid larvae allows them to re-emerge into the better defended
activates neutrophils, eosinophils, and platelets. All four blood cell host hemocoel without being encapsulated.
types respond to the antibody-labeled worm tegument with cyto-
toxins. Macrophages and neutrophils attack the host tegument Detoxification of host humoral defenses
using toxic oxygen and nitrogen metabolites, while eosinophils
attack using toxic proteins. Worm antigens also bind to specific IgE Parasites are able to neutralize a very wide range of toxic host
receptors on mast cells, and these in turn are involved in activating compounds, including toxins generally present in the body fluids,
the eosinophils. the complement system, toxic reactive oxygen and nitrogen inter-
mediates, and antibodies. Where hosts sequester compounds to
17.7.2 Parasite countermeasures deter attackers, specialist parasites are usually able to detoxify these
compounds, although generalist parasites may be susceptible. For
There are two kinds of protection available to parasites in or on their example, larvae of moths of the genus Zygaena sequester cyanogenic
hosts. One type is associated with resisting chemical attack in compounds from the food plants and are avoided by most para-
extreme environments, particularly the gut. The second is asso- sitoids, but a few specialist parasitoid wasps possess enzymes that
ciated with avoiding specific antiparasite aspects of host physiology. detoxify these compounds.
Some aspects of parasite protection are common to both types of
environmental challenge. Parasites show a range of responses to humoral products of the
immune system. Metazoan parasites are often able to resist attack
Physical protection by the host complement system through the possession of surface
glycoproteins that mimic host molecules that inhibit the comple-
Isolation of the parasite from external conditions confers protec- ment cascade. A number of parasites show enzyme-based defenses
tion from all unfavorable aspects of the surrounding environment. against the reactive oxygen and nitrogen intermediates from cyto-
Some parasite larvae resist host defenses in their intermediate hosts toxic phagocytes. The enzymes are the typical metazoan antioxid-
by constructing thick-walled protective cysts, as in the nematode ants (see Chapter 7) and may either be secreted from the parasite’s
Trichinella spiralis. These cysts are broken down when the parasite body or bound to its surface. Thus the nematode Onchocerca
enters the next host in its life cycle (normally by predation of its secretes superoxide dismutase, filarial nematodes inhabiting the
intermediate host), either by host- or parasite-generated enzymes. lymph system use a surface-bound glutathione peroxidase, and
Adult parasites in their definitive host may avoid immune responses schistosomes use a surface-bound glutathione S-transferase.
by inducing host tissues to form a cyst around them. This can
perhaps be regarded as parasite adaptation to survive within a cyst Detoxification of antibodies is achieved in some nematodes and
following detection of a host encapsulation response. trematode flukes by cleaving the antibody molecules with proteases.
The antibody molecules are split in such a way that the part of the
heavy chains essential for detection of the antibody by host cells is
removed.
Immunologically privileged sites Hiding and molecular mimicry
These are regions of the host body in which immune responses are Intracellular parasites such as protistan plasmodia or coccidia are
reduced or lacking, usually due to the absence of host white blood able to “hide” inside host cells, such that their antigens are not
PARASITIC HABITATS 703
exposed to host immune systems. Relatively few metazoan parasites viduals with a new type of glycoprotein forming their surface coat.
are small enough to hide inside cells, but the filarial nematode This type of strategy has been suggested to explain the low immune
Trichinella is an example, hiding inside the large cells of pig skeletal responses mounted against some nematodes, such as Wuchereria
muscle. bancrofti (the agent of elephantiasis), which can survive in the lymph
system even though this is the heart of the human immune system.
Parasites are sometimes able to avoid detection by the host
immune system in other ways, either coating their surface with host Active suppression of host defenses
tissues, or disguising their tissues with host antigens (molecular
disguise). Schistosoma mansoni absorbs host antigens soon after Some parasites reduce host defenses by interfering with the struc-
invading the human body, and so effectively disappears from host tural and/or functional integrity of host leucocytes. For example,
detectors of “nonself ”. The larva is able to absorb surface antigens bilharzias schistosomes produce neuropeptides that directly sup-
corresponding to blood groups and the MHC. An immune response press their snail host’s hemocytes. Other parasites are able to divert
is mounted to the antigens presented immediately after invasion, the recruitment of attacking host blood cells. For example, the com-
but the larvae have “disappeared” by the time the host response plement system activates neutrophils and macrophages through a
becomes effective. However, later invasions by cercariae are often protease enzyme, elastase, and tapeworms are able to secrete an
destroyed by the activated defenses during penetration of human elastase inhibitor, preventing the generation of characteristic com-
skin. Immunity to reinfection established by the first wave of para- plement fragments following elastase digestion of targets and so
sites is termed “concomitant immunity”, and may help reduce over- hiding the parasite from host defensive cells.
exploitation of hosts by a given parasite species. Schistosomes are
able to incorporate host antigens in both their snail and human Suppression of detection may also be involved in the defense of
hosts; their ability to take up host antigens is highly host specific, parasitoid eggs inside insect hosts. Within its egg, the parasitoid
and cercaria larvae invading the incorrect host are rapidly destroyed. embryo is surrounded by a layer of cells called teratocytes, and in
For example, the cercariae of marine schistosomes, normally living in many species these continue to surround the young larva when the
sea birds, occasionally try to penetrate the skin of human swimmers egg shell is lost. The surface of the teratocytes is covered in micro-
or fishermen. They are halted by host defenses and die in the skin, villi, and the cells are also supplied with extensive endoplasmic
leading to a dermatitis condition known variously as “swimmer’s reticulum, suggesting a secretory function. Some property of terato-
itch”, “clam-digger’s itch”, “seabather’s eruption”, and “weed itch”. cytes (as yet unidentified) suppresses host abilities to encapsulate
the parasitoid; embryos from which these cells have been removed
There is also some evidence that parasites can synthesize their are quickly encapsulated.
own host-like molecules (molecular mimicry). For example, a few
insect parasitoids appear able to coat their eggs with virus-like par- A fascinating mechanism of host defense suppression in insect
ticles that mimic host proteins. Likewise, pentastomids living in parasitoids involves the release into the host of polyDNA viruses by
vertebrate lungs evade the hosts’ immune defenses and reduce the egg-laying female. These viruses have a characteristic structure,
inflammation by coating their cuticles in their own stage-specific either rod-shaped or spindle-shaped, and always contain double-
lipid surfactants, very similar to the host surfactants that line the stranded circular DNA molecules coiled into superhelices. The
alveoli. origin of polyDNA viruses remains a subject of debate. One attract-
ive theory is that viruses are in fact parts of the parasitoid genome
Changing the antigens presented to the host that are injected into the host to provide local delivery of venom.
Evidence for this is the similarity between the polyDNA viral
If a particular set of surface antigens on a parasite have been sequence and other parasitoid genes expressed in the venom glands.
changed by the time the host can produce antibodies to them, then After injection by the female parasitoid, the viruses rapidly infect a
the parasite can stay one step ahead of the host’s immune system. whole range of host cells (transcription products of the viral genome
Changing parasite antigens is sometimes associated with molts or are detectable within 2 h of infection), and suppress the host encap-
metamorphoses in the parasite life cycle. This strategy is illustrated sulation of parasitoid eggs.
by the nematode Nippostrongylus in rats. Infective larvae penetrate
the skin, and migrate to the lungs in less than 24 h. In the lungs they Parasites in vertebrates show a further set of immunosuppressant
molt, presenting a different set of stage-specific antigens. The next adaptations. Some are able to cause direct damage to leucocytes
larval instar moves from the lungs to the intestine, where it molts through the release of toxic secretions. In others, the ability of the
again to present yet another set of surface antigens. In each case the immune system to produce suitable antibodies is disrupted by the
change is quick enough to prevent effective host immune responses. release of large quantities of materials that interfere with antigen
However, the effect of memory in the Th- and B-cells in vertebrate processing by macrophages. Alternatively the activity of defensive
immune systems is that antibodies against each larval instar can cells in the immune system may be reduced by parasite-induced
be produced far more rapidly in subsequent infections, leading to release of immunosuppressants, such as prostaglandins and other
levels of acquired host immunity. hormones. This may be achieved either through parasite mani-
pulation of host secretions or (in the case of filarial nematodes and
A number of parasites are able to maintain a rapid turnover of tapeworms) by secretion by the parasites themselves. Schistosoma
surface antigens within a single life stage. The best known example mansoni secretes endorphins, which probably have immunosup-
of this is provided by protozoan trypanosomes, the agents of sleep- pressant effects in both invertebrate and vertebrate hosts. Similar
ing sickness. By the time the host has mounted an immune response disruption of host defenses may also be achieved by altering the
against one set of antigens, the parasite population consists of indi- balance of cytokines; filarial nematodes induce human hosts to
704 CHAPTER 17
release high concentrations of an IgG which inhibits protective IgE- the acanthocephalan, perhaps through depletion of essential nutri-
mediated responses. Similarly, patients infected with schistosomia- ents or the release of alcohol as a toxic excretory product, may be
sis produce IgM and IgG antibodies that inhibit normal cytotoxic involved. However, just as so many parasites are able to overcome
responses by neutrophils and eosinophils. host defenses, some parasites (regarded as specialized opportunists)
are able to cope with other parasite species in the same host, and
17.7.3 Parasite exploitation of host defenses consistently parasitize previously infected hosts.
Parasites are adept at turning the tables on their hosts’ attempts at 17.8 Conclusions
defense. For example, they may feed on the tissues produced as a
host defense in response to them, or induce such complex and costly Parasites may be the single most important cause of reduced fecund-
defenses that the host is weakened and is more likely to be preyed ity and/or early mortality in natural populations of animals, thus
upon by a predator that is itself a host in the parasite life cycle. Some regulating populations and ecological balances at the most funda-
parasites actually need part of the host immune response to survive. mental level. There has been an increasing realization that parasites
Here an example is seen in remoras (marine fish) infected with the may be one of the major factors shaping all host populations, both
fluke Dionchus remorae, since the egg bundles of this ectoparasite in terms of ecological distribution (ranges occupied) and cyclical
induce the gill epithelium to which they attach to grow around the behavior of population numbers. This is linked to models of how
egg bundles, thus usefully anchoring them in place. Similar immune host–parasite interactions may evolve. Are they in a sense mutual-
response-based attachment of parasites is seen in the reaction istic, the parasite and the host both seeking to minimize the damage
around the heads of acanthocephalan worms in vertebrate guts, done, or entirely aggressive, both host and parasite always seeking
which holds the worms firmly in place. The nematode Strongyloides, to outdo the other, and selection always operating to maximize
parasitic on rats, appears to use the host’s immune system as a trig- individual success?
ger for its own sexuality, only producing sexual phases from larvae
that encounter hosts with acquired immune protection; here sex is Early work on parasitism tended to stress mutualisms, giving
perhaps being used as an adaptation to counter the rapid evolution examples like trypanosomes in Africa that are relatively benign to
of vertebrate immunity. native cattle (with whom they are coevolved) but lethal to intro-
duced cows and to humans. “Older” parasites (in the evolutionary
17.7.4 Chemical warfare between parasites sense) do seem to be generally less virulent and have slower popula-
tion increases. However, more recent studies have concentrated
Parasites not only have to contend with host defenses, but also with on aggressive models, seeing host–parasite relations as a coevolu-
competition and attack from other parasites. Sometimes this occurs tionary arms race, in which each organism always tries to keep one
within species (even between siblings) and sometimes between step ahead of the opposition and have maximal growth rate and
species. Suppression of host defenses by one parasite may lead to maximal virulence. Perhaps a balanced view now is that either
increased susceptibility to attack by others, an outcome which may model (or an intermediate model of a “prudent parasite”, doing
well be detrimental to the first parasite. only as much damage as the host can take) may apply in different
circumstances. Whether a parasite evolves towards greater or lesser
Perhaps in response to this, parasites may deploy secondary host virulence will depend on its genetics and its epidemiology, including
defenses (termed “parasite-mediated internal defenses”) to prevent factors such as its lifespan relative to its host, its reproductive rate,
damage to the host or to the first parasites by later opportunists. its transmission mode, the host’s population size and dispersion,
Such defenses may be very general; the bactericidal anal secretions and so on. In very simple terms, microparasites that have already
from some insect parasitoids are thought to protect their hosts infected a few hundred other hosts will not “care” at all about killing
(which are in effect living carcasses) against bacterial decay, pro- off an original host, and nor will a parasite that achieves trans-
longing the “shelf-life” of the larval food supply. Other examples mission by one host being eaten by the next. However, many
are more specific; some insect parasitoids lay eggs in previously macroparasitesahelminths and insects, generallyamay have relat-
parasitized hosts that inhibit the development of the resident para- ively low reproductive rates, longer lifespans relative to their host,
sitoids. Competition among insect parasitoid larvae is often deter- and more secure transmission systems, so that they need and benefit
mined by direct combat, but differing physiological tolerances for from much lesser virulence.
limiting resources, particularly oxygen, may also influence the out-
come of these fights. For example, in ichneumonid wasps the eggs Given these various possibilities, different types of parasites can
and young larvae have a much lower tolerance of oxygen depletion clearly have wildly different ecological consequences for their hosts.
than older larvae, and older larvae are able to deplete oxygen levels For highly virulent, strongly “r-selected” microparasites, epidemics
in the host such that younger competitors die. Competition is also and mass mortalities are always possible, and such organisms invad-
recorded for nematode and platyhelminth parasites in the gut. Two ing new habitats or new hosts are often lethal. For more benign para-
parasites that normally occupy the same region of intestine when sites, effects may be more subtle. For example, the ranges of hosts
alone may be spatially separated if both invade one host, the com- may be controlled by their susceptibilities to endemic parasites. One
petitively inferior species being displaced to a new region. The acan- example here is the grazers of North America, where the bighorn
thocephalan Moniliformis causes the cestode Hymenolepis to move sheep range is largely determined by the prevalence of lungworms
further back in the rat intestine, but if the acanthocephalans are (Protostrongylus). Similarly, rinderpest virus in Africa seems to con-
killed the cestodes migrate anteriorly. Physiological interference by trol distribution of native ungulates: it is usually fatal to kudu and
PARASITIC HABITATS 705
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Index
Page numbers in bold indicate pages with tables or boxes; page numbers in italic indicate pages with figures
A-selection 5, 621 acid rain primary 62–5
absolute aerobic scope, definition 128 causes 522–3 secondary 65–6
abundance, and body mass 42 consequences in urine production 90–2, 94–6
for freshwater animals 523 see also calcium pumps (Ca2+-ATPase); hydrogen
carnivores vs. herbivores 610 for terrestrial animals 615
acanthocephalans regional patterns 522 pumps (H+-ATPase); ion pumps; sodium
and soil pH 616 pumps (Na+/K+-ATPase)
and cestodes 704 activins 359
cuticles 687 acid waters activity, and metabolic rates 127–8
nutrients, competition 685 adaptation to 534 acyl carnitine, synthesis 123
outer surfaces 685 habitats 534 acyl-CoA
parasitism 683 beta-oxidation 123
proboscis 686 acidification transport 122–3, 123
acceleration, vestibular system response 271–2 of atmosphere 615–16 adaptation
acclimation 6, 9–10 of biosphere 615–16 concept of 6–7
capacity 201 freshwater habitats 501, 522–3 detection, comparative methods 7–8
cellular 77 lakes, regional patterns 522 and environmental disturbance 6
cold, in carp 181 treatment strategies 523 enzymatic 177–80
enzymes 178 evidence for 6–7
and oxygen conformity 143 acidosis feedback in 33–5
and permeability 84 and respiratory alkalosis 169 at genome level 17
resistance 201 tolerance 586 mechanisms 17–35
in thermal biology 196–202, 401, 466, 497, 503 at molecular level 17
and torpor 660 acoustic energy, transmission 427–8 and morphology 14
see also thermal acclimation actin 291, 293 nature and levels of 3–15
acclimatization 6, 9–10 photoreceptors 278, 280
acetate cross-bridge formation 299, 300, 301, 302 and phylogenetic relationships 10
absorption 608 filaments in sarcomere 293, 294, 294, 296 process 6–8
synthesis 683 and proteins 17
acetoacetate F-actin 294 see also homeoviscous adaptation (HVA); ionic
as fuel 125 G-actin 294 adaptation; thermal adaptation
roles, in aerobic metabolism 123 muscle contraction 300–5 adenohypophysis 351
acetoin, synthesis 683 regulation 312, 313 adenosine diphosphate (ADP)
acetyl-CoA, and Krebs cycle 119 troponin-based control 304, 306 structure 113
acetylcholine 237 smooth muscle 312 synthesis 112–13, 114–15
effects on skeletal muscles 32 Actinia spp. (anemone) adenosine triphosphatase (ATPase) 62–5, 66,
neuromuscular junction 303, 318 avoidance strategies 457 114–15, 461
postsynaptic actions 240 conformity 457 ion pumps 63
acetylcholine receptors actinin 296 myosin 30, 114, 178, 179, 300, 309–11, 404, 503
developmental aspects 263 action potentials 225–30, 227, 228, 303–5 see also calcium pumps (Ca2+-ATPase); hydrogen
muscarinic 240, 241, 244 developmental aspects 262 pumps (H+-ATPase); ion pumps; sodium
neuromuscular junction 299–300, 300, 303 information content 232 pumps (Na+/K+-ATPase)
nicotinic 240, 244 in muscle 303–5, 317, 318 adenosine triphosphate (ATP)
“patch clamp” studies 229 binding 17
regulation 257 saltatory progression 231, 234 energy storage 683
structure 298, 300 self-propagation 230–1, 231 hydrolysis 20, 64, 113
acetylcholinesterases sensory receptor signaling 266–7 muscle contraction 299, 300–1, 309–10
action 244 synaptic transmission 232–46 roles in metabolism 112–13
excretion in parasites 687 threshold values 226 splitting 62
gene expression 178 velocity 230 structure 112, 113
Achatina spp. (snail), eggs 587 “voltage clamp” studies 229, 229 synthesis 34, 119–23, 683–4
acid–base balance 364 active secretion
see also pH markers 91
mechanisms 89
active transport
mechanisms 62
714 INDEX
adenosine triphosphate (ATP) (continued) air-breathers (aquatic) 473, 510 roles
turnover rates 113, 114, 473 see also breathing, bimodal in aerobic metabolism 123
yields 115, 117 in anaerobic metabolism 30, 117
air bubbles, freshwater arthropods 510, 510
adenyl cyclase air pressure detectors 269–70 in solutions 53, 466
activation 683 air sacs symport 66
peptide hormone signaling 344 synthesis 498, 685
roles 30 birds 146–7, 151 uptake rates 430
insects 148, 150, 171, 192 para-aminohippuric acid (PAH), and kidney
adhesion molecules 237, 262 as insulation 192
adipokinetic hormones 370 alanine, roles, in aerobic metabolism 125 function 91
adipose tissue alanopine, synthesis 117 aminopeptidase-I, occurrence 462
alarm pheromones 384 ammonia
in high latitude animals 658 Alaskozetes spp. (mite)
as insulation 406, 658 freeze avoidance 654 accumulation, in burrows 625
leptin secretion 360 glycerol content 652 excretion 100
and lipids 122 occurrence 651
rabbits 122 thermal regulation 651 by fish gills 497, 498, 534
see also brown adipose tissue (BAT) albedo by land animals 559, 563
ADP see adenosine diphosphate (ADP) and greenhouse warming 610 properties 100
adrenal glands 355, 356 polar habitats 646, 646 see also excretion
cortex 355 aldosterone 355 ammonotelic animals 100
medulla 355 blood volume regulation 363 AMP deaminase, catalysis 115
stress responses 370–1 ion balance regulation 363 AMPA receptors 240, 242, 260
adrenal sex steroids 355, 375 roles 436 amphibians
adrenaline see epinephrine algae basking 569
adrenocorticotropic hormone (corticotropin) 354, distribution 394 bimodal breathing 171, 507, 586
as food sources 515 bladder 102
355 ALH see ascending loop of Henle (ALH) brain/CNS 602
release 595 alkaline waters, habitats 533–4 cutaneous respiration 103
roles, in lipolysis 122 alkaloids, occurrence 604 eggs 590
adversity selection see A-selection Allanaspides spp. (crustacean), blood pH 534 electroreceptors 287
Aedes spp. (mosquito) allantoic acid, occurrence 101 estivation 638
body fluids, regulatory mechanisms 534 allantoin freeze tolerance 185
habitats 530 occurrence 101 freshwater 496, 503–4, 515
hyporegulation 531 properties 100 hearts 157
ion uptake 497 allatostatin 349 hyperosmosis 84
permeability 496 allatotropin 349 jumping 598, 599, 599
reproduction 373 alleles kidneys 499, 561
in soda lakes 534 occurrence 6, 18–19 life cycles, temperature effects 11
urine composition 499 polymorphism 138, 178, 462 littoral 454
as vector 691 allelochemicals, occurrence 604 lungs 146, 146, 171
aerial exposure, in aquatic animals 459, 471, 502, Allen’s rule, tundra animals 649 marine 436
alligators in montane habitats 666
507 blood pressure, patterns 441 permeability 83, 496
aerial life 671–3 body temperature 504 reproductive strategies 590
aerobic capacity, and endothermy 218 allohormones 383 respiration 170–1
aerobic metabolism/respiration allometric analysis 39 respiratory gas exchange 153
allometric variation 37, 38 salt uptake 84
adenosine triphosphate synthesis 119, 121, 122 allomones 385 thermal acclimation 201
control of 125 allostatin 314 torpor 213
in endoparasites 682 allosteric binding urea retention 633
evolution 112 competitive 18 ureotely 100
fuels for 121–5 cooperative 18 urine, hyposmotic 561
in insects 125 allozymes, use of term 28, 178 walking 598
in littoral animals 471–3 Alma spp. (oligochaete), respiration 507, 582 water balance, hormonal regulation 361
pathways 119–25 alpha-actinin 296 water loss 80, 552
waste products 119 alpha-helices, structure 21 water permeability 83
Aeropedellus spp. (grasshopper), life cycles 671 Alpheus viridari (shrimp), salinity tolerance 470 water uptake 496, 633
afferent (sensory) neurons 247–8 altitude, and pressure 669 see also anurans; frogs; toads
afforestation, and freshwater habitats 524 see also high-altitude habitats Amphibolurus spp. (lizard), cooling 573
AFGPs see antifreeze glycoproteins (AFGPs) altricial strategies, terrestrial mammals 593 amphipods
AFPs see antifreeze proteins (AFPs) Alvinella pompejana (polychaete), habitats 536 reproductive strategies 588
age at maturity Alytes spp. (toad), eggs 590 see also gammarids; Gammarus spp. (amphipod)
and generation time 138 amacrine cells 282, 288 amplification, transduction processes 266
and growth rates 138 ambient temperature, and body temperature ampullae of Lorenzini 287
aggregation 384 ampullary organ 287
aggression, hormonal regulation 381 566–81, 569, 572, 575 amygdala 252, 324
agriculture, and manmade habitats 617 Amblyomma spp. (tick), hydrophilic cuticles 565 Anableps spp. (fish), eyes 514
agrin 263, 299 Amblyrhynchus cristatus (iguana), thermal anabolism, mechanisms 112
Agrotis spp. (caterpillar), freeze tolerance 668 anaerobic metabolism/respiration
air adaptation 468, 572, 573 conditions 473
composition 581 amine neurotransmitters 237 in endoparasites 683
density 542 amino acids evolution 112, 141
gas diffusion 542 lifestyles 474
properties 542 as hormones 237 muscle contraction 310, 331
refractive index 542 and Krebs cycle 123 in parasites, pathways 685
sound velocity 542 as osmolytes 71, 73, 74, 399, 462, 463, 497, 633
viscosity 542
INDEX 715
pathways 115–18 antelope ground squirrel, body temperature 625, reproductive strategies 588
roles 115 626 water and solute balance 606
in shore and estuarine animals 473–5 aphotic zone 423
anaplerotic pathways, use of term 119 antelopes Apis spp. (bee)
Anax spp. (dragonfly), warm-up recordings 578 desert 624 aerobic metabolism in flight 125
Ancyclostoma duodenale (nematode), life cycle running speed 334 caste pheromones 384
water conservation 642–3 color vision 280
688 huddling 577
androgens 345, 374, 375, 376, 381 antennal glands 362 parental care 595
terrestrial crabs 559 swarms, thermal regulation 577
adrenal glands 355 water balance 560 temperature regulation 208, 575
release 594 thermal insulation 207
roles, in fetal development 595 Antheraea polyphemus (moth), mate location Aplasia (sea slug)
anemones 382–3 antidiuretic hormone 361
avoidance strategies 457 synaptic transmission 242
chemical signaling 427 Anthopleura (anemone), pheromones 384, 427
conformity 457 anthopleurine, chemical signaling 427 learning 255, 258, 259
Anemonia spp. (anemone), conformity 457 anthropogenic issues apnea, and diving 440
anemotaxis 382 apnoeic response, mechanisms 171
angiotenin-converting enzyme (ACE) 358 cold biomes 662–3 apoptosis 263
angiotensin I 358 deserts 644, 644
angiotensin II 358 estuarine habitats 481–3 metamorphosis 366–7
blood volume regulation 363 freshwater habitats 518–24 aposematism, butterflies 605
drinking behavior regulation 363 littoral habitats 481–3 appetite, hormonal regulation 370
sodium pump regulation 360 marine habitats 430–2 Aptenodytes spp. (penguin)
Anguilla spp. (eel), swim-bladders 421 terrestrial habitats 610–17
anguilliform motion 331 antibodies 701 huddling 657
anhydrobiosis see cryptobiosis detoxification 702 occurrence 648
annelids in host-parasite systems 701–2 apterygote insects 87, 102, 337, 564, 582, 588, 598,
anaerobic metabolism 473 production 697
brackish habitats 454, 465 structure 701 624
brain 249, 251 see also immunoglobulins aquatic habitats
buoyancy mechanisms 418 antidiuretic hormone (ADH) 72, 96, 109
direct chemical uptake 65, 430 invertebrates 361, 362 feeding habits in 543
extracellular fluids 497 see also vasopressin hormonal regulation of water balance 361
filter feeding 150, 477 antienzymes, release 687 osmotically peculiar 529–34
freeze tolerance 184 antifouling agents, tributyltin 482 properties 542
freshwater, oxygen consumption 507 antifreeze compounds 186, 436–7, 438, 438, 655 salt availability 543
hearts 155 antifreeze glycoproteins (AFGPs) special 526–39
hemoglobin 163, 472 mechanisms 186 and terrestrial habitats compared 542–3
hydrostatic skeleton 326 occurrence 437, 438, 438 thermally extreme 535–9
larvae 412 roles 186 transient 526–39
littoral habitats 451 structure 187, 438 trophic structures 543
lungs 145 synthesis 438 see also brackish habitats; freshwater habitats;
metamorphosis 367 antifreeze proteins (AFPs)
nerve function 465 classes 438 marine habitats
nervous system 248–9, 250, 251 mechanisms 186 aqueous solutions
neurohormones 347, 348 occurrence 437, 655
reproduction, hormonal regulation 372 roles 186 biochemistry 51–5
sodium loss 459 seasonal production 439 colligative properties 54
terrestrial 548 antigens concentrations 53–4
urine concentrations 499 and cell recognition 697 freezing points 186
ventilation 149 changes, in host–parasite conflicts 703 osmotic coefficient 55
see also earthworms; leeches; oligochaetes; antioxidants supercooling 185
detoxification 170 aquifers 493
polychaetes roles 141 arachidonic acid, precursors 32
Anodonta spp. (bivalve) antiport arachnids
mechanisms 62 book lungs 150
acidity problems 501 use of term 65 coxal glands 559
osmoregulation 108 antiporters, roles 65–6 cuticles 83, 557
stenohaline characteristics 496 ants eggs 589, 595
Anolis spp. (lizard), body temperature during fever desert 623, 626, 629, 630, 632, 636 evolution 541
metabolic rates 629 feeding 609
220 microclimates 547 reproductive strategies 588
Anopheles spp. (mosquito), as vector 691 nests 636, 636 see also mites; scorpions; spiders
anoxia spiracles, mechanisms 172, 585 Aral Sea, surface area loss 521
anurans Arapaima spp. (fish)
coping strategies 169–70 desert 624 lungs 150
in brackish animals 473–4 eggs 590 swim-bladders 507
in freshwater animals 507 herbivory 607 Archaeopteryx spp. (extinct “bird”), turbinates,
in parasites 682, 683 jumping 337, 598, 599
metamorphosis 368, 369 absence of 220
occurrence 115, 141 see also amphibians; frogs; tadpoles; toads Archips spp. (beetle), pheromones 601
Antarctic Aphelocheirus spp. (bug) Arctic
mechanoreception 515
boundary definitions 647 plastrons 511 boundary definitions 647
fauna 648 aphids fauna 648
fresh water 647 in deserts 624 flowers 651
ice-sheet thinning 662 Arctic insects, hibernation 655
Antarctic mites, freeze intolerance 185 see also polar animals
see also polar animals Arenicola spp. (polychaete)
anaerobic metabolism 474
716 INDEX
Arenicola spp. (polychaete) (continued) ascending loop of Henle (ALH), fluids 94–6 barnacles
bioturbation 450, 450 aspartate, fermentation 117, 473 beach height, thermal responses 468
hemoglobin levels 472 Astacus spp. (crayfish), permeability 496 invasion by 483
metamorphosis 367 Athene spp. (owl), acidosis tolerance 586 occurrence 484
respiratory integration 170 atmosphere parasitism 690, 690, 695
sperm maturation 372 pheromones 427
ventilation 149 acidification 615–16 sense organs 692
greenhouse effect gases 612
Arenivaga spp. (cockroach) ATP see adenosine triphosphate (ATP) barophilicity, marine animals 415
burrowing 624 ATP synthase, roles 20, 119 barracudas, lactate dehydrogenase 179
water vapor uptake 565, 634 ATPase see adenosine triphosphatase (ATPase) basal metabolic rate (BMR)
atrial natriuretic hormone 360
arginine phosphokinase 310 blood volume regulation 363 definition 127
arginine vasotocin, occurrence 496 atropine, occurrence 604 in desert rodents 626
Argopecten irradians (mollusc), jet propulsion 329 attractants scaling 40–2, 573
Argyroneuta spp. (spider), air bubbles 510 pheromones 427, 588, 594, 601 and taxonomy 41, 42
arid zones see deserts in plants 604 basilar membrane (cochlea) 272
aridity 521–622 auditory cortex 274 basking
auditory systems 272–4 butterflies 651
causes of 621 Aurelia spp. (jellyfish) caterpillars 651
aromatase 345 nerve net 248 and color 570–1
arousal, from torpor 215, 661 sulfate levels 417 and heat conservation 572
arrow worms, buoyancy mechanisms 418 auricle high-altitude animals 666–7
Artemia spp. (crustacean) earthworm 156 insects 570
fish 157 lizards 667
cryptobiosis 532 invertebrates 156 polar endotherms 656
drinking rates 531 vertebrates 157 reptiles 570
habitats 530 see also heart and temperature regulation 207–8
hemoglobin concentrations 531 Australian wood duck, digestion 607 terrestrial ectotherms 569–70
hormonal regulation of water balance 361 Austropotamobius pallipes (crayfish), heat death tundra endotherms 656
hyporegulation 532 BAT see brown adipose tissue (BAT)
hyposmosis 109 200 Bathylagus spp. (fish), bioluminescence 426
tolerance 79 autocrine communication 343, 343 bats
arteries autonomic nervous system 248 air pressure detectors 270
countercurrent heat exchange 206, 405–6, 440, autoregulation 314 altitudinal ranges 666
aversion conditioning 259 ammonia production 100
577, 658 avoidance echolocation 601
elastic 160 flight 339, 599, 672, 673
from heart 156, 160–1 and behavior 11–13
muscular 161 and climate 197 and scaling 44
pressure in 156 and environmental change 11 huddling 577
arterioles in estuarine animals 77–8, 455 hyposmotic urine 562
autoregulation 314 in freshwater animals 495 low basal metabolic rate 541
structure 161, 206 of host defenses 702–3 migration 216
arteriovenous anastomoses 161 in osmotic biology 76–9 torpor 214, 579, 579, 661
arthropods of predation, freshwater animals 517–18 beaches
chemoreceptors 276–7 strategies 12, 14, 456–7 exposure 431, 446
color vision 280 in terrestrial animals 566–7 pollution on 432
critical equilibrium humidity 87, 87 in thermal biology 197–8 sorting 450
cuticle transition temperatures 83 axogenesis 261–2 wave action 431
desert 622–3, 628, 629, 630, 632, 635–6 axons 223–31 see also littoral habitats; shorelines
diffusion barriers in 147–8 action potential propagation 230–1, 231 bears
exoskeletons 329 electrical analog of membrane 226 fur 658
as food 609 giant 230, 231, 232 migration 656
heart 156 growth cones 262, 263 occurrence 648
hygroreceptors 286 size factors 620
locomotion selective adhesion 262 snow dens 656
maintenance 263–6 bees
jumping 336–7 myelin sheath 230–1 aerobic scope 125
swimming 330–1 size–conduction velocity relationship 230, 232 body temperature 220
walking 334, 335 transport processes 264 in deserts 108, 624
marine, direct development 414 endothermy 190
mechanoreceptors 268–9 B cells, accumulation 701 feeding 636
motor neurons 319, 319 baboons, nose size 583 magnetic sensitivity 287
multineuronal innervation 319 bacteria metabolic water 108
muscle stretch receptors 321, 321 microclimates 547
nervous system 248–9, 250 in gastrointestinal tract 135 thermal regulation 205, 547, 575, 577, 627
terrestrial 548, 552, 554, 556, 557, 560–1, 563–5, in rumen 608 tracheae, parasites in 677
sulfur-oxidizing 537 trails 626
588–9, 596–8, 597 bacterial remediation, future trends 617 warm-up rates 577
see also arachnids; crustaceans; insects Baetis spp. (mayfly), respiratory conformity 507 see also Apis spp. (bee); Bombus spp. (bee)
Ascaris spp. (nematode) Baiomys taylori (mouse), critical arousal temperature beetles
anaerobic metabolism 683–4 burrows 626
eggs 689, 692, 693 661 cryptonephridial system 561
life cycle 683 Balaenoptera spp. (whale), migration 217 desert 624, 629, 630, 631, 633, 638
malate dismutation 684 balance 268–72 digestion 606
metabolism 683, 684 Balanus spp. (crustacean), occurrence 484
nervous system 248
oxygen uptake 682, 683 see also barnacles
see also nematodes Barbus neumayeri (fish), surface respiration 511
INDEX 717
freeze tolerance 186, 668 mechanisms 424–6 metabolic rates 41, 44, 129
larvae 652 occurrence 424 and ambient temperature 205
life cycles 670 regulatory mechanisms 424 and body mass 130
locomotion terrestrial animals 600
biomes, concept of 4 microclimates 547
jumping 337 Biomphalaria spp. (snail), respiration 507 migration 45–6, 216, 217, 656, 657
speeds 597 biosphere, acidification 615–16 monogamy 592
Malpighian tubules 561 biota nasal turbinal systems 104, 583, 583, 640, 644
microclimates 568, 623 brackish habitats 444–55 nectar feeding 81, 100, 639
montane, cutaneous evaporative water loss 668 desert 609 neonates 593
pheromones 601 endorheic lakes 529 nests 547, 592
plastrons 510 freshwater habitats 494–5 osmoregulation 86, 103
size factors 620 ice 538–9 oviparity 590
spiracles 150 littoral habitats 448–54 panting 210, 572
supercooling points 668 marine habitats 393–6 reproduction 414
vapor uptake 564 polar 646–7
wax blooms 556, 557, 630, 631 terrestrial 538–9 strategies 592
behavior biotic defenses 604 respiratory cycles 672–3
and avoidance 11–13 biotic habitats respiratory gas exchange 153
breeding, birds 594 characteristics 677 respiratory regulation 172–3
courtship 376 and parasitism 676 respiratory water loss 673
fixed action patterns 322 bioturbation, mechanisms 450, 451 sex determination 375, 592
maternal 380, 383 bipolar cells 281, 288 shivering 574
terrestrial animals 595 birds skin 83
mating 382–4 air pressure detectors 270 snow burrows 656
control 594 air sacs 146–7, 151 speeds 542
neuronal oscillators 322 basal metabolic rate 41, 42, 127 swimming 332
patterned activity 322, 323 body mass, and lower critical temperature 199 terrestrial 552
pheromones 381–6 body temperature, diurnal variations 203 thermal insulation 83, 192, 207, 658
and plant defenses 605 brains 250, 252, 254, 602 torpor, characteristics 215, 660
respiratory effects 506–7, 511 breeding behavior uricotely 100
as response level 11–13, 73 urine 562
rhythms 466, 477–8 courtship 376, 379 uropygial glands 207
thermal effects 180, 191, 207–8, 212, 219, 466, hormonal effects 594 ventilation 151, 152
burrowing 598, 620, 656 water balance 86, 103
503, 566, 625–8, 651 carotid rete, brain cooling 210, 640, 643 water loss, tolerance of 80, 633
water balance 531, 543, 552–4, 564 cell membranes 181 water permeability 83
see also cognition; learning; memory circulatory systems 159 see also wading birds
behavioral sensitization 255 color vision 280 Birgus spp. (crab), urinary ions 560
Benedenia spp. (fluke) countercurrents 659 birth, processes 595
parasitism, species diversity 680 in legs 579, 579 bivalves 117, 138, 404, 451, 457, 463, 464, 477, 495,
salinity tolerance 681 in nose 580
benthic animals 395–6 desert 624, 629, 633, 639–40, 644 498, 537
feeding 515 developmental plasticity in nervous system 255 burrowing 327, 328
food sources 430 diffusion barriers 147 and emersion 502
in freshwater habitats 494 diving 415, 505, 510 genetic variations 138
respiration 507 echolocation 601 jet propulsion 329, 329
see also deep sea; depth eggs 106, 107, 575, 592, 670 metabolic neurohormone 370
Bergmann’s rule 620 development 376, 379 muscle
beta-oxidation 123 eggshells 107
acyl-CoA 123 embryos, P50 591 adductors 316, 328, 329
mechanisms 123 endothermy 181, 189–90, 218, 220, 573, 574 catch state 314–15, 315
beta-sheets, structure 21 energy allocation 672 see also clams; cockles; mussels
bicarbonate 364 estuarine 445, 478, 479, 481 blood
levels, in hemolymph 584 excretory systems 563 distribution
regulatory mechanisms 90 feathers 83, 192, 658 and heat exchangers 205–6, 209–10, 405–6,
flight 43, 44, 339, 542, 592, 671–3
tetrapod kidney 97, 97 modes 339–40 510, 643
bicoid protein, sequences 22 muscles 339, 340 and heat loss 209–10
bile acids, and tapeworms 687 flightless 550, 644 freezing points 186
bilharzia 678 gular fluttering 213 gas distribution 585
hearts 157 melting points 186
see also Schistosoma mansoni (fluke) heat load tolerance 673 oxygen-carrying capacity, species differences
billfish, endothermy, regional 406 heat loss, thermal regulation 578
binocular vision 257 herbivory 607 165
bioassay, hormones 347 high-altitude, capillarity 670 as parasite environment 677, 678
biochemical reactions, temperature coefficients huddling 577, 657 pigments 669, 670
insulation 204, 505 roles 14, 162
177 legs, thermal gradients 579 use of term 154
biochemistry, and conformity 13 loop of Henle 562 see also body fluids; extracellular fluid (ECF);
biodeposition, mechanisms 450 lungs 146, 152, 153
biological oxygen demand (BOD), raw sewage 519 magnetic sensitivity 287 hemolymph
bioluminescence male sexual physiology 375 blood–brain barrier 264–6, 265, 344
marine 431, 435, 481 blood cells
emission wavelengths 426
extracellular 424 functions, species differences 162
luciferin–luciferase systems 424 types of 162
marine animals 424–6 blood feeders 684, 685, 686
marine fish, mechanisms 425 blood flow
and blood pressure 160
and heat distribution 205–6, 209–10
718 INDEX
blood flow (continued) and swimming 409 sensorimotor integration neurons 290
panting dogs 580 and temperature 574, 575, 629–31, 640, 642 somatotopic projection 289–90
terrestrial animals 586 and water flow 514 size variations 602
body size see body mass; sizes of animals temperature, and heater tissue 406–7
blood Pco2, species differences 171 body solids, and body water distributions 51 vertebrates 250–1, 253
blood pressure body surfaces voluntary movements 323–4
exchanges 80–4 brainstem 324
autoregulation 314 external, osmoregulation 84–7 Branchiostoma (amphioxus), central nervous system
and blood flow 160 see also cuticles; skins
closed circulatory systems 158 body temperature 188–221 250
diastolic 157 see also temperature; thermal acclimation; thermal breathing 149–53
patterns, during diving 441
systolic 157, 160 adaptation; thermal regulation bimodal 472, 510–11
blood temperature, and pH 167 bogs see also respiration
blood vessels breeding behavior
properties 160 characteristics 494 birds 594
productivity 494 desert animals 638 –9
vertebrates 160 Bohr shift freshwater animals 511
types of 160–1 definition 166 littoral animals 475
blood volume hemocyanins 166 marine mammals 414
mammals 40 hemoglobins 166 salmonids 217
regulation 363 Bombus spp. (bee) 652 terrestrial animals 587
BMR see basal metabolic rate (BMR) anatomy 578 breeding seasons 374, 376
BOD see biological oxygen demand (BOD) countercurrents 577 brine flies see Ephydra spp. (fly)
body cavities, patterns 15 locomotion cost 44 brine seeps, deep-sea 532
body compartments, exchange routes 14 nonshivering thermogenesis 576 bromeliads, water pools 527
body fluids thermal adaptation 575, 577, 578 brooding, freshwater invertebrates 512
antifreeze mechanisms 436–7 thermal regulation 575 brown adipose tissue (BAT)
brackish-water animals 457 warm-up recordings 578 heating, mechanisms 205
composition bombykol 277, 382 mammals 205, 576
structure 382, 601 metabolism 372, 661
elasmobranchs 432 Bombyx mori (sik moth), bombykol 382 and nonshivering thermogenesis 661
freshwater animals 496, 496 Bonellia spp. (marine worm), sex pheromones 427 structure 205
marine animals 397, 397, 399, 399 bones tetrapods 205
marine fish 433 calcium balance regulation 364, 365 Bryozoa 36, 412, 512
marine vertebrates 432, 433 size 36 buccal cavities
terrestrial animals 552–3, 553 bonitos, endothermy 406 and breathing 150, 171, 408
terrestrial arthropods 553, 554 book lungs parasites in 677
dilute, cold sea survival 436–7 arachnids 150 budding, marine animals 412
freezing points 186 terrestrial animals 581, 582, 582 Bufo spp. (toad)
hyposmotic use of term 145 arginine vasotocin synthesis 496
marine teleosts 434–5 Boophilus spp. (tick), cuticles 557 hygroreceptors 287
marine tetrapods 435 boreal animals bulbus arteriosus, vertebrates 157
melting points 196 fur 657–8 bumble-bees see Bombus spp. (bee)
patterns 15 torpor 660 Bunoderina spp. (fluke), occurrence 678
regulatory mechanisms 534 boreal forests buoyancy
responses, to osmotic concentrations 79 biomass 649 freshwater animals 514
water loss 79–80 boundary definitions 647 marine animals 417–22
see also blood; extracellular fluid (ECF); characteristics 649–50 burrowing
climate 649–50 as avoidance strategy 545
hemolymph fauna 650 and carbon dioxide sensitivity 586
body mass microclimates 650 costs 598
vegetation 650 in desert ectotherms 624–6
and abundance 42 boring, mechanisms 478 in high-altitude animals 667–8
carnivores vs. herbivores 610 Bosmina spp. (rotifer), feeding 515 hydrostatic skeleton 327–8, 328
bouncing locomotion 336–7 in large cold climate endotherms 656–7
changes, invertebrates 73 brackish habitats 444–55 in lizards 667
and extreme terrestrial habitats 620–1 see also estuarine habitats; littoral habitats mechanisms 327–8, 478
and fur depth, ungulates 642 brackish-water animals 448–83
and gill surface area 153, 409 Bracon cephi (sawfly), freeze tolerance 652 in marine animals 422
and ingestion rates 134, 135 bradycardia penetration anchors 328, 328, 478
and locomotion 43–4 and diving 440, 441 terminal anchors 328, 328
and lower critical temperature 199 fish 170 in terrestrial vertebrates 598
and maximum velocity 46 in hypoxia 410, 509 and water balance 563
and metabolic rates 45, 130, 131 bradymetabolic, use of term 189 burrows
brain cooling 210, 640, 643 depth, vs. shore height 470
mass exponents 130 see also carotid rete; countercurrents food storage 625
and optimal velocity 46 brains 250–5 humidity 625
and oxygen consumption 131 insects, neurohormones 348 microclimates, equable 625
and oxygen demand 132 invertebrates 249 montane habitats 667–8
patterns 47 membranes, homeoviscous adaptation 181 problems 625
scaling issues 37–40 and sensory coordination 602 temperatures 623
and thermal inertia 197 sensory information processing 287–90, 289 bursicon 366
and thermal time constant 197 butterflies
and thermoregulation 197–8, 204, 219, 469, 504 feature detectors 290 aposematism 605
vs. latitude 620 projection centers 289 basking 651, 667
and water content 51
see also scaling; sizes of animals
body shape
and allometry 36–9
and diffusion 144
INDEX 719
eggs 667 brain cooling 643 osmoregulation 108
hemolymph concentration 554 drinking rates 642 oxygen-affinity curves 472
migration 217, 651 humps 643 cardiac muscle 316–18, 317
phagostimulants 605 metabolic water 108 action potentials 317, 318
toxification strategies 605 montane habitats 664 contractile fibers 316
see also caterpillars; moths strategies 641–3 pacemaker (conducting) fibers 316–17
Bythograea spp. (crab) sweating 211 cardiac output, control signals 170
habitats 538 urine concentrations 643 cardioactive peptides 371
respiratory pigments 411 water conservation 642–3 cardiovascular changes, during exercise 209
water loss 642 Cardisoma spp. (crab)
cacti, occurrence 623 camouflage 371 oxygen-affinity curves 472
cadherins 239, 262 color change 211, 467, 572, 630 urinary ions 560
Caenorhabditis (nematode) marine animals 424 Caretta spp. (reptile), sex ratios 591
ventral 424 caribou, migration 649
neuromuscular junction 297 cAMP see cyclic AMP (cAMP) carnivores
osmosensing 274 cAMP-dependent protein kinase see protein kinase A freshwater habitats 515, 517
calcitonin 357 cAMP phosphodiesterase, roles 30 and herbivores compared 610
calcium balance regulation 364 Camponotus spp. (ant) P50 values 670
phosphate balance regulation 364 metabolic rates 629 strategies 609
calcitriol 364 temperature coefficients 629 terrestrial animals 543, 609
calcium canalization 11 carotid arch, chemoreceptors 171
and cAMP interactions 31 use of term 11 carotid bodies, vertebrates 172
concentrations 70 Cancer spp. (crab) carotid rete, brain cooling 210, 406, 643
hyperosmotic regulation 457 carp
in blood 78, 400, 496 membrane fluidity 470 cold acclimation 181, 182
in cells 30, 60, 65 volume regulation 463 myosin ATPase activity 178
hormonal regulation 364, 365 capacitance vessels, use of term 161 Carpachne spp. (spider), locomotion 626
muscle contraction 291, 312, 313 capacity acclimation, use of term 201 cassava, toxicity 605
cross-bridge cycle initiation 303, 304 capillaries caste pheromones 384
mechanisms 314 roles 154 catabolism, mechanisms 112
sarcoplasmic reticulum accumulation/release structure 161 Cataglyphis spp. (ant), respiratory evaporative water
capillarity, birds, high-altitude 670
304–5 carbohydrates loss 634
smooth muscle 312, 314 availability 543 catch muscles 314–15, 315
troponin C binding 304 compensatory solutes 73 catchin 315
photoreceptor adaptation 278 as energy sources 118, 125, 607–8 catecholamines 237, 345, 355
presynaptic events 234, 235
release 406–7 parasites 683 activity 30
resorption 90 reserves in ecosystems 543 cardiac muscle regulation 317–18
roles 30–1 carbon dioxide effects 357
as second messenger 30 atmospheric 610–14 metabolism regulation 370
synaptic facilitation 245 roles 441
calcium/calmodulin-dependent kinases 245 patterns 611 see also epinephrine; norepinephrine
calcium channels 30, 32, 59–60, 406 dissociation curves 168 caterpillars
synaptic transmission 234, 255 effects basking 651
voltage-gated 234 feeding strategies 605
muscle contraction 303 in fresh water 537 hemolymph concentrations 554
calcium phosphate, as ice-nucleating agent 652 on oxygen binding 165–6 lifespans 655
calcium pumps (Ca2+-ATPase) 64, 114, 406, 461, in respiration 173 locomotion 596
on terrestrial animals 613–14 overheating avoidance 566
501 in greenhouse effect 610–11 toxification strategies 605
caldesmon 312, 314 levels, effects on oxygen-carrying capacity 166 cation channels see potassium channels; sodium
Calidris canutus (bird), migration 656 loss 171, 505
Callinectes spp. (crab) terrestrial animals 586 channels
profiles, lakes 506 cation pumps see calcium pumps; sodium pumps
hemocyanins 472 regulatory mechanisms 543
hypoxia 508 in sea water 408 (Na+/K+-ATPase)
oxygen consumption 143 sensitivity reduction 586 cats, reproduction 379
sex pheromones 427 sensors 172–3, 586 Cauricara spp. (moth), water loss 631
Calliphora (fly) solubility 144 CD see collecting duct (CD)
diapause 369 transport 168–9 cecum
rectal papillae 561 in erythrocytes 168
calmodulin 235, 305 as waste product 119 and fermentation 607, 608–9
binding 30 see also hypercapnia water balance 102
smooth muscle contraction 312 carbon, emission rates 612 CEH see critical equilibrium humidity (CEH)
calorimetry, whole animal apparatus 127 carbon monoxide, neurotransmitter function 238 cell adhesion molecules 237, 262
calreticulin, occurrence 30 carbonic anhydrase, catalysis 168 cell contents
calsequestrin 304 Carcharodon carcharias (shark), endothermy, concentrations 70
occurrence 30 regulatory mechanisms 71–4
Calyptogena spp. (bivalve) regional 406 cell death
digestive system 537 Carcinus spp. (crab) heat effects, mechanisms 187
spawning 414 thermal limits 187
sulfide-binding proteins 537 copper uptake levels 482 cell membranes
symbiosis 537 gills 145 bilayer 55, 56
CaM see calmodulin hemocyanins 165 brain, homeoviscous adaptation 181
camels 641–3 hyperosmotic regulation 457 cholesterol content 55, 56
basking 576 invasion 483 composition and fluidity 55, 178, 416, 468, 503,
body temperatures 202, 211, 642 membrane fluidity 470
536
720 INDEX
cell membranes (continued) cardioactive peptides 371 chill injury, species differences 184
electrical excitability 223–4 central nervous system 249, 251 chimaera, ureo-osmoconforming 433
electrochemical balance 58–61 direct development 414 Chiromantis spp. (frog)
evolution 70 eyes 424
exchange site 14 gas floats 419 cooling 573
fluidity, detection 180 glycolysis 117 excretory modes 100
ion pumps 62–5 jet propulsion 328 permeability 555
junctions 67–9 kidney 401 chironomids (midges)
lipids 180 neurohormones 348 in lakes 492, 493
osmosis 57–8 reproduction, hormonal regulation 373 oxygen consumption 507
permeability 56–8, 220 respiration countercurrent 149, 408 in puddles 526
diffusion 56–7, 57 sulfate levels 417 chitin
osmotic 57–8, 58 see also Nautilus spp. (cephalopod); Octopus spp. in cuticles 82, 83, 147, 556, 588
pressure adaptation 416 in eggshells 588
properties 55–6 (cephalopod); squids indigestibility 609
protein-mediated movements, “gate” and “ferry” Cerastoderma edule (bivalve), freezing resistance chitinase, occurrence 609
models 62 chloride cells 84, 86
resting potential 224 471 salt transport 85, 435, 462, 501, 534
scanning freeze fracture electron micrograph 57 ceratopogonids, in puddles 526 structure 85
semipermeable, osmosis 58 cercariae use of term 85
structure 55–6 chloride channels 86, 435
temperature effects on 180–2 anaerobic respiration 684 chloride pumps 534
thermal adaptation 180–1 life cycles 683 chloride shifts, mechanisms 168
transport mechanisms 70 skin penetration 691, 703 chlorine, levels, increase 615
water channels 57 see also flukes chlorofluorocarbons (CFCs)
cerci 273, 276 effects, on ozone layer 614–15
cell volume, regulatory mechanisms 72 cerebellum 251, 290, 290, 325 lifespan 614
cells cerebral cortex 252 cholecystokinin 357
cortical fields 252, 255 cholesterol
in adaptive immunity 701 voluntary movement 323, 324–5 effects on homeoviscous adaptation 180
B-cells 701 cerebral hemispheres 252 hormone precursor 344
evolution 70 cerebrospinal fluid 264 hydroxymethylglutaryl-CoA control 34
heater, thermogenesis 406, 407 cerebrum 252 chordates, central nervous system 251
high-temperature effects on 187 cestodes see tapeworms chordotonal organs 274
in immune systems 700 cetaceans chorion 379
ionic concentrations 68–74, 399 communication systems 428 structure 107, 107
kidney, ultrastructure 92 see also dolphins; whales chorionic gonadotropin 359, 379
low-temperature effects on 184–6 CEWL see cutaneous evaporative water loss (CEWL) chorionic thyrotropin 380
lymphocytes 701 CFCs see chlorofluorocarbons (CFCs) chromophores 278, 371, 423
memory 23 cGMP see cyclic GMP (cGMP) chromosomes
as osmotic effectors 73, 74 Chaetopterus spp. (polychaete), ventilation 149, crossing-over 25
permeability 56–61, 58, 72–4 gene organization 25
phosphorylation 20 150 and sex determination 592
prokaryotic 181–2 chameleons, color changes 571–2 Chrysemys spp. (turtle), lactate buffering 511
regulatory mechanisms 496–9 cheetahs, speed 542 Chthamalus spp. (crustacean), occurrence 484
self vs. nonself, in host–parasite systems 697 chelicerates see also barnacles
surfaces, active processes 66–70 cicadas
T-cells 701 terrestrial 548 in deserts 624, 639
T-helper 701 see also mites; scorpions; spiders tymbal muscles 133
temperature effects on 180–2 Chelydra spp. (turtle), sex ratios 591 cichlids
see also blood cells; epithelial cells; erythrocytes; chemical control systems 342, 342–87 ammonia excretion 534
chemical defenses, plants 604, 604–5 in lakes 493, 514
hair cells; hemocytes; leucocytes; muscle cells; deserts 637 reproduction 514
neurons; phagocytes; sensory receptors chemical messengers 342, 343 Cicindela spp. (beetle), microclimates 568
cellulases, roles 603 types 342–3 cilia
in digestion 606 chemical potential, and concentration 54 function, thermal acclimation 404
cellulose chemical reactions, temperature coefficients 176–7 surface gliding 326
digestion 605 chemical senses 274–7 circadian rhythms 477
food content 602 freshwater animals 515 color change 467
ingestion 135 littoral animals 455, 479 locomotion 477–8, 554
solubilization 607, 608–9 marine animals 426–7 migration, parasites 678
centipedes terrestrial animals 600–1 torpor 638
gait 597 chemical signaling and water balance 554
locomotion, speeds 597 littoral animals 479 circatidal rhythms 477–8
reproductive strategies 588 marine animals 426–7 circulatory systems 154–62
terrestrial 548, 563, 588, 589 parasites 694 circuits 158
tracheae 583 terrestrial animals 600–1 closed 154
see also millipedes see also hormones; pheromones
central pattern generators 322, 324 chemicals, pollution 520–1 blood pressure 158
command system 322 chemoreception see chemical senses evolution 154
cephalization 247, 249, 251 chemoreceptors exchange sites 143
cephalopods feeding 108 freshwater animals 509
absence from fresh water 514 in parasites 694 open 154
blood vessels 156 and pheromones 277, 427, 600–1 portal 158
body color changes 372 respiratory 170
chemotaxis 383
Cherax spp. (crayfish), oxygen uptake 501
pressure variations 161 cold habitats INDEX 721
pulmonary 158 endurers 655–62
pumps 155–6 littoral animals 470–1 marine animals 76–9
roles 154 terrestrial, characteristics 645–50 in osmotic biology 76–9
species differences 155, 159 terrestrial animals 566, 645–63 and physiology 13
systemic 158, 158 strategies 650–62 and regulation compared 12, 13
Cirrichthys spp. (fish), specific dynamic action 137 types of 645–50 and respiration 471
citrate, as intermediate 119 see also polar habitats; tundra strategies 12, 14, 457–8
citric acid cycle see Krebs cycle connectin 296
cladocerans cold hardiness, concept of 184 connexons 246
brooding 512 Colias spp. (butterfly) contamination, and eutrophication, freshwater
cyclomorphosis 513
feeding 515 basking 651, 667 habitats 522
cladogenesis, mechanisms 6 migration 651 continuous lability, use of term 10
clams collecting duct (CD) contraction of muscles see muscle contraction
acidity 501 hormonal control 362–3 contramensalism, use of term 675
amino acids 74 roles 95 conus arteriosus, vertebrates 157
spawning 414 collembolans cooling 53, 84, 105, 196, 197, 415, 469, 557, 580,
thermal acclimation 202 desert 623, 624, 638
see also bivalves jumping 597 639–40
classic (Pavlovian) conditioning 259 colligative cryoprotectants, accumulation 184 regulatory mechanisms 208–12
climate colloid osmotic pressures, factors affecting 162 see also brain cooling; evaporative water loss
and avoidance 197 color
change 176 and basking 570–1 (EWL)/cooling
sensitivity, models 611 desert animals 629–31, 640, 642 copepods
terrestrial habitats 543–7 gazelles 642
see also microclimates high-altitude animals 666 brooding 512
clines, use of term 28 hormonal regulation in ectotherms 371–2 eggs 512
Cloeon spp. (mayfly), regulation 507 patterns, insects 571 larvae, buoyancy mechanisms 418
cnidarians and temperature 194, 467, 570–2, 629–30 coprophagy 607
avoidance strategies 457 and thermal radiation 194 copulation, pheromones 383
buoyancy mechanisms, and sulfate extrusion color changes 207, 211, 579, 630–1 coral reefs
desert animals 630–1, 640 distribution 395, 397
419 polar animals 651 thermal adaptation 470
chemical signaling 426–7 thermal regulation 211, 570–2 corals, microalgal symbionts 480, 481
circulatory systems 155 color vision 278–80, 423–4, 479, 600–1 cornea 280, 281
extracellular fluids 497 commensalism, use of term 675 corpora allata 348–9, 373
feeding 515 communication systems corpora cardiaca 348
larvae 414 at altitude 671 corpus luteum 377, 378
nerve nets 247, 248 marine 428–9 corpus striatum 252
parasitic behavior 511 in parasites 695 corpuscles of Stannius 355, 364
see also anemones; corals; jellyfish terrestrial animals 600–2 corticosteroids 345
coarse particulate organic matter (CPOM), patterns see also hormones; nerves body temperature regulation 372
comparative method 7–8 stress responses 370–1, 372, 381
490 comparative physiology corticotropin see adrenocorticotropic hormone
coastal energy 483 field of study 3 corticotropin-releasing hormone (CRH) 355
coastlines overview 3–4 release 595
problems 7 cortisol 355
alterations 482–3 compensatory osmolytes see osmotic effectors control of release 371
classification 445 complement, in host–parasite systems 701–2 effects 370–1, 371
invasions 483 compound eyes 280, 282–4, 284 cortisone, release 595
Mediterranean habitats 550 apposition 284, 285 Cotesia congregatus (wasp), host metamorphosis
tourism 482–3 superposition 284, 285
types, global distribution 446 concentrations inhibition 695
see also shorelines aqueous solutions 53–4 cotransport see symport
cochlea 272–4, 273 of cell contents 70 countercurrent exchange 205–6, 406
amplitude coding 274, 275 gas 144
frequency detection 272, 275 measurement 54, 54 mechanisms 94, 94
tonotopic nature 272, 274 urine 92–8 countercurrent multiplication 410, 562
cochlear nerve 274 see also osmotic concentrations; urine
cockles, freezing resistance 471, 471 mechanisms 94, 94–5
cockroaches concentrations countercurrents
desert 623, 625, 634 condensation, and desert animals 633
peptide hormones 362 conditioning 259 Bombus spp. 577
resorptive epithelium 93 conductance 228 freshwater endotherms 440, 505
sequestration 102 marine mammals 440, 440, 658–9
survival potential 617 see also thermal conductance nasal 104, 106, 562, 640
vapor uptake 564, 634 conduction see neurons; thermal conduction polar animals 659
cocurrents, ventilation 151 cones 281, 282 rectal, concentration systems 98–9, 562
coefficient of gut differentiation 603 respiratory 104, 151, 153, 406–8
coelacanths, ureo-osmoconforming 433 receptive fields 281 in siphuncle 419
Coenobita spp. (crab), osmosis 564 confidence limits, linear regression 38, 38 thermal 205–6, 206, 208, 572, 578–9, 640
coevolution, use of term 604 conformity urine concentration 93–8, 99, 562
cognition 261 courtship behavior 376
cold blooded, use of term 188 and biochemistry 13 pheromones 383
ectotherms 565 coxal glands 362
and environmental change 11 arachnids 559
freshwater animals 507 terrestrial arthropods 560
coxal sacs, terrestrial insects 564
CPK see creatine phosphokinase (CPK)
CPOM see coarse particulate organic matter
(CPOM)
722 INDEX
crabs crevices, aquatic habitats 527–9 salt-regulating hormones 361
amino acids 74 CRH see corticotropin-releasing hormone (CRH) salt uptake 84, 496, 633
antennal glands 559 crickets size 36
bimodal breathing 473, 511 smooth muscle 314
circatidal rhythms 477–8 deserts 623 sodium loss 459
cold acclimation 461 tympanic organs 273, 276 swimming 330, 331, 332
communication systems 600 Cricotopus spp. (midge), habitats 530 terrestrial 548, 588, 600
copper uptake 482 cristae, in mitochondria 683 thermal tolerance 200
deep-sea vents 538 critical arousal temperature 215, 661 ultrafiltration 89
diffusion barriers 148 critical equilibrium humidity (CEH), arthropods urine concentrations 499
eggs 512 vapor uptake 564–5
gills 145 87, 87, 564 vision 600
hemocyanins 165, 472 critical partial pressure walking 334
herbivory 604 water stores 457
hyposmotic 400 definition 142 water uptake 86, 87
hypoxia 508 species differences 143, 143 see also amphipods; copepods; crabs; crayfish;
invasions 483 crocodiles
littoral habitats 451 blood circulation 157, 158 woodlice
lungs 145, 582 eggs 590 crustecdysone 368
mating 588 salt glands 435 cryoprotectants 177, 184
membrane fluidity 470 sex ratios 591
osmoregulation 108, 457, 556, 559–60, temperature-dependent sex determination 591 synthesis 177, 184, 185
563–4 crosscurrents, ventilation 151 types of 184
oxygen-affinity curves 472 see also countercurrents cryptobiosis 466, 495, 513, 527–9, 547, 623, 624,
oxygen consumption 143 crossed extension reflex 320, 321
parasites 681, 690, 696 crustacean cardioactive peptide 368 637
reproductive strategies 588 crustaceans control mechanisms 527–8, 530
respiratory pigments 164, 411, 472, 508 acidification effects 523 definition 637
respiratory systems 145, 150, 408, 473, 582, 669 active secretion 92 eggs 513
rhodopsin absorbance 600 adenosine triphosphate 115 mechanisms 527
sex pheromones 427 antennal glands 89, 499, 531, 559 in salt lakes 532
swimming 330 ATP turnover rates 473 as survival strategy 528
terrestrial 559–60, 588, 600, 604 blood pH 534 cryptogams, deserts 623
in thermally extreme waters 538 body mass, and gill surface area 409 Cryptomys spp. (mouse), nests, ambient temperature
urine 500, 560 brackish habitats 454
vision 600 breathing modes 472 574
volume regulation 463 brooding 512 cryptonephridial system, terrestrial insects 561,
in water pools 526, 527 buoyancy mechanisms 418
water uptake 84, 87, 472, 563–4 central nervous system 249 562, 633, 669
see also crustaceans central pattern generators 322, 324 cryptozoic animals 547, 553, 554–7, 566
chitinase 609 crystalline cone 282
cracks, aquatic habitats 527–9 circulatory systems 155 ctenophores, buoyancy mechanisms 419
crane flies color change 211, 467 Culex spp. (mosquito)
cryptobiosis 531
ice-nucleating proteins 652 drinking 531 hemolymph, and sodium concentrations 461
life cycles 670 endocrine system 349, 350 as vector 691
Crangon spp. (crustacean) escape reactions 322, 324, 325 cupula 271, 272
body color changes 372 excretory systems 500 curare, shivering mediation 204
mortality factors 484 extracellular fluids 497 cursorial gait 334
cranial nerves 253 eyes 424 cutaneous evaporative water loss (CEWL) 80, 580
Crassostrea spp. (bivalve), thermal acclimation 201 gills 84, 145, 400, 455, 507, 509 birds 580
crawling 334–6 hemocyanins 163–4, 511, 585 desert animals 631, 645
hydrostatic skeleton 327 hemoglobins 531 desert insects 631
littoral animals 479 in high salinity 530, 531 and evaporative cooling 573
marine animals 422 hyposmosis 109, 459, 533 frogs 573
mechanisms 422, 479 hypoxia 410–11, 472 minimization 83
metachronal rhythm 322 ion uptake 84, 496 montane beetles 669
terrestrial animals 596–7 kidneys 560 panting 211
crayfish larvae 412 reptiles 557
eggs 512 life cycle 512 supplementary 211
excretory systems 500 lungs 145 sweating 211
eyes 514 metamorphosis 368 terrestrial animals 80, 81, 211, 554, 580
habituation 259 molting 368 cutaneous patches, terrestrial animals 582
heat death 187, 200 muscle fibers, multiterminal 319 cutaneous respiration see skins
hyperventilation 509 osmoregulation 108–9, 399, 457, 458, 461, 530, cuticles
osmoregulation 108 arthropods 80–2, 147–8, 556
synaptic integration 254, 257 531, 531 direct absorption, in parasites 685
see also crustaceans oxygen consumption 507 hydrophilic 565
creatine phosphate 331 permeability 458, 459, 531 jumping locomotion 336–7
creatine phosphokinase (CPK) 310 pheromones, mate location 382–3 lipids 82, 83, 556–7
roles 114 reproduction 588 and locomotion 597
creatinine, occurrence 101 mechanoreceptors 268–9, 269
creeping locomotion, pedal waves 326–7 hormonal regulation 374 molting process 366
crepuscular animals, use of term 549 reproductive strategies 588 parasites 687
respiratory systems 409 permeability 58, 80–1, 554
salinity tolerance 79, 466, 469, 470
in salt lakes 530 regulation 362
and pollution 523
structure, insects 556
INDEX 723
tanning 366 dendritic spines 239 and permeability 81
terrestrial animals 83, 554–5 deoxycholic acid, parasite tolerance 687 and respiratory quotient 126
and water loss 80–1, 631–2 deoxyribonucleic acid (DNA) see DNA and specific dynamic action 136
see also skins depressed metabolism see hypometabolism diffusion 55
cuttlefish depth 411 barriers 147–9
cuttlebone structure 420 and body fluids 61
gas floats 419 and hydrostatic pressure 415, 514 coefficients 55, 55, 103
sulfate levels 417 receptors 269
see also cephalopods Dermatophagoides spp. (mite) gases 148
cyanide, occurrence 605 habitats 617 Fick’s law 55, 55
cyanobacteria, prokaryotic 541 hygroscopic fluids 564 in respiratory systems 36, 84, 143, 144
cyclic AMP (cAMP) Derogenes varicus (fluke), thermal adaptation 681 temperature coefficients 177
activation 654 desaturases see also facilitated diffusion
and calcium interactions 31 catalysis 181 diffusional flux 55
peptide hormone signaling 344 levels, in carp 182 digeneans see flukes
protein kinase A activation 32 descending loop of Henle (DLH) digestion
roles 30 fluids 95–6 and gut form 102
synthesis 30, 683 roles 94–5 heat production 205
cyclic GMP (cGMP), roles 32 desert animals 621, 623–44 ruminants 607–8, 608
cyclomorphosis, freshwater animals 513, 513 desert endurers 621 see also diets; gastrointestinal tract (GIT); guts
Cyclops spp. (crustacean), brooding 512 desert evaders 621, 624–39 dihydropyridine receptors 297, 305, 306
cyprinids, thermal acclimation 404 desert evaporators 621, 639–41 dimensions, of variables 37
Cyprinodon spp. (fish), habitats 530 desertification 644, 645 dimethylsulfoniopropionate (DMSP), as antifreeze
cytochrome c, electron transfer 119 deserts 621–4, 622
cytochrome oxidase anthropogenic issues 644 compound 539
activity 202 desmin 296 Dimetrodon spp. (dinosaur), basking 208
electron transfer 119 determination in neuronal development 262 dinosaurs
cytochrome reductase, electron transfer 119 detoxification systems, herbivores 603
cytochromes deutocerebrum 249 digestion, as heat source 205
in anaerobic metabolism 683 development endothermy 191, 220
in electron transfer system 119, 141 and diapause 638 turbinates, absence of 220
cytokines direct, marine invertebrates 414 Dionchus remorae (fluke), host defense exploitation
effects 699 environmental factors 4, 10, 666
and immune responses 697 fetal, terrestrial mammals 595 704
types of 697, 698 hormonal regulation 364–9 dioxins, pollution 432
cytoplasm parasites 623, 676, 682, 683 2,3-diphosphoglycerate (2,3-DPG), as hemoglobin
density 415 and phenotype 7
glycolysis in 115–17 in toads 639 affinity modulator 167, 669
cytoplasmic degradation, mechanisms 24 viviparous 655 Diphyllobothrium latum (tapeworm), vitamin B12
cytoskeletal proteins, myofibrils 296, 297
mechanisms 595 affinity 687
DAG see diacylglycerol (DAG) development time, and temperature 188, 189 Dipodomys spp. (kangaroo rat)
dams, and freshwater habitats 523 developmental heterochrony, use of term 11
Danaus plexippus (butterfly) developmental plasticity see phenotypic plasticity feeding 637
dews, and water uptake 86, 563 nasal heat exchange 635
chemical defenses 605 diacylglycerol (DAG) 274 water retention 633
migration 217, 381, 651 Dipsosaurus spp. (lizard), thermal regulation 570
Daphnia spp. (crustacean) peptide hormone signaling 344 Diptera (flies)
brooding 512 roles 31, 31, 32 blood concentration 552
cyclomorphosis 513 eggshells 107
feeding 515 in aerobic metabolism 125 excretion 102, 531
phenotypic plasticity 513 synthesis 31 feeding 609, 685, 686
reproduction 374 diapause freeze tolerance 652
see also cladocerans in copepods 512 larvae 589
Darcy’s law of flow 160 definition 212, 637, 638 life cycles 671
Dasyhelea spp. (midge), in puddles 526 in insects 10, 212–14, 566, 652 parasitism 677
Davson–Danielli phospholipid bilayer model 55 rectal papillae 561
DCT see distal convoluted tubule (DCT) regulatory mechanisms 214, 369 respiration 584
DDT see dichlorodiphenyltrichloroethane (DDT) and life cycles 670–1 water loss 585
decapeptides, occurrence 125 regulatory mechanisms 214 see also Drosophila spp. (fly); mosquitoes; parasitic
decapods see crabs; crayfish
deep sea 189, 411 hormonal 369 flies
brine seeps 532 diapause hormone 369 discontinuous ventilation cycle (DVC)
fauna 416 Diaptomus spp. (copepod crustacean), brooding
deer, antlers, scaling problems 40 desert animals 635
deer mice 512 mechanisms 584
burrows 625, 667 Diceroprocta spp. (cicada) diseases, and freshwater contamination 521
water loss 668 distal convoluted tubule (DCT), roles 95
defoliation, surveys 616 evaporative cooling 639 Ditylenchus spp. (nematode), cryptobiosis 528
deforestation, and freshwater habitats 524 sweating 572 diving
dehydration tolerance see water loss dichlorodiphenyltrichloroethane (DDT), toxicity blood pressure patterns 441
11-cis-3-dehydroretinal, as visual pigment 423 blood volume 40
dendrites 223 520, 521 freshwater animals 510
Diclidophora merlangi (fluke), blood feeding 685 hematocrit 162
Dictyostelium (slime mold), myosin 303 hypoxia 115
diets insects 495, 510
marine animals 415, 441
assimilation efficiencies 134 respiration strategies, marine vertebrates
composition 134
effects on basal metabolic rate 41 440–1
and excretion 89, 102, 108, 563, 606 DLH see descending loop of Henle (DLH)
and membrane composition 180 DMSP see dimethylsulfoniopropionate (DMSP)
724 INDEX dwellings, as man-made habitats 617 and terrestrial habitats 677
dynein 264 thermal adaptation 682
DNA dysphotic zone 423, 423 transmission 688
in haploid genome 24 dystrophin 296 use of term 677
information transfer, to proteins 21 water balance 681
organization 24–5 ear ossicles 272 see also fleas; leeches; mites; ticks
roles 17 eardrum (tympanic membrane) 272 ectotherms
transcription 21 early response genes, metamorphosis 365, 366–7 Allen’s rule 649
and UV-B radiation 615 ears body temperatures 189, 191, 401–2
DNA ligase, roles 25, 26 insects 273, 274, 276 elevated 682
DNA polymerase, roles 25, 26 vertebrates 272 preferred 198
DNA repair see also hearing; mechanical senses bradymetabolic 189
earthworms cold habitats 651–62
mechanisms 25 burrowing 549 conformity 565
types of 25 chitinase 609 cytochrome oxidase activity 202
DNA repair nucleases, roles 25, 26 excretory systems 103, 557, 558 desert 620, 637–9
dogs feeding 587, 603 diapause 212–14
aerobic scope 42 heart 155 estivation 213
erythrocytes 168 locomotion 596, 596 freshwater 503–5, 513
panting 213, 580 heat production 198
dolphins metachronal rhythm 322 ingestion rates 135
communication systems 428 lungs 145, 582 littoral 550
echolocation 428 nephridia 557 marine 401, 436
see also cetaceans osmoregulation 557 metabolic rate 371–2
domains, protein, structure 21 reproduction 372 metabolic rate–temperature curves 128, 131
Donnan equilibrium 58–9, 61, 399 migration 216
semipermeable membranes 58 strategies 587 mitochondrial density 202
dopamine 237, 314 respiration 103, 145, 582 mole rats 638
command network regulation 323 urea production 100 montane 667
roles 32 see also annelids; Lumbricus spp. (oligochaete); nocturnal, thermal regulation 566
nonshivering thermogenesis 205
in gill processing 560 oligochaetes parasites 682
sodium pump regulation 360 ecdysiotropin (prothoracicotropic hormone) 348 polar 651
dormancy ecdysis-triggering hormone 366 regional endothermy 550
freshwater animals 512 ecdysone 348, 349, 365, 593 respiratory pigments 165
terrestrial animals 566 shivering 203
see also estivation; hibernation; torpor apoptosis induction 366–7 sizes 191
dorsal root ganglia 250 diapause regulation 369 terrestrial 566–73
2,3-DPG see 2,3-diphosphoglycerate (2,3-DPG) early response gene activation 366–7 thermal acclimation 201–2
Dracunculus medinensis (nematode), parasitism heat shock protein regulation 182 thermoregulation 202, 203, 212–14
mimics 604 torpor 212–14
688 molting regulation use of term 189
dragonflies ectothermy
crustaceans 368 advantages 218
flight muscles 673 insects 365 use of term 189, 190
respiratory systems 147 in parasites 695 ECV see extracellular volumes (ECV)
warm-up recordings 578 release 593 eels
Dreissena spp. (bivalve) ECF see extracellular fluid (ECF) parasites 681
invasions 524 Echiniscus spp. (tardigrade), cryptobiosis 528 swim-bladders 421
reproductive output 512 Echinococcus granulosus (tapeworm), and bile acids efferent (motor) neurons 247
stenohaline characteristics 496 effluent discharge, effects on rivers 519
volume regulation 498 688 egg development neurosecretory hormone 373
drinking echinoderms egg-white protein mRNAs, estrogen effects on 29
behavior 363 eggs
rates, regulatory mechanisms 564 freshwater, absence from 495, 495 arachnids 589
water gain 108 gills 145 birds, respiratory problems 670
Dromaius spp. (emu), strategies 644 ionic regulation, lack of 399 butterflies 667
Drosophila spp. (fly) larvae 412 care, littoral animals 476
bicoid protein 22 nerve nets 247 cleidoic 590, 591
cuticles 556 neurohormones 348 cooling 644
ecdysone-induced apoptosis 367 reproduction, hormonal regulation 373 cryptobiosis 513
flight 338 skins 82 desert animals 638
heat shock proteins 34, 284 tube feet 329 development, control 595
mutations 27 echolocation fish, buoyancy mechanisms 418
neuromuscular junction 297 bats 601 freshwater animals 512, 587
parasites 681 estuarine animals 480 hatching 595
reproduction 383 freshwater animals 515 maturation, control 595
respiration 585 littoral animals 480 parasites 678, 688, 689
RNA roles in 26 marine mammals 428 pH sensitivity 693
thermal acclimation 201 terrestrial animals 601, 601 trigger stimuli 691
water loss 631 eclosion 348 pelagic 587
dry habitats 621–45 eclosion hormone 366 post-hatching care 595
Dryas integrifolia (butterfly), basking 651 ecological density, scaling 42
ducks ectoparasites
behavior manipulation 696, 696 feeding strategies 685
blood pressure, patterns 441 respiratory adaptation 682
dunes, temperature and humidity patterns 622 salinity tolerance 680–1
DVC see discontinuous ventilation cycle (DVC) settling sites, detection 688
on skins 677
temperature control 592 endorphins 238 INDEX 725
terrestrial animals 586–7, 588–9, 590 parasitic secretion 703
water balance 105–7 in excreted products 137
eggshells, structure 107 endoskeletons 329, 330 in metabolism 134
eicosanoids endothelins 359, 360 energy storage
hormones 345 endotherms 189–203, 218–20 in extreme terrestrial habitats 621
precursors 32 fats 122–3
Eisenia (annelid), reproduction 372 aquatic, shunt vessels 209 in locomotion 597–8
El Niño, mechanisms 467 body temperatures 189, 191, 202–3, 203 migration 657
elasmobranchs cold habitats 620, 649, 650 and size 14
body fluids, composition 432 cytochrome oxidase activity 202 energy supply
electroreception 429, 515 desert 620, 635, 638, 641–3 for growth and production 137–9
endothermy 404 fever 682 and metabolism 112–39
freshwater 499 fish 404 muscle contraction 309–10
gills 145 freshwater 505, 510, 514 enhancers, roles 23
heart 157 heat production 202 Enhydra lutra (otter), insulation 658
myotome muscles 331 hibernation 215 enkephalins 238
neurosecretory cells 359 hypothermia 214–15 enteroglucagon 357
rectal glands 86, 109, 433 ingestion rates 135 Entobdella soleae (fluke)
trimethylamine oxide, use of 101, 417 insulation 202 life cycles 689
urea, uses of 90, 417, 432–3 lungs 145 parasitism 682
see also fish marine 404, 432, 439–40 environment–genotype interrelationships 4
elastase inhibitors, secretion 703 metabolic rate–temperature curves 128, 131, environmental change, physiological responses
electric fish 515, 516
electric membrane potential, determination 59 203 11–12
electric organs 287 migration 216 environmental disturbance, and adaptation 6
marine fish 429 mitochondrial density 130–1, 202 environmental effects, on phenotypic plasticity 10, 11
see also electroreception montane 669 environments, concept of 4–6
electron transfer system (ETS) oxygen consumption 146 enzyme activities, mass-specific, scaling 132, 132
localization 119 parasites of 581, 682 enzyme kinetics
mechanisms 119, 121 polar, basking 656
electroreception 287 sizes 191 and Km 63
freshwater fish 515 tachymetabolic 189 lactate dehydrogenase 179
littoral animals 480 terrestrial 541, 565, 569, 573–81 enzymes
marine fish 429 thermal acclimation 202 adaptation 177–80, 402
Eleodes spp. (beetle) thermoneutral zone 203 affinities 179
cuticles 556 thermoregulation 13, 14, 191 and body temperature, structural differences
evaporative water loss 634 torpor 214–15
elephants 641 tundra, basking 656 178–9
Elminius modestus (crustacean), invasion 483 use of term 189 inhibition 18
see also barnacles see also thermal regulation marine animals, thermal stability 179
Elmis spp. (beetle), plastrons 511 endothermy pressure sensitivity 416
embryos 10, 26, 528, 586 advantages 219 rate–temperature curves 183
osmosis 459 regulatory mechanisms 18–19, 177
respiration 408 aerobic capacity 219
temperature 188 thermoregulatory 218–19 feedback systems 33–5
emissivities 194 and body temperature 220 fossil record 34
emissivity embryos 586 seasonal variations, freshwater animals 503
materials 194 evidence for, fossils 220 and thermal environments 177–80
thermal radiation 193 evolution 407 variations, in fish 404
emus 644 theories 218–20 eocrepuscular animals, use of term 549
end-plate see neuromuscular junction facultative 190 eosinophils, roles in adaptive immunity 701
end-plate potential 303, 304 inertial 190–1 ephemeral plants, deserts 623
endocrine communication 343, 343–60 partial 190 Ephestia spp. (moth), water gain 108
endocrine systems 347–60 regional 190 Ephydra spp. (fly), habitats 530
see also hormones in ectothermic vertebrates 404–8, 405 Ephydrella spp. (fly)
endocytosis temporal 190 habitats 530
mechanisms 67 use of term 189, 190 urine, hyperosmotic 531
receptor-mediated 67 energy epidermis
endoparasites acoustic, transmission 427–8 mechanoreceptors 268
aerobic respiration 682–3 apparent digestible, food 134 parasites 678
anaerobic pathways 683 assimilation efficiency 134 and permeability 83, 557
gas exchange 682 coastal 483 structure 14, 83, 557
and host defenses 676, 696–704 conversion in sensory systems 266 epifauna, characteristics 451
life cycles 681 free, changes 176 epilimnion, lakes 491
osmotic adaptation 680–1 transduction in sensory systems 266 epinephrine 345, 355
oxygen uptake 682 energy budgets 133–9 body temperature regulation 372
respiratory adaptation 682–4 and genotypes 138 –9 cardiac muscle regulation 317–18
thermal adaptation 681 and life-history theory 137–8 receptor linking 32
use of term 677 and mortality rates 138 roles, in lipolysis 122
endoplasmic reticulum (ER), calcium regulation in reproduction 137–8 see also catecholamines; norepinephrine
seasonal, desert habitats 628 epithelia
31 units 134 marine animals 80
energy content, food 126, 134 midgut 102
energy exchanges, plants 546 in osmoregulation 109
energy losses permeability 68
pumps 109
resorptive 93, 93
726 INDEX ETS see electron transfer system (ETS) insect herbivores 606
Eubostrichys dianeie (nematode), sulfur-oxidizing mechanisms 76–110
epithelia (continued) and osmoregulation 88
solute movements 66 bacteria 537 and toxin avoidance 605
transport 66 euphotic zone 423, 423 use of term 88
Euphydryas gillettii (butterfly), eggs 667 excretion products
epithelial cells, electron micrographs 67, 68 Eupsilia spp. (moth), thermal regulation 575 energy losses 137
equilibrium relative humidity (ERH) see critical Europe, forest survey 616 nitrogenous 100–1
Eurosta spp. (fly) osmoregulatory organs 88–102
equilibrium humidity (CEH) routes 137
ER see endoplasmic reticulum (ER) freeze tolerance 652 sequestration 102
ERH see critical equilibrium humidity (CEH) glycerol synthesis 652 excretory systems 88, 91, 94–9
Eriocheir spp. (crab) sorbitol synthesis 652 aerial exposure effects 502
euryhaline animals 78, 79, 108, 166, 399, 455–66, birds 563
amino acids, changes 74 freshwater animals 500
euryhaline characteristics 496 496, 538, 614 mechanisms 88–102
invasion 483 hormonal regulation of water balance 361 reptiles 563
osmoregulation 108 euryoxic animals 455, 471 roles 90
parasitism 681 eurythermal, use of term 191 schematic 88
urine production 500 eurythermal animals 455, 466–71, 536, 565, 613 terrestrial animals 557
erythrocytes 162 eusociality see sociality vertebrates 110
carbon dioxide transport 168 eutrophic lakes 482 exercise, cardiovascular changes 209
freshwater fish 508 eutrophication 482, 515, 519, 520 exocrine communication 343, 343
glucose uptake 62 and contamination, freshwater habitats 522 exocytosis, mechanisms 67
hemoglobins 163, 537, 585 lakes 520 exons
use of term 162 mechanisms 519, 520 recombination events 27
erythropoiesis, mechanisms 168 evaporative water loss (EWL)/cooling 53, 80, 81, RNA splicing 25
erythropoietin 359 exoskeletons 329, 330
escape reactions 247, 322, 323, 324, 325, 331 151, 195, 196, 211 molting process
Esox spp. (fish), eyes 514 desert animals 620, 625, 639, 640
estivation factors affecting 81 crustaceans 368
definition 212, 637 frogs 526 insects 365
desert animals 637–8 and heat loss 211 and regulation strategies 13
terrestrial snails 554–5 limitations 196 see also cuticles
see also dormancy littoral animals 469 exponents, applications 39
estrogens 345, 359, 374, 375 mechanisms 195–6 extracellular fluid (ECF)
behavioral effects 378–9 minimization 625 composition
calcium balance regulation 364 rates 107 animals 77, 78
effects on egg-white protein mRNAs 29 reptiles 557 freshwater animals 497
fetal development 595 strategies 469 freshwater vertebrates 499
gestation 380 terrestrial animals 80, 557, 572, 580, 581, 582 concentrations 95–6
negative feedback regulation 376, 377 see also cutaneous evaporative water loss (CEWL); osmolarity 564
as pollutants 520 patterns 15
roles 594 panting; respiratory evaporative water loss regulatory mechanisms 462
sex determination 592 (REWL); sweating roles 14
in terrestrial reproduction 592–5 evolution of see also blood; body fluids; hemolymph
estrus, initiation 594 adenosine triphosphatases 64 –5 extracellular pathways, solutes 67–8
estuaries 444–85 anaerobic metabolism 112, 141 extracellular volumes (ECV), diversity
abundance patterns 455 circulatory systems 154
characteristics 452–3 endothermy 218–20 51–74
mixing patterns 454 high body temperatures 220 extreme terrestrial habitats 620–73
mudflats 452–3 immune systems 698
salt marshes 453 metabolism 112 adversity selection 621
estuarine animals 77, 444–85 oxygen 112, 113 biogeography 621
feeding 480–1 plants 141, 541 and body mass 620–1
ionic adaptation 455–66 proteins 26–8 characteristics, common 620–1
life-cycle adaptation 475–6 rates 613 energy storage 621
locomotion 477–9 sex, and parasitism 705 eusociality in 621
osmotic adaptation 455–66 terrestrial animals 541, 552 gregariousness in 621
reproductive adaptation 475–6 thermal strategies 218–21 lifestyles in 621
respiratory adaptation 471–3 traits 6, 7 range 621
senses 479–80 water balance 76 selective regimes 621
thermal adaptation 466–71 evolutionary physiology size factors 620
water balance 455–66 comparative, limitations 7 types of 620
estuarine habitats 451–4 development 4 extremophiles, habitats 535–9
anthropogenic problems 481–3 holistic approach 7 exuviation hormone 368
biota 451–4 overview 3–4 Exxon Valdez (ship), pollution 431
herbivory 480 use of term 3 eyes 280–1, 281, 281
physical damage 476–7 EWL see evaporative water loss (EWL)/cooling compound 280, 282–5, 285
pollution 482 Exatostoma spp. (stick insect), water vapor uptake deep-sea animals 536
species diversity 452 634 desert animals 643
zonation 453, 483 excitation–contraction coupling 303–5, 304, 307 freshwater animals 514
ethanol excitatory postsynaptic potentials (EPSPs) 243–4, littoral animals 479
as adenosine triphosphate endpoint 117 244 marine animals 423
synthesis 683 excretion 88–102
tolerance, and parasitism 681 and gut functions 102–3
INDEX 727
sensitivity in relation to habitat 284–5, 285 marine animals 412, 427 ureo-osmoconforming 432–3
simple 280, 281–2 terrestrial animals 586, 595 urine concentrations 499
terrestrial 600–1 fetal development, terrestrial mammals 595 urine production 89
fever 372 ventilation 149, 150
F-1,6-BP see fructose 1,6-bisphosphate (F-1,6-BP) as adaptive response 220 water balance 77, 458, 459, 497, 499, 500
F-ATPases and parasites 682
fiber (dietary) see cellulose hormonal regulation 361
evolution 64 fibronectin 262 see also elasmobranchs; goldfish; teleosts
proton pumps 64 Fick’s law, of diffusion 55, 55, 62 fitness, concept of 4
facilitated diffusion filament gills 145 fixed action patterns 322
uniport 62 fine particulate organic matter (FPOM), patterns 490 flame cells
use of term 62 fish structure 499, 500, 557
factorial aerobic scope, definition 128 ammonia excretion 503 ultrafiltration 89, 91
FAD see flavin adenine dinucleotide (FAD) blood flow 586 flamingos, habitats 532
FADH2 see flavin adenine dinucleotide (reduced) body mass, and gill surface area 409 flatworms
brackish habitats 455 feeding 517
(FADH2) bradycardia 170 locomotion 326
Fahrenholz’s rule, and parasitism 680 brains 251 terrestrial 557, 587, 596, 596
farming, intensive 617 buoyancy mechanisms 419 flavin adenine dinucleotide (FAD), proton transfer
fasciclins 262 calcium balance regulation 364
Fasciola hepatica (fluke) chemoreceptors 170, 276–7 119
circulatory systems 159 flavin adenine dinucleotide (reduced) (FADH2)
life cycle 689 color vision 280
oxygen uptake 682 cutaneous respiration 511 roles 121
fasting, and oxygen consumption 135–6 development time, and temperature 188, 189 synthesis 119
fats eggs, buoyancy mechanisms 418 fleas
as energy store 122–3, 657 electroreceptors 287 jumping 337, 597
increase, and buoyancy 419 enzymes, variations 404 reproduction 385
see also lipids eyes 514 water balance 677
fatty acids freshwater 498, 502, 504, 507–13, 515 flies
absorption 608 gills, lamellae 410 basking 651
in lipids 180 glomerulus filtration rate 499–500 eggshells 107
in phospholipids 178, 181 hair cells 427 flight 584
saturated 180 heart 156–7, 157 freshwater 575
storage 122 heat exchangers 206 in hot springs 538
in terrestrial animals 182 heat production 205 mating behavior 588, 655
unsaturated 180 hemolymph, oxygen-binding curves 410 rectal papillae 561
feathers, birds 658 ingestion rates 135 see also Diptera (flies); Drosophila spp. (fly);
feedback ion uptake 496
in adaptation 33–5, 34 kidney tubules 101, 438 mosquitoes; parasitic flies
and amplification 34 lateral line system 270 flight 337–9, 597–9, 671–3
in enzyme regulation 33–5, 34 lungs 150, 507
and greenhouse effect 613 marine 186, 408–10, 424–6, 425, 429, 433, costs 671–3
feeding flapping 599
cold climate animals 655 436–7, 438, 497 gliding 599
desert animals 636–7 microtubules 182 and high-energy foods 672, 673
deterrents 604–5 migration 45–6, 124, 216–17, 404 insects 316, 597–8
estuarine animals 480–1 mitochondria, temperature differences 178
filters 429 muscle lactate dehydrogenase 178 anaerobic metabolism 125
freshwater animals 515–17 olfactory organs 427 sensory information procesing 290
littoral animals 480–1 osmoregulation 77, 101, 108, 109, 458, 461–2, scaling of 44
marine animals 429, 430 speeds 542
microphagous 515–17 463, 496–7 terrestrial arthropods 597–8
parasites 684–8 oxygen consumption 417 terrestrial vertebrates 598–9
terrestrial animals 602–9 permeability 83, 84 transport costs 45
terrestrial herbivores 602–9 polar, heat death 187 velocity, and metabolic rates 45
see also diets polymorphism 513, 513 see also bats; birds; hovering
females regional endothermy 406 flight muscles
reproduction reproduction 415 and aerobic metabolism 125
respiration 408–11, 472, 507, 511 birds 115, 133
energy expenditure 587 respiratory gas exchange 153 central pattern generators 322
estrogens 592–5 schreckstoff phenomenon 427, 515 insects 125, 147, 153, 316, 322
hormonal control 376–9, 593, 593 specific dynamic action 137 direct/indirect 338, 338
sex determination 592 swim-bladders 146, 419 mitochondria 133
fens 494 white anaerobic 671–2
fermentation gas glands 421 flightin 316
foregut 607 swimming 331–2, 332, 333, 334 floodplains, characteristics 494
in gastrointestinal tract 606, 607 floral patterns, mountain ranges 665
hindgut 607 myotomes 331 flow, Darcy’s law of 160
postgastric 608–9 thermal balance 178, 179, 186, 188, 191, 200, flow receptors, lotic species 515
fertilization 105–6, 376 flowing waters see lotic waters
freshwater animals 512 401–2, 436–8, 503, 504 fluidity
and infective agents 595 thermal tolerance 200 of cell membranes 180
littoral animals 475 tolerance polygons 200 concept of 180
mammals 595 torpor 212–13 flukes
urea production 90, 100 anaerobic respiration 637, 685
blood feeding 685
728 INDEX
flukes (continued) concept of 184 waterproof 83, 555, 573
eggs 678 high-altitude animals 668 see also amphibians; anurans; treefrogs
endorphins 703 and supercooling 185 fructose, roles, in glycolysis 118
feeding, stimuli 678 freeze tolerance 184–7, 504–5 fructose 1,6-bisphosphate (F-1,6-BP), roles 34
host behavior manipulation 695 advantages and disadvantages 186 fructose 6-phosphate
host defense exploitation 703 animals 184–5 and nonshivering thermogenesis 576
host reproduction modification 695 characteristics 186 synthesis 118
life cycles 678–9, 679, 689 concept of 184 fruit flies see Drosophila spp. (fly)
occurrence 677 ectotherms 652–4 FSH see follicle-stimulating hormone (FSH)
respiration 683, 684 endotherms 656–62 fumarate reductase 684
in respiratory passages 677 frogs 654 Fundulus spp. (fish)
salinity tolerance 681 high-altitude animals 662 muscle lactate dehydrogenase 178
sense organs 693 insects 652 pigments 472
species diversity 680 occurrence 185 thermal acclimation 404
teguments 687 terrestrial animals 566 fungi
thermal adaptation 681 freezing points desert 623
aqueous solutions 186 in rumen 608
fogs, and water uptake 563, 633 body fluids 186 fur
follicle-stimulating hormone (FSH) 354, 374, 375, freezing resistance, cockles 471 boreal animals 657–8
fresh water 487–525 color changes 631
376 characteristics 487 depth, and body mass 642
female sexual physiology 376 composition 506 polar mammals 657, 658
male sexual physiology 376 contaminated, as source of diseases 521 thermal insulation 193
release 32, 595 uses of 524 thickness 193
roles 593 freshwater animals 487–525 winter coats, mammals 658
food freshwater habitats 487–95 see also insulation
apparent digestible energy 134 acidification 501, 522–3
availability and afforestation 524 G-proteins
anthropogenic problems 518–24 activation 30, 32
on land 543 benthos 494 binding sites 30
in lotic waters 490 biota 494–5 cascade effects 19
calorific values 126 carnivores 515, 517 in glycolysis 119
detection 426 contamination, and eutrophication 522 interactions 30
energy content 126, 134 and dams 523 opsins coupling 278
fiber content 602 and deforestation 524 postsynaptic receptor signaling 241, 255
high-energy, and flight 671–2 and global warming 524 roles 20, 29, 423
ingestion, energy budgets 134–6 invasions 524
metabolism 607–8 and irrigation systems 523 gait
nutrient data 126 permanence of 487 arthropods 334, 335
oxidation, water yields 107 plants, productivity 494 centipedes 597
regulatory mechanisms 108 pollution 518–21 cursorial 334
vitamins 607 productivity 494 desert rodents 626
water content 107 and reproductive strategies 511 molluscs 327
water gain 108 taxa 494 montane animals 671
see also diets; feeding types of 487 snails 596
food storage, burrows 626 waste 518–21 terrestrial vertebrates 598, 598
foraging see also lakes; ponds; rivers tetrapods 334, 336
ants 626, 627 frogs
patterns, diel 626 bimodal breathing 171 galactose, roles, in glycolysis 118
range 45 body shape 631 gall-wasps, gall formation 694
forest belts, migration 614 brains 602 galls, formation 605–6, 694–5
forests circulatory systems 159 Gallus spp. (bird), embryos 591
riverine 494 color changes 211, 372, 571, 631 Gambusia spp. (fish), habitats 538
surveys 616 cooling 573 gametes
temperate 550 crab-eating 85, 433
see also boreal forests; trees; tropical rain forests cutaneous drinking 363 attractants 427
fossil fuels, and carbon emission 612 eggs, in water pools 526 fertilization, control 594–5
fossils, endothermy, evidence for 220 estivation 213, 631, 633, 638 and lotic waters 512
fossorial lifestyle 624 excretory modes 100 production, control 593
fovea 281 freeze tolerance 654 release, control 594–5
foxes glucose levels 654 gametogenesis, and sexual reproduction 412
Allen’s rule 649 growth, and temperature 11 gamma-amino butyric acid (GABA) 237, 254
fur 657 hyposmotic urine 86 receptors 240, 242, 244, 254
FPOM see fine particulate organic matter (FPOM) hypoxia 509 gammarids, as intermediate hosts 695, 696
free energy, changes, in chemical reactions 176 jumping 599 Gammarus spp. (amphipod)
free radicals, detoxification 141 reproductive strategies 590 as intermediate host 696
freeze avoidance 184, 185–7 respiration 147, 507 ion uptake 497, 498
characteristics 186 skins 84, 459 oxygen consumption 507
concept of 184 sweating 83, 211 permeability 459
high-altitude animals 668 thermal tolerance, high-altitude 667 predation 518
small ectotherm evaders 654–5 urea retention 433 ganglion cells of retina 282
terrestrial animals 566 water loss 80, 552, 633 large field (Y) cells 282
freeze intolerance 185–7 water uptake 84, 564 small field cells 282
advantages and disadvantages 186 gap junctions 246
animals 185–7 roles 68
and antifreeze compounds 186 structure 69
INDEX 729
gaping, of shells 469 590 roles 22–3 and marine habitats 430
gas concentrations types of 23 and rainfall 524
general transcription factors, binding 23 and terrestrial biome changes 614
in respiratory systems 144 generation time, and age at maturity 138 globin, gene family 28
see also carbon dioxide; oxygen genes glomerulus, roles, ultrafiltration 88–9, 90, 94
gas exchange 87 early response, metamorphosis 365, 366–7 glomerulus filtration rate, fish 499–500
barriers, thickness 148 homeobox 23 Glossina spp. (fly)
ectoparasites 682 master control 23 feeding 609
endoparasites 682 models 24 larvae 589
marine animals 408–10 multiple copies 28 proline 125
models 153 size 26 reproduction 374
structure 147 genetic drift, mechanisms 7 respiration 584
terrestrial animals 581 genetic recombination, mechanisms 26, 27 transmission 688
see also gas losses; gas uptake; respiration; genetics, and sex determination 592 water loss 585
genomes, point mutation 17 glucagon 357–8, 359
ventilation genotype–environment interrelationships see body temperature regulation 372
gas floats, types of 419 metabolism regulation 370
gas glands environment–genotype interrelationships; roles 118, 369–71
reaction norm
functions 421, 421 genotypes, and energy budgets 138 in lipolysis 122
mechanisms 420 genotypic variation, and natural selection 4, 6 glucocorticoids
gas losses, respiratory systems 144–9 Geococcyx californianus (bird), body temperature
gas solubilities, in respiratory systems 144 576 body temperature regulation 372
gas uptake, respiratory systems 144–9 Geolycosa spp. (spider), burrows 625 stress response 370–1, 372
gases gerbils glucose
delivery 162–9 body temperature 625, 626 binding 17
diffusion coefficients 148, 148, 149 estivation 638 blood–brain barrier 264–5
in fresh water 505–6, 506 Geukensia spp. (bivalve), enzyme adaptation 470 control of levels 370
increase, and buoyancy 419–22 gigantism, and parasitism 695 as energy source 683
Gasterochisma melampus (fish), endothermy, gill books, use of term 145 oxidation, via aerobic metabolism 119
gill chamber 457, 469, 472, 499, 563 phosphorylation 115
regional 406 gill reprocessing of urine 560 roles, in glycolysis 118
Gasterophilus spp. (fly), oxygen uptake 682 Gillichthys spp. (fish) uptake rates 430
gastric-inhibitory peptide 357 lactate dehydrogenase, species differences glucose 6-phosphate, synthesis 115, 118
gastrin 238, 357 179–80 glucose transporters
gastrointestinal tract (GIT) malate dehydrogenase 178, 404 GLUT1 265
thermal adaptation 466 GLUT2 358
bacteria 135 gills 145 glucosinolates
fermentation 607 arthropods 145 occurrence 604
see also guts calcium balance regulation 364 as phagostimulant 606
gastropods chemoreceptors 170 Gluphisia spp. (butterfly), salt uptake 603
anaerobic respiration 471 diffusion barriers 145 glutamate receptors 240, 242, 243
brackish habitats 454 filament 145, 408 glutamate-pyruvate transaminase, activity 462
central nervous system 251 freshwater animals 507 glyceraldehyde 3-phosphate, synthesis 122
eggs 587 heat exchange 406, 503 glycerol
estivation 638 hormonal regulation of water uptake 361 as antifreeze 186, 215, 652, 653
growth rates 476 ion uptake 84, 169, 436, 460, 461–2, 497 as cryoprotectant 184
kidney 559 lamellae 410 in insects 652, 653
littoral habitats 451 lamellar 145, 408 as membrane protectant 528
locomotion 596 marine fish 145, 408, 409 in mites 653
permeability 556 osmoregulation 86 as osmotic effector 633
pheromones 427 parasites 677 synthesis 185
reproduction perfusion 170 glycerol-3-phosphate acyltransferase, effects on chill
permeability 460
hermaphroditism 373 processing of urine 560 sensitivity 181
hormonal regulation 373 respiratory gas exchange 153 glycerophosphatide, structure 57
respiratory system 409, 507 soda lake animals 534 glycine receptors 240
see also slugs; snails structure, and activity levels 411 glycogen
Gastrotheca spp. (frog), reproductive strategies surface area, and body mass 153, 409, 409
gazelles in tadpoles 590 bonding 118
brain cooling 643 tuft 145 roles, in glycolysis 118
color 642 types of 145 source for cryoprotectants 185, 652
desert habitats, strategies 641–3 vent animals 537 structure 118
orientation patterns 643 ventilation 149–50, 150, 170, 408 glycogen phosphorylase, activation 33, 34
GCMs see global circulation models (GCMs) see also chloride cells; respiration glycolysis 34, 115–18, 116, 473, 683, 684
Gecarcinus spp. (crab), burrows 546 GIT see gastrointestinal tract (GIT) in cold habitats 654
geckos, water uptake 633 glial cells 223–4, 225, 230 in gas gland 421
gene duplication, mechanisms 26, 27 axon maintenance 263, 264 in littoral animals 473
gene expression neuromuscular junction 298 muscle contraction 310
control points 22 global circulation models (GCMs) 614 in parasites 683–4
regulatory mechanisms 24 global warming glycoproteins, roles 427
physiological 28–35 and cold biomes 662–3 see also antifreeze glycoproteins (AFGPs)
gene families and freshwater habitats 524 Glyphocrangon spp. (crustacean), respiratory
diversity 28 and high-altitude animals 672
evolution 27 pigments 411
sources of 27 Glyptonotus spp. (crustacean), hemocyanins 165
gene regulatory proteins Gnathophausia ingens (crustacean), hypoxia, coping
binding 22
encoding 23 strategies 410
730 INDEX
Gnathostoma spp. (nematode), mouthparts 686 gums, occurrence 604 651 mechanisms 205–6
goats, desert 640 gut peptide hormones 357 see also countercurrents; heat exchangers
golden moles, metabolic rates 629 guts heat exchangers
goldfish and blood distribution 209–10
elongated 603 countercurrent 205–6, 406
glycolysis pathways 117 functions, and excretory functions 102–3 in desert animals 643
myosin ATPase activity 178 hormonal control 357 in fish 406
Goldman–Hodgkin–Katz relation/equation 60, 61, insects 104 and heat gain 205–6
mammals, conditions 693 and heat loss 209–10
61, 225, 266 as parasite habitats 677–8 in mammals 440, 578–9
gonadal hormones 372 parasites polar animals 658–9
see also carotid rete; countercurrents; nasal heat
see also estrogens; progesterones; sex hormones distribution 692
gonadotropin 346, 354, 359, 372, 373 feeding strategies 685 exchange
water balance 102–3 heat gain 189, 192, 576–7
and parasitism 695 see also gastrointestinal tract (GIT); midgut;
regulatory mechanisms 593 littoral animals 467
secretion 657 rectum regulatory mechanisms 202–8
terrestrial animals 593 Gynaecotyla adunca (fluke), host behavior
gonadotropin-releasing hormone 238, 374, 376 behavioral 207–8, 570–1
gonads, endocrine activity 349, 359 manipulation 696 insulation 206–7
gophers, parasites 680 Gynaephora groenlandica (caterpillar), basking terrestrial animals 576–7, 620, 642
gossypol heat loss 190, 208–12
as phagostimulant 605 habituation 259, 259 cold climate animals 658–9
toxicity 605 Habronestes (spider), kairomones 385 desert animals 631, 639–41
grain silos, as manmade habitats 617 Hadrurus spp. (scorpion), burrow temperatures in diving 505
granivores, in deserts 636 and exercise 200, 580
grasshoppers 623 huddling 212, 657
basking 667 hagfish, body fluids, composition 432 licking 211
color changes 631 hair beds 268 littoral animals 467
cuticles 556 hair cells 270, 270 panting 211
evaporative cooling 639 regulatory mechanisms 208–12, 572, 576, 657
feeding, behavioral strategies 605 auditory system 272, 274 behavioral 212, 572, 633
freeze tolerance 668 mechanisms 427 blood distribution 209–10
life cycles 671 vestibular system 271 change in surface properties 210–11
metabolic rates 629, 668 hair follicles, mechanoreceptor linkage 268 evaporation 211
respiration 585 Halobates spp. (bug), respiration 442 sweating 211
respiratory evaporative water loss 634 hamsters see also fur; heat exchangers; insulation
tympanic organs 273 fur 658 heat production
water loss 635 reproduction 657, 695 endotherms 202–3
grasslands haploid genome, DNA in 24 large cold climate endotherms 660
temperate hares and oxygen consumption 126
fur 657 shivering and nonshivering 203–5
soil animals 551 metabolic rates 629 heat shock factor (HSF), mechanisms 183
terrestrial animals 550 urine 633 heat shock proteins (HSPs) 345
gray matter 252 Haustorius spp. (crustacean), survival strategies 477 expression 182
Great Ocean Conveyor Belt 398 HBTS see high body temperature setpoint (HBTS) families 182
greenhouse effect hearing 272–4, 599–600 HSP27, regulatory mechanisms 182
factors affecting amplitude coding 274, 275 HSP70
feedbacks 613 central pathways 274 expression 182
human activities 613 developmental plasticity 255 roles 183
gases 612 frequency detection 272, 275 HSP90, roles 34
and temperature rise 610–14 tonotopic representation 274, 290 mechanisms 183
see also global warming see also ears; mechanoreceptors in parasites 681
group behavior 384 heart 155–7 regulatory mechanisms 183
growth, energy supply 137–9 endocrine function 360 roles 21, 183
growth factors, roles 32 fish 156–7, 157 synthesis 183, 403–4
growth hormone 345, 354, 369 innervation 317–18 heat storage 196, 209, 580, 642
metabolism regulation 370 invertebrates 155–6 heater cells, thermogenesis 407
secretion 32 mammals 157 heater tissue, and brain temperature 406–7
growth inhibitors, occurrence 604 structure 155 heavy metals, pollution 520, 617
growth rates use of term 155 heavy minerals, reduction, and buoyancy 416–17
and age at maturity 138 vertebrates 156–7, 581 Helice spp. (crab), distribution 450
and heterozygosity 138 heart function, changes 472 Heliocranchia spp. (squid), ion levels 417
GTP see guanosine triphosphate (GTP) heart muscle cells, stimulation 32 heliothermy see basking
GTP-binding proteins, regulatory mechanisms see also cardiac muscle Heliothis spp. (moth), feeding, behavioral strategies
heart rate 38, 170, 200, 209, 440, 463, 559, 572, 581
19–20 see also bradycardia; tachycardia 605
GTPases, roles 20 heat Helix spp. (snail)
guanine detection, terrestrial animals 601
metabolic, and body temperature 202–3 cardioactive peptides 371
occurrence 101 sources of 205 estivation 638
properties 100 see also temperature; thermal adaptation kidney 559
guanosine triphosphate (GTP) heat death 180, 642 lungs 150
hydrolysis 20 polar fish 187 permeability 555
roles 32 heat distribution sperm release 595
synthesis 119 and blood flow 205 helix-turn-helix motif, binding 22
guinea pig, metabolic rates, and body mass 130 high-altitude animals 668
gular fluttering, birds 213, 580, 639
INDEX 731
helminths freshwater habitats 515 hopping 336–7
anaerobic parasitic, classes 683 in littoral habitats 480 horizontal cells (retina) 281
energy sources 683–4 in terrestrial habitats 543, 603–9 hormone response elements, binding 29
occurrence 675 heritability 613 hormones 342–87
see also flukes; nematodes; platyhelminths; hermaphroditism
tapeworms marine animals 412, 413 antidiuretic 361, 362, 560
molluscs 373 definition 344
hematocrit, use of term 162 Hesiocaeca methanicola (polychaete), habitats 539 enzyme regulation 177
heme, structure 163 Heterocephalus glaber (mole rat), sociality 639 evolutionary aspects 386–7
hemerythrins, occurrence 163 Heterogamia spp. (cockroach), deserts 624 and immune responses 697
Hemideina maori (grasshopper), freeze tolerance heterotherms, terrestrial 569, 573–81 mode of action 344–6, 346, 346
heterothermy patterns of release 344
668 insects 576 peptide 344, 344–6, 345
Hemilepistus spp. (woodlouse), water resorption regional 206, 208, 579 protein kinase activation 30
temporal 190 regulatory systems 386, 386–7
560 use of term 189 roles 32, 109, 342–86
hemocyanins vertebrates 541 specificity 346
heterozygosity steroid 344, 344, 345
binding 163 and growth rates 138 study methods 346–7
Bohr shift 166 mechanisms 27 target cells 346
in crustaceans 511 hexokinase thermal effects 217–18, 371
occurrence 163–4, 472 catalysis 115 tropic 346
regulatory mechanisms 508 glucose binding 17 types 343–6, 344
Root effects 167 isoenzymes 117 see also androgens; cholesterol; ecdysone;
temperature effects on 165 hibernation
hemocytes definition 212 estrogens; juvenile hormone (JH);
roles 162 regulatory mechanisms 215 progesterone; steroid hormones;
use of term 162 small ectotherm evaders 655 testosterone; and other hormones
hemoglobins 163 use of term 215 horses
affinity see also dormancy; torpor loop of Henle 562
Hif-1 see hypoxia-inducible factor 1 (Hif-1) running speed 334
at altitude 670 high-altitude animals 663–73 host–parasite conflicts 696–704
modulators 167, 670 size factors 620 host defenses 676, 696–702
Bohr shift 166 high-altitude habitats 663–73 parasite countermeasures 676, 678, 702–4
concentrations 38, 531 see also montane habitats host–parasite relationships 676, 678, 680, 696–702
and diving 440 high body temperature setpoint (HBTS), iguanas hosts
freshwater animals 508 behaviors, parasite-induced 695–6
high-affinity 670 217 definitive 688
littoral animals 472 high-latitude animals 645–63 intermediate 688
occurrence 163, 472 high-level waste (HLW) location mechanisms 689–90
organic modulators 167 hot habitats 621–45
oxygen-binding curves 509 disposal 617 hot springs, habitats 538
in parasites 682 production 617 houses, as manmade habitats 617
pigment adaptation 508 hippocampus 252, 260, 261, 324 hovering, locomotion cost 44
Root effects 167 histamine 242, 357 HSF see heat shock factor (HSF)
in salt lake animals 531 effects on parasites 701 HSPs see heat shock proteins (HSPs)
structure 163, 163 HLW see high-level waste (HLW) 5-HT see serotonin (5-HT)
temperature effects on 165, 411 homeobox genes, roles 23 huddling
types of 163 homeodomain proteins, roles 22 desert animals 639
vent animals 537, 538 homeostasis heat loss 208, 212
hemolymph cellular 71, 184 high-altitude animals 650–1, 657, 667–8
bicarbonate levels 584 and circulation 154, 209 montane animals 667–8
concentrations 553, 554 and CO2 586 terrestrial ectotherms 572
ion movements 561 of colonies 577 terrestrial endotherms 574, 577
oxygen-binding curves 410 and endothermy 219 terrestrial heterotherms 577
roles 162 and environmental adaptation 11 humans, sweating, heat loss 212
and sodium concentrations 461 and hormones 342 humidity
use of term 154 mechanisms 11 and burrows 620, 636, 657
see also blood; body fluids; extracellular fluid (ECF) metabolic 170, 473 increase 546
Heodes spp. (butterfly), microclimates 568 oxygen 170 and land plants 541
herbicides, pollution 520, 617 and pH 100, 603, 669 patterns, dunes 623
herbivores 135, 602–9 homeothermy profiles, soils 546
and carnivores compared 610 inertial 190–1, 219 on seashores 457
characteristics 602–4 use of term 189, 190 and spiracles 171–2, 583–4
defenses against 604–5 homeoviscous adaptation (HVA) 180, 416, 468, and water loss 79, 195
detoxification systems 603 and water uptake 86, 564
groups 603 503, 651 see also microclimates
insect 604–6 brain membranes 181 humidity receptors see hygroreceptors
polysubstrate monooxygenase 605 effects of cholesterol on 180 hummingbirds
salt uptake 603–4 roles 180 flight muscles 115, 133, 311
sequestration 605 homozygosis, mechanisms 27 hyposmotic urine 563
tundra 649 honey-bees see Apis spp. (bee) oxygen demand 581
vertebrate 606–9 hookworms torpor 190, 214, 573
herbivory host entry 691 use of ammonia 100, 563
defenses 604–5 life cycles 689
in desert habitats 636–7
in estuarine habitats 480
732 INDEX
HVA see homeoviscous adaptation (HVA) hyperosmotic urine 88, 92, 109, 435, 531, 534, 562, IL-1 see interleukin-1 (IL-1)
Hyalophora spp. (moth) 633, 640 IL-6 see interleukin-6 (IL-6)
ILW see intermediate-level waste (ILW)
diapause 369 hyperthermia Ilyanassa obsoleta (snail), behavior manipulation
shivering 575 adaptive 642
Hydra spp. (cnidarian) tolerance, desert birds 640 696
feeding 515 transient, and temperature regulation 209 imino acids, synthesis 117
locomotion 328 see also fever immune responses
neurosecretory granules 347
hydrins 363 hyperventilation, high-altitude animals 669 chemical mediation 697
Hydrobia spp. (snail), climbing patterns 478 hypocalcin 364 metazoans 697
hydrocarbons Hypogastrura tullbergi (insect), lifespan 655 and parasitism 697
effects, on marine birds 431 hypolimnion, lakes 491 types of 697
pollution 617 hypometabolism immune systems
hydrogen ions 364 cell types 700
hydrogen peroxide, reactivity 141 conditions 125 evolution 698
hydrogen pumps (H+-ATPase) 64, 497 and diving 440 invertebrates 700
hydrogen sulfide induced 169 and UV-B radiation 615
accumulation 537 hypoperfusion, and diving 440 immunity
coping strategies 537 hyposmosis 54, 399 adaptive
hydrophilic animals, osmotic tolerance 553 in Artemia spp. 532
Hydropyrus spp. (fly), habitats 530 marine teleosts 434–5 cells in 701
hydrostatic skeleton in marine vertebrates 85–6, 184, 399, 433, in host–parasite systems 698, 699–701
burrowing 328, 328 nonspecific, in host–parasite systems 698–9
compressive elements 326 434–5 immunoglobulin (Ig) 700, 701–2
crawling 327 regulatory mechanisms 72, 73, 78, 85–6, 109, structure 701–2
jet propulsion 328 immunologically privileged sites
leg-like structures 329 463, 500, 531 parasitic flies 702
locomotion 326–9 and salt excretion 85–6 and parasitism 678, 702
looping 328 hyposmotic urine 92, 108, 499, 561, 562, 563 immunosuppressants, parasitic release 703
muscles 326 hypothalamic peptides, release 32 IMP see inosine monophosphate (IMP)
shape change 326 hypothalamus 252 implantation 379
smooth muscle 314 body temperature regulation 372 imprinting 260
somersaulting 328 osmoreceptors 363 Inachis io (butterfly), hemolymph concentration
swimming 327 releasing hormones 354, 354, 355
tensile elements 326 hypothermia 214–15 554
hydrothermal vents 535–8 behavioral 506 INAs see ice-nucleating agents (INAs)
distribution 535 and heat conservation 579 incipient lethal temperature, use of term 198
fauna 536 large endotherms 659–60 incubation see eggs
3-hydroxybutyrate, roles, in aerobic metabolism regulatory mechanisms 215 inebriated (ine) 74
terminological issues 214–15 infauna 396
123 see also dormancy; hibernation; torpor
20-hydroxyecdysone, synthesis 695 hypothesis testing, species comparisons 8 characteristics 451
hydroxymethylglutaryl-CoA, feedback control 34 hypoxia distribution 396
5-hydroxytryptamine (5-HT) see serotonin (5-HT) and anaerobic conditions 112 littoral 451
hygrophilic animals coping strategies 125, 144, 167, 169–70, 408 infective agents, and fertilization 595
freshwater animals 506–7, 508 ingestion rates
circadian rhythms 554 littoral animals 471 and body mass 134, 135
habitats 547, 549 marine animals 410–11 factors affecting 134–5
regulatory organs 557 occurrence 115, 141 and temperature 135
thermal adaptation 565 parasites 682 see also feeding; guts
water balance, strategies 553–4 terrestrial animals 581, 586 inhibins 359, 376
hygrophilic arthropods hypoxia-inducible factor 1 (Hif-1), activity 169 inhibitory postsynaptic potentials (IPSPs) 243–4,
regulatory organs 559, 560 hyrax, montane habitats 666
sacculus 560 244
hygroreceptors 285–7 ice inosine monophosphate (IMP), synthesis 115
hygroscopic fluids, accumulation 565 contact prevention 652 inositol pentaphosphate (IPP), roles, in embryo
Hyla spp. (frog) latent heat of fusion 53
behavioral adaptation 503 melting point 51 development 590
freeze tolerance 654 polar, habitats 538–9 inositol triphosphate (IP3) 274
Hymenolepis spp. (tapeworm) structure 52
and acanthocephalans 704 see also water calcium release 30
anaerobic metabolism 683 peptide hormone signaling 344
migration 678 ice crystals, formation 52 roles 31–2
hypercapnia 141, 169 ice sheets, thinning, antarctic 662 INPs see ice-nucleating proteins (INPs)
littoral animals 471 ice-nucleating agents (INAs) insects
perception of 171 active secretion 64, 89, 90, 92
and respiratory systems 586 occurrence 652 adaptation 442
terrestrial animals 586 roles 184 adipokinetic hormones 370
hyperglycemic hormone 368 ice-nucleating proteins (INPs) aerobic metabolism 125
Hyperolius spp. (frog) occurrence 652–3 aerobic scope 128
color changes 631 roles 184 air sacs 148, 150, 171, 192
permeability 555 ICF see intracellular fluid (ICF) allantoin production 101, 503
hyperosmosis 54, 72, 73, 108, 399, 455 Ig see immunoglobulin (Ig) antifreezes 186, 655
regulatory mechanisms 78 iguanas aquatic 510
and salt uptake 84 desert, thermal setpoints 217 basking 208, 570, 571
digestion 607 blood feeding 609, 685
marine 435, 468 body temperature 188, 198, 208, 220, 565, 567,
thermal adaptation 468, 572
see also lizards; reptiles 639
burrows 626
carnivory 517
INDEX 733
central nervous system 249, 251 pheromones 277, 382 intra-auricular septum, vertebrates 157
chemoreceptors 277, 278 aggregation 384 intracellular fluid (ICF) 14
circulatory systems 155 mate location 382
cold tolerance 177, 186, 652 olfactory receptors 277 regulation 68–74
colonies 208, 595, 639 introns
color 571, 571, 651 plastrons 510
color changes 211, 372 r-selection 587 incorporation 27
color vision 280 rectum 65, 70, 93, 102–3, 362, 531, 565 numbers of 25, 26
compound eyes 282–5, 285 reflectance 41 RNA splicing 26
cooling mechanisms 217, 220, 566, 567, 580, reproduction 586, 587 inulin, as filtration marker 88, 90
invasions
639, 654 hormonal regulation 373–4, 374 coastlines 483
cryptonephridial system 98–9, 564 regulatory mechanisms 593, 595 freshwater habitats 524
cuticles 82, 83, 84, 194, 538, 557, 573, 634 resorptive epithelium 93, 93 iodopsins 278, 280
respiration 147, 507, 585 ion balance
structure 556 discontinuous 584–5, 634 across membranes 58–9
desert 623, 624, 626, 631, 632, 633, 636 rhodopsin absorbance 600 in animals 79–102
diapause 10, 212–14, 369 in salt lakes 531 in cells 62–71
salt uptake 84 costs 108–9
regulatory mechanisms 214 shivering 575 electrochemical 58–61
diffusion barriers 148 sociality 595, 639 energetics 108–9
diving 510, 515 sound production 600 hormonal regulation 363–4
eggs 595 spiracles 105, 171–2, 584–5 and ion transport 61–70
endocrine system 348–9, 349 storage excretion 102 see also ionic adaptation
endothermy 573–81, 652, 668 sweating 84, 217, 572–3, 639 ion channels 30, 59–60, 67, 83–4
extracellular fluids 497 terrestrial 548, 552, 560–1, 562, 564, 569, 570, gating mechanisms 60
eyes 600 nerve function 224–5, 226–30, 229
flight 125, 290, 338–9, 339, 560, 597–8, 673 581, 585, 588–9, 589, 604–6 and selective permeability 59–60, 109, 225–30
thermal acclimation 201–2 sensory receptors 266
central pattern generators 322 thermal conductance 581 stretch sensitivity in mechanoreceptors 268, 270
wingbeat frequency 339 thermal regulation 208, 565, 576, 576 transmitter-gated 240–1
flight muscles 316, 322 tracheae 147, 150, 507
direct/indirect muscles 338, 338 triacylglycerols 122 reversal potentials 243
food 108, 515, 649 uricotely 100 types of 60
freeze intolerance 668 urine concentrations, countercurrents 99, 104 voltage-gated 226–7, 227, 228, 228, 230, 234
freeze tolerance 184, 652, 662 urine secretion 90, 109 see also calcium channels; potassium channels;
freshwater 499, 507, 510, 510, 515, 517, 523 as vectors 678, 688
oxygen consumption 507 ventilation 105, 149, 150, 171, 584–5 sodium channels
galls 694–5 vibration detection (hearing) 273, 274, 276 ion pumps 62–5, 109, 564
gamete release 594–5 walking 334
gills 507 warm-up 208, 577, 578, 668 types 63–4
glycerol content 186, 652, 653 water balance 103, 564, 640 see also adenosine triphosphatase (ATPase);
gut bypass 108
guts 104 hormonal regulation 362 calcium pumps (Ca2+-ATPase); hydrogen
habituation 259 water loss 80, 564, 639, 669, 673 pumps (H+-ATPase); sodium pumps
heat production 205, 573–81, 651, 668 water uptake 86, 87, 107, 634 (Na+/K+-ATPase)
herbivory 108, 515, 604–6, 649 water vapor uptake 87, 564–5, 634 ion transport 61–70
excretory problems 606–9 see also bees; beetles; flies; moths; and other insects see also ion channels; ion pumps; ionic
heterothermy 573–8, 576 insulation adaptation
hygroreceptors 286 freshwater endotherms 505 ion uptake see ion pumps
ion uptake 497 high-altitude animals 668 ionic adaptation 79–102
jumping 597–8 high-latitude animals 657–8 estuarine animals 455–66
juvenile hormone 32, 593 large endotherm endurers 657–8 freshwater animals 495–503
larvae and wetting 505 littoral animals 455–66
eyes 282 see also air sacs; feathers; fur; thermal insulation marine animals 396–7
swimming 329 insulin 345, 358, 359, 386 parasites 680–1
legs 600 body temperature regulation 372 terrestrial animals 552–65
life cycles 512, 587, 670 metabolism regulation 370 ionotropic receptors 240, 241, 243
Malpighian tubule 92, 99, 499, 531, 560–1 sodium pump regulation 360 ions
marine, adaptation 175, 442 insulin-like growth factors (somatomedins) 369 hydration states 59
mating behavior 594 integrins 262 ionic radii 59
mechanoreceptors 268–9, 269 Intergovernmental Panel on Climate Change (IPCC) levels
metabolic rates 668 rainfall model 524 effects on oxygen-carrying capacity 166–7
metabolic water 107–8 temperature projections 612 maintenance 463–5
metamorphosis 349, 365–7 interleukin-1 (IL-1), functions 697 mobilities 59
microclimates 198, 566, 567, 568, 591, 667 interleukin-6 (IL-6), effects 699 and osmotic physiology 51–74
midgut 65, 102 intermediate-level waste (ILW) reduction, and buoyancy 417
migration 217, 651 disposal 617 see also calcium; potassium; sodium
molting 348, 365–6, 367 production 617 IP3 see inositol triphosphate (IP3)
montane habitats 667 interstitial fauna IPCC see Intergovernmental Panel on Climate
muscle fibers, multiterminal 319 characteristics 451 Change (IPCC)
nonshivering thermogenesis 205, 575 distribution 396 IPP see inositol pentaphosphate (IPP)
osmoregulation 530, 531, 560–1 habitats 547 iridophores, occurrence 631
osmotic effectors 503 land 563 iris 281
parasitoids 682, 685, 695, 702 littoral 455–7 irrigation systems, and freshwater habitats 523
parental care 595 marine 396 islets of Langerhans 357, 358
permeability 84, 572–3, 631 interstitial fluids see extracellular fluid (ECF) isometric muscle contraction 307, 308
isometric shapes, principles 36
isometric variation 38
734 INDEX
isopods kinases, roles 19 temperature profiles 503, 503
body temperatures 469 in metabolism 114 thermoclines 491
color change 467 trophic webs 517
permeability 459, 459 kinesin 264 underground 493
reproductive strategies 587 kinocilium 270 see also lentic waters; salt lakes; soda lakes
respiratory systems 478 Kleiber relation 40 lamellar gills 145, 408
salinity tolerance 469 Km laminin 262
water resorption 560 land animals see terrestrial animals
see also crustaceans; woodlice definition 63 Lanius excubitor (bird), hyperthermia tolerance
determination 63
isotonic muscle contraction 307, 308 pressure effects on 416 640
isozymes 28, 114, 117 salt transport 85, 400, 461, 497 LAP see leucine aminopeptidase (LAP)
temperature effects on 180, 404 larvae
and temperature 179 knee-jerk reaction 320
iteroparity, occurrence 5, 414–15, 512 koalas and environment 10
cecum 608 eyes 282
jellyfish feeding 606 food supplies 414
gas floats 419 Krebs cycle 119–25 free-swimming 689–91
jet propulsion 328–9 and amino acids 123 freshwater 509, 534
larvae 412 control 125 in insects 84, 102, 147, 168, 186, 213, 461, 497,
sulfate levels 417 fuels for 121–5
and glycolysis 117 505, 507, 515, 531, 538, 549, 568, 569, 589
jet propulsion 147, 328–9, 422 and ion concentrations 75 lecithotrophic 414
JH see juvenile hormone (JH) and malate dismutation 683 littoral animals 472, 483
Johnston’s organs 273, 276 mechanisms 119, 121 marine animals 412
joints 329, 330 schematic 120 metamorphosis, inhibition 695
jumping 336–7, 337, 337, 338 of parasites 675–6
Lacerta spp. (lizard) planktotrophic 414
anurans 598, 599 basking 569 respiration 147
frogs 599 freeze tolerance 654 thermal stress 199
terrestrial arthropods 597–8 viviparity 655 vent animals 538
terrestrial vertebrates 151, 598–9, 671 water balance 105–6, 465
juvenile hormone (JH) 32, 345, 349, 372, 381, 604, lactate lateral line system 270, 270
accumulation with muscle contraction 310 latexes, occurrence 605
695 and diving 440 Latimeria spp. (fish), ureo-osmoconforming 433
crustacean reproduction 374 as end-product 117, 123–4, 184, 473, 511, 655, latitude, vs. body mass 620
diapause regulation 369 683 LBTS see low body temperature setpoint (LBTS)
insects 593 as fuel 123–4 LCT see lower critical temperature (LCT)
LDH see lactate dehydrogenase (LDH)
reproduction 373 lactate dehydrogenase (LDH) leaf-rolling, strategies 605
metamorphosis 367 alleles 7, 178 Leander spp. (crustacean), tolerance 79
molting regulation, aquatic larvae 368 catalysis 117 learning 254, 255, 259–61
enzyme kinetics 179 associative 259
K-selection 5 pressure sensitivity 416 by observation 260
desert animals 638 pyruvate breakdown 180 heterosynaptic intergration in Aplysia (sea slug)
thermal effects 416
kairomones 385 variations 402, 404 258
kangaroo rats nonassociative 259
lactation, terrestrial mammals 592 lecithotrophic larvae 414, 538
gait 626 Lactobacillus vaginalis (bacterium), effects on leeches
jumping 337, 338 active secretion 89
nasal heat exchange 635 fertilization 595 feeding 609
seed-eating 638 lactose, hydrolysis 118 locomotion 327, 328, 596
kangaroos lakes 491–5 in respiratory passages 677
digestion 608 urine 499
jumping 151, 337 acidification, regional patterns 522 see also annelids; earthworms
reproduction 593 amictic 491 legs 329
temperature control 211 carbon dioxide profiles 506 arthropods 334
kelp forests, distribution 397 crater 493
kidney 88–101 swimming 330–1
brackish vertebrates 460 alkalinity 533–4 terrestrial 597
endocrine function 358–9, 360 dimictic 491 evolution 597
fish 101, 438 epilimnion 491 and gaits 599
freshwater animals 499–500 eutrophication 520 scaling 43
hormonal regulation 362–3 high-salinity 529–32 and soft-bodied locomotion compared 597
mammals, structural diversity 97 hypogean 494 and “stilting” 574, 626
marine invertebrates 401 hypolimnion 491, 493, 495 tetrapods 334
marine mammals 435 largest 491 lemmings
marine vertebrates 435, 460 metalimnion 491 fur 657
permeability 109 monomictic 491 migration 656
nutrients 492 lens 281, 282
control of 362–3 oligomictic 491 lentic waters
pH balance 97, 97, 169 oligotrophic 492 characteristics 490–5
portal blood flow 158 oxyclines 491 ecological problems 490
secretion-based 90 oxygen profiles 506 stratification 490
terrestrial snails 101, 558–9, 559 pH 533, 533 see also lakes
ultrafiltration 90, 550 pollution 520 leopards, montane habitats 666
use of term 88 polymictic 491 Lepidochora spp. (beetle), water uptake 633
vasopressin actions 362–3, 363 productivity 494
vertebrates, function 88–9, 94–6 profundal habitats 492
kidney cells, ultrastructure 92 stratification 491, 492, 492–3
killifish, pigments 472
INDEX 735
lepidopterans, desert 624 Limulus spp. (horseshoe crab) estuarine animals 477–9
see also butterflies; caterpillars; moths eyes 278 exoskeletons 329–40
oxygen consumption 143 freshwater animals 514
Lepidosiren spp. (lungfish), lungs 507 receptors 170 on hot sand 626
Leptinotarsa spp. (beetle), proline 125 legs vs. soft-bodied 597
leptins 360 linear regression, confidence limits 38, 38 limbs 329–40
Lineweaver–Burk plots 63
effects in ectotherms 371 Liolaemus multiformis (lizard), basking 667 energy storage/exchange systems 329, 334–6,
metabolism regulation 370 lipids 337
Leptograpsus spp. (crab), bimodal breathing 472
Lernaeodiscus porcellanae (crustacean), parasitism in aerobic metabolism 122–3 littoral animals 477–9
in buoyancy 419 marine animals 422
690, 690 in cuticles 82, 538, 556–7, 638, 651 metachronal rhythm 322, 326
see also barnacles as food reserve 538, 577, 651, 657, 673 rhythmic 477–8
leucine aminopeptidase (LAP), occurrence 462 in membranes 55, 56, 181, 416 scaling of 42–5
leucine zipper motif, mechanisms 22 in skins 83, 557, 577
leucocytes structure 57 environmental implications 45–6
and immune systems 700 see also fats; homeoviscous adaptation (HVA) size factors 422
mediation 699 lipoclin 277 soft-bodied animals 596–7
surface receptors 697, 701 lipolysis, mechanisms 122–3 terrestrial animals 596–7
Leucorchestris spp. (spider), juveniles 638 liquid uptake voluntary movements 323–5
LH see luteinizing hormone (LH) mechanisms 86–7, 497, 634 see also crawling; diving; flight; jumping; running;
LHRH see luteinizing hormone-releasing hormone terrestrial animals 563–4
Litomosoides carinii (nematode), aerobic respiration swimming; walking
(LHRH) locusts
Libinia spp. (crab), oxygen consumption 143 682
lice Litoria spp. (frog), permeability 555 desert 623
littoral animals 451–81 digestion 606
mouthparts 686 littoral habitats 445–51 migration 640, 641
parasitism 680 reproduction 373
water vapor uptake 87, 564 anthropogenic problems 481–3 respiratory systems 585
lichens herbivory 480 logarithms
deserts 623 of lakes 492 applications 39
mountains 664 oxygen availability 471 equations 38
tundra 648 physical damage 476–7 long-term depression 261
licking, heat loss 211 pollution 482 long-term potentiation 260, 260–1
life cycles salinity variations 456 loop of Henle
desert animals 657 temperature variations 456 ascending 95–6
freshwater animals 511–14 tides 446 birds 562
high-altitude animals 670–1 waves 447 descending 94–5
marine animals 411–15 zonation 448, 483 desert rodents 633
montane animals 670–1 Littorina spp. (gastropod) terrestrial animals 562
montane invertebrates 670–1 dislodgement 477 looping locomotion 328
parasites 678–9, 679, 688 invasion 483 lordosis 379
shoreline and estuarine animals 475–6 occurrence 448 lotic waters 487–90
small desert ectotherms 655 lizards environmental changes 490
and temperature 218, 219 basking 652, 667 food availability 490
terrestrial animals 587–95 body temperature 188, 211, 566, 573, 682 and gametes 512–13
life history station-keeping problems 514
patterns 587 during fever 220 low body temperature setpoint (LBTS), iguanas
theory, and energy budgets 137–8 patterns 196, 571
lifespans regulation 211, 220 217
caterpillars 655 burrowing 667 low-level waste (LLW)
mites 655 circulatory systems 159
parasites 688 color changes 211, 571–2 disposal 617
scaling 137–8 eggs 107, 590 production 617
springtails 655 epidermis 557 lower critical temperature (LCT)
ligands freeze tolerance 668 acclimation 201
activity 17 locomotion 626, 626 and body mass 199
allosteric effects 17, 18 metabolic rates 629 luciferase, roles, in bioluminescence 424
light microclimates 566, 567 luciferin, roles, in bioluminescence 424, 426
attenuation 423 overheating avoidance 566 Lumbricus spp. (oligochaete)
cycles 202–3 panting 573 oxygen consumption 143
freshwater habitats 519 predation 637 reproduction 372
littoral habitats 479 temperature patterns 571 see also earthworms
marine habitats 423–4 temperature regulation 210, 211, 371 lungfish see Protopterus spp. (lungfish)
radiation 193–4 upper critical temperature 188 lungs 145
terrestrial habitats 606 water loss 573 diffusional 581
Ligia spp. (crustacean) see also reptiles freshwater animals 507
body temperatures 469 llamas, montane habitats 664 receptors 172
color changes 371, 467 LLW see low-level waste (LLW) respiratory gas exchange 153
osmosis 564 Lobatosoma manteri (fluke), sense organs 693 terrestrial animals 581–2, 582
limbic system 252 locomotion 325–40 vascularization 581
limbs central pattern generators 322 ventilation 150, 581
energy storage/exchange systems 329, 334–6, command system 322 water conservation 104, 582
costs 43, 44 see also book lungs
337 desert animals 626 luteinizing hormone (LH) 354, 374, 375, 376
locomotion 329–40 endoskeletons 329–40 female sexual physiology 376
see also legs male sexual physiology 375–6
release 32, 595
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