Sea water transport and submersion tolerance as dispersal ...

Polar Biol (2011) 34:1591–1595
DOI 10.1007/s00300-011-1020-3

ORIGINAL PAPER

Sea water transport and submersion tolerance as dispersal
strategies for the invasive ground beetle Merizodus soledadinus
(Carabidae)

D. Renault

Received: 18 February 2011 / Revised: 7 April 2011 / Accepted: 8 April 2011 / Published online: 30 April 2011
Ó Springer-Verlag 2011

Abstract The alien ground beetle Merizodus soledadinus may facilitate the dispersal range of M. soledadinus across
was introduced to the sub-Antarctic Kerguelen Islands in the Kerguelen Islands, comprising over 300 islands and
1913. It colonized several small islands and islets of this islets in total.
archipelago, without any apparent human assistance in
some locations, and crossed several large rivers and allu- Keywords Biological invasion Á Insect Á
vial plains. As aggregations of this species on the tidal drift Flotation Á Survival Á Kerguelen Islands
line are common at the Kerguelen Islands, the present work
examined whether adult individuals of M. soledadinus Introduction
could disperse by flotation on the sea. Different sample
sizes of ground beetles (from 1 to 10) were placed on sea Human-assisted invasions increase the frequency of long-
water at 8°C in plastic vials. Survival (50% lethal times) distance dispersal events by invertebrates, facilitating the
significantly increased from 2.1 ± 0.2 days for single colonization of remote terrestrial areas, such as Antarctica
beetles to 6.5 ± 0.3 days for groups of 10 beetles per vial, and the surrounding sub-Antarctic islands (Bergstrom and
with there being no difference in the survival duration for Chown 1999; Clarke et al. 2005; Chown et al. 2009). At the
groups of 2, 5, and 10 beetles per vial. Similar survival sub-Antarctic islands, the modes of introduction are typi-
durations were found for beetles in vials with artificially cally associated with anthropogenic activities, and most
agitated water and controls. In addition, the duration of alien invertebrates have been introduced at a single site
survival was twice as high under freshwater versus sea (specifically research stations and/or sites of industrial
water conditions, when groups of 10 adults were used. operations) as a result of visiting ships (Chown et al. 2005;
Finally, the survival to total submersion in freshwater was Whinam et al. 2005; Convey and Lebouvier 2009). In
evaluated, and ranged from 3 to 4 days. This ability to addition, anthropogenic activities on these islands are
survive extended periods both floating on and/or sub- limited compared to temperate continental ecosystems
merged beneath salt and freshwater conditions, indicates (Chown et al. 2005; Lebouvier et al. 2011), thus reducing
the presence of a successful dispersal mechanism, which human-assisted dispersal of alien insects, and hence
inhibiting quick colonization between geographically dis-
Electronic supplementary material The online version of this tant points.
article (doi:10.1007/s00300-011-1020-3) contains supplementary
material, which is available to authorized users. At the Kerguelen Islands, Frenot et al. (2005) and
Schermann–Legionnet et al. (2007) listed the presence of
D. Renault (&) 30 invasive and naturalized invertebrate species, of which
Universite´ de Rennes 1, UMR CNRS 6553 Ecobio, 16 belonged to the class Insecta and three were defined as
263 avenue du Gal Leclerc, 35042 Rennes, France flightless. The flightless ground beetle, Merizodus soled-
e-mail: [email protected] adinus (Carabidae) was introduced to the Kerguelen
Islands in 1913 at a single site (Port Couvreux) (Jeannel
D. Renault 1940; Laparie et al. 2010) (Fig. 1). The natural dispersal of
Station Biologique de Paimpont, Universite´ de Rennes 1,
UMR CNRS 6553 Ecobio, 35380 Paimpont, France

123

1592 Polar Biol (2011) 34:1591–1595

adult individuals of M. soledadinus occurs most often M. soledadinus through their use of flotsam in nest build-
through microscale movements via locomotor activity ing, which they may collect from the coasts of other islands
(walking) (Chevrier 1996; Lebouvier et al. 2011). In the- (Chevrier 1996). However, this explanation is not suffi-
ory, the geographical spread of the beetle should have thus cient, at least in certain cases, as specimens of M. soled-
remained limited by geographical barriers, including sea adinus have been found on small islands and islets within
water, rivers, rocky cliffs lacking coastal vegetation, and the Golfe du Morbihan, where there are very few bird
large colonies of penguins (Lebouvier et al. 2011). How- colonies and the human presence is anecdotal (to non-
ever, across several decades, this alien insect has exhibited existent).
progressive dispersion into the northern and eastern coastal
areas, without any apparent human assistance (Chevrier Several insect species are known to have the ability to
et al. 1997). This ground beetle crossed several rivers of survive temporarily submerged in habitats of saltwater or
1–15 m in breadth (see Davaine and Beall 1997 for a freshwater conditions, or through rafting on the water
description of the main rivers that can be found on the surface (Howden 1977; Peck 1994; Hoback and Stanley
eastern part of the archipelago), as well as lakes, ponds, 2001; Coulson et al. 2002; Brust et al. 2005). In addition,
and alluvial plains, and has successfully colonized several terrestrial beetles have been reported to walk beneath the
islands and islets surrounding the mainland (Lebouvier and water by clinging to substrates when submerged (Topp and
Renault unpublished result). Phalacrocorax (atriceps) Ring 1988). As aggregations of M. soledadinus on the tidal
verrucosus, commonly known as Kerguelen shags, may drift line are common at the Kerguelen Islands (Laparie
have contributed to the geographical expansion of et al. 2010), the possible transport of M. soledadinus on
floating seaweed and debris, or directly on sea water, has

0 20 km

Port Couvreux

Bryer Péninsule Courbet
Port-aux-Français

Golfe du Morbihan
49°

Penn N
WE
Australia
Mayes S

Direction of major
wind

69° 70°

Fig. 1 Map of the Kerguelen Islands with a focus on the Golfe du Morbihan. The scientific station is based at Port-aux-Franc¸ais, and the ground
beetle Merizodus soledadinus was introduced at Port Couvreux. The large-scale outline map was redrawn from Frenot et al. (2005)

123

Polar Biol (2011) 34:1591–1595 1593

thus been hypothesized. Hence, this study aimed to assess and the beetles were directly transferred to Petri dishes as
whether (1) adult M. soledadinus could disperse through previously described. The survival was scored as the
flotation on the sea and/or freshwater, and (2) if this species number of walking insects after 2 days in Petri dishes at
could endure prolonged periods of submersion in fresh- 8°C (L/D: 15 h/9 h).
water allowing large ponds and rivers to be traversed.
All means are given with standard errors. Survival
Materials and methods curves were compared using log-rank (Mantel–Cox) test.
v2 contingency tests were used to compare mortality rates.
Imagoes of Merizodus soledadinus (Coleoptera: Carabidae) Survival data were subsequently expressed as lethal times
were sampled on the Kerguelen Islands in the surroundings for 50 and 90% of the samples (Lt50 and Lt90, respectively).
of the research station at Port-aux-Franc¸ais (70°130E, Time–mortality regression equations and hours to Lt50 and
49°21S). Imagoes of 5.5–6 mm long (Laparie et al. 2010) Lt90 were calculated using probit analysis. Statistical
were all hand-collected from beneath stones at coastal analyses were conducted using MINITAB Statistical
areas in January 2010 to February 2010, and were main- Software Release 13 (MINITAB Inc., State College,
tained under controlled conditions (8.0 ± 1.0°C) for 1 day, Pennsylvania) and Prism V5 (GraphPad Software Inc., San
under a 15/9 h (Light/Dark) cycle, before being used in the Diego, California).
experiments. Adults were fed ad libitum for 24 h with first
instar dipteran larvae. Results

In the first experiment, the tolerance to flotation was Survival significantly differed across the experimental
examined by transferring ground beetles to plastic vials conditions (Mantel–Cox: v2 = 14.00; df = 4; P \ 0.01;
(6 cm diameter, 7 cm depth) half-filled with sea water. In Fig. 2). Survival significantly increased when the number of
the first scenario, adults were randomly assigned to each of adult M. soledadinus increased from 1 to 5 individuals in
the four following experimental conditions: 1, 2, 5, or 10 each vial (v2 = 6.22; df = 1; P \ 0.01). The 50% lethal
ground beetles per plastic vial. In order to distinguish the times (Lt50) increased gradually as the number of ground
effects of flotation from the effects of salinity on the beetles increased from 1 to 10 (Lt50 = 2.1 ± 0.2 days for
duration of survival, a complementary experiment was one beetle and Lt50 = 6.5 ± 0.3 days for 10 beetles), with a
conducted, in which groups of 10 ground beetles were significant increase in the duration of survival being found
transferred to plastic vials (6 cm diameter, 7 cm depth) that for two or more beetles (Fig. 2). There was no significant
were half-filled with freshwater. For each experimental difference in survival among the experimental conditions in
condition, a total of 12 plastic vials were prepared. In the which 2, 5, and 10 beetles were exposed to sea water
second scenario, the effects of water movement on flotation (v2 = 1.72; df = 2; P = 0.4236). Similar durations of
survival was assessed by transferring groups of 10 ground survival were found for beetles in vials with artificially
beetles to plastic vials that were half-filled with sea water. agitated water (v2 = 0.26; df = 2; P = 0.8758; Fig. 3).
Batches of 12 vials were then assigned to each of the three
following experimental condition: 1/agitated 6 times per A significant difference was observed between the
day with clamps, 2/continuously rocked with a 3D agitator groups of 10 adults of M. soledadinus exposed to fresh-
to mimic turbulent conditions (wave action), and 3/controls water versus the groups of 10 adults exposed to sea water
(no surface water turbulence). In each scenario, one plastic
vial was removed from the treatment at daily intervals. The Fig. 2 Survival (percent ± SE) of groups of 1, 2, 5, or 10 adult
beetles were directly transferred to Petri dishes, the bottom Merizodus soledadinus kept on sea water, and groups of 10 adults
of which was covered with a disk of paper (6 cm diameter, kept on freshwater. Specimens were maintained at 8°C. Survival was
60 g m-2) saturated with freshwater. The survival of the evaluated at 2 days after recovery at 8°C in Petri dishes
ground beetles was scored as the number of walking insects
after 2 days in Petri dishes at 8°C (L/D: 15/9 h).

In the second experiment, tolerance to total submersion
was determined by placing groups of 10 ground beetles in
sealed plastic vials (6 cm diameter, 7 cm depth). A total of
twelve vials were completely filled with freshwater and
placed under controlled conditions (L/D: 15/9 h, tempera-
ture: 8.0 ± 1.0°C). Circular mesh was placed 2 cm under
the water level to prevent ground beetles breathing at the
surface. One plastic vial was removed every 8 h for 4 days,

123

1594 Polar Biol (2011) 34:1591–1595

Fig. 3 Survival (percent ± SE) of groups of 10 adult Merizodus M. soledadinus survived several days on sea water under
soledadinus kept on sea water in one of each of the three following controlled conditions, even when the water surface was
conditions; 1/water was agitated 6 times per days with clamps, 2/vials agitated to mimic wave action. At the Kerguelen Islands, the
were agitated continuously with a 3D agitator, and 3/control. Survival presence of aggregations of M. soledadinus around the tidal
was evaluated at 2 days after recovery at 8°C in Petri dishes drift line is common (Laparie et al. 2010), which would
facilitate the flotation of adult M. soledadinus when algae
Fig. 4 Survival (percent ± SE) of groups of 10 adult Merizodus and debris are resuspended during high tides and/or strong
soledadinus completely submerged in freshwater. Survival was winds. This possible transport mechanism may have con-
evaluated at 2 days after recovery at 8°C in Petri dishes tributed to the colonization of pristine islands, in the absence
of any human assistance, both within (i.e., Pender and Bryer
(v2 = 4.02; df = 1; P \ 0.05), with 90% lethal times Islands, classified as integral nature reserves) and outside
(Lt90) being twice as high under freshwater conditions (i.e., Bellouard Island) the Golfe du Morbihan. In addition,
(P \ 0.05). individuals of M. soledadinus were found on the west coast
but not the east coast of recently colonized islands (e.g.,
Adult M. soledadinus exhibited high survival abilities to Australia or Mayes) in the Golfe du Morbihan (Chevrier
submersion (Fig. 4). All beetles survived submersion for 1996; Lebouvier et al. 2011). As major wind currents occur
3 day, with survival declining at the beginning of the fourth from the west to the east (Sampe and Xie 2007), colonization
day. of these islands may have occurred through passive transport
on flotsam (Fig. 1).
Discussion
In the present work, it was found that when forming
Several insect species, including ground beetles, have been aggregations, individuals started to climb on one another as
observed floating on flotsam at the sea surface in the Gala- soon as two or more beetles were present in the plastic
pagos archipelago (Peck 1994) and in the brackish seawater vials. Rafts have been demonstrated to be a survival
of the Baltic area (Palme´n 1944). In addition, there is a report strategy in a number of social insect species during
of a live specimen from the genus Oopterus, which is closely flooding periods (Lude et al. 1999; Anderson et al. 2002),
related to Merizodus, found on the surface of a sample of but further behavioral experiments on larger open water
plankton several hundred kilometers southeast of mainland surfaces are required to assess the evidence of raft forma-
New Zealand (Johns 1974). In the present work, adult tion as a dispersal strategy in adult M. soledadinus. When 5
to 10 ground beetles were present, the time spent in contact
with sea water conditions was reduced for each adult,
possibly leading to increased survival duration by limiting
the problems of osmoregulation of the body fluids pre-
sented by salt water. This finding is further supported by
the highest duration of survival of the ground beetles
occurring in individuals exposed to freshwater.

Another interesting finding was the duration of survival
by completely submerged adults. The maximum duration
that adult M. soledadinus could spend under water excee-
ded 3 days, without any significant mortality effect. Many
arthropod species are known to survive extended periods of
flooding in habitats subject to regular inundation (Adis and
Junk 2002; Pe´tillon et al. 2009; Fielden et al. 2011). Var-
ious behavioral and morphological adaptations enable
arthropods to respire underwater, with the mechanism of
plastron respiration (see Flynn and Bush 2008) being found
in several adults of terrestrial insects, including Coleoptera
(Thorpe and Crisp 1949). Additional field observations
revealed that adults of M. soledadinus could cross small
ponds by walking underwater along the river bed carrying
an air bubble between the abdomen and elytra (Renault
unpublished result). However, the exact mechanisms
assisting the underwater survival of adult M. soledadinus
requires further exploration.

123

Polar Biol (2011) 34:1591–1595 1595

To conclude, this work presents the first evidence for Coulson SJ, Hodkinson ID, Webb NR, Harrison JA (2002) Survival of
flotation on sea water as a possible mean of dispersal for terrestrial soil-dwelling arthropods on and in seawater: implica-
the invasive ground beetle Merizodus soledadinus at the tions for trans-oceanic dispersal. Funct Ecol 16:353–356
Kerguelen Islands. When considering the wingless com-
ponent of adult M. soledadinus, its capacity to survive Davaine P, Beall E (1997) Introduction de Salmonide´s en milieu
flotation is probably a key fitness attribute to the successful vierge (Iˆles Kerguelen, Subantarctique) : enjeux, re´sultats,
colonization of this archipelago, comprising a total of over perspectives. Bull Fr Peˆche Piscic 344(345):93–110
300 islands and islets. This dispersal mechanism may also
contribute toward explaining the expansion of this species Fielden LJ, Knolhoff LM, Villarreal SM, Ryan P (2011) Underwater
to South Georgia, and more particularly the recent expan- survival in the dog tick Dermacentor variabilis (Acari: Ixodi-
sion observed in the Greene Peninsula, which is charac- dae). J Insect Physiol 57:21–26
terized by very limited human visitation (Convey et al.
2011). Flynn MR, Bush JWM (2008) Underwater breathing: the mechanics
of plastron respiration. J Fluid Mech 608:275–296
Acknowledgments This research was supported by the ‘‘Institut
Polaire Francais’’ (IPEV 136) and the ‘‘Agence Nationale de la Frenot Y, Chown SL, Whinam J, Selkirk PM, Convey P, Skotnicki M,
Recherche’’ (ANR-07-VULN-004, EVINCE). I would like to thank Bergstrom DM (2005) Biological invasions in the Antarctic:
Darwin that initiated the study of flotation tolerance with plant seeds extent, impacts and implications. Biol Rev 80:45–72
150 years ago. I thank P. Vernon for helpful discussions on earlier
versions of this manuscript. I’m grateful to four anonymous referees Hoback WW, Stanley DW (2001) Insects in hypoxia. J Insect Physiol
for their constructive comments that improved the manuscript. 47:533–542

References Howden HF (1977) Beetles, beach drift and island biogeography.
Biotropica 9:53–57
Adis J, Junk WJ (2002) Terrestrial invertebrates inhabiting lowland
river floodplains of Central Amazonia and Central Europe: a Jeannel R (1940) Croisie`re du Bougainville aux ˆıles australes
review. Freshwater Biol 47:711–731 franc¸aises. III. Cole´opte`res. Mem du Museum National d’His-
toire Naturelle, France. se´rie A 14:63–202
Anderson C, Theraulaz G, Deneubourg J-L (2002) Self-assemblages
in insect societies. Insectes Soc 49:99–110 Johns PM (1974) Arthropoda of the Sub-Antarctic islands of New
Zealand. 1. Coleoptera: Carabidae. Southern New Zealand,
Bergstrom D, Chown SL (1999) Life at the front: History, ecology Patagonian and Falkland Islands insular Carabidae. J R Soc N Z
and change on southern ocean islands. Trends Ecol Evol 14:427– 4:283–302
477
Laparie M, Lebouvier M, Lalouette L, Renault D (2010) Variation of
Brust ML, Hoback WW, Skinner KF, Knisley CB (2005) Differential morphometric traits in populations of an invasive carabid
Immersion Survival by Populations of Cicindela hirticollis predator (Merizodus soledadinus) within a sub-Antarctic island.
(Coleoptera: Cicindelidae). Ann Entomol Soc Am 98:973–979 Biol Invasions 12:3405–3417

Chevrier M (1996) Introduction de deux espe`ces d’insectes aux Iles Lebouvier M, Laparie M, Hulle´ M, Marais A, Cozic Y, Lalouette L,
Kerguelen: processus de colonisation et exemples d’interactions. Vernon P, Candresse T, Frenot Y, Renault D (2011) The
Dissertation, Universite´ de Rennes 1 significance of the sub-Antarctic Kerguelen Islands for the
assessment of the vulnerability of native communities to climate
Chevrier M, Vernon P, Frenot Y (1997) Potential effects of two alien change, alien insect invasions and plant viruses. Biol Invasions
insects on a sub-Antarctic wingless fly in the Kerguelen Islands. 13:1195–1208. doi:10.1007/s10530-011-9946-5
In: Battaglia B, Valancia J, Walton DWH (eds) Antarctic
communities–Species. structure and survival, Cambridge Uni- Lude A, Reich M, Plachter H (1999) Life strategies of ants in
versity Press, United Kingdom, pp 424–431 unpredictable floodplain habitats of alpine rivers (Hymenoptera:
Formicidae). Entomol Gen 24:75–91
Chown SL, Hull B, Gaston KJ (2005) Human impacts, energy
availability and invasion across Southern Ocean Islands. Glob Palme´n R (1944) Die anemohydrochore ausbreitung der insekten als
Ecol Biogeogr 14:521–528 zoogeographischer faktor. Ann Zool Fennici 19:175–181

Chown SL, Spear D, Lee JE, Shaw JD (2009) Animal introductions to Peck SB (1994) Sea-surface (Pleuston) transport of insects between
southern systems: lessons for ecology and for policy. Afr Zool islands in the Galapagos Archipelago, Ecuador. Ann Entomol
44:248–262 Soc Am 87:576–582

Clarke A, Barnes DKA, Hodgson DA (2005) How isolated is Pe´tillon J, Montaigne W, Renault D (2009) Hypoxic coma as a
Antarctica? Trends Ecol Evolut 20:1–3 strategy to survive inundation in a salt-marsh inhabiting spider.
Biol Lett 5:442–445
Convey P, Lebouvier M (2009) Environmental change and human
impacts on terrestrial ecosystems of the sub-Antarctic islands Sampe T, Xie S-P (2007) Mapping high sea winds from space—a
between their discovery and the mid-twentieth century. Pap Proc global climatology. American Meteorological Society, December
R Soc Tasmania 143:1–14 2007, doi:10.1175/BAMS-88-12-1965

Convey P, Key RS, Key RJD, Belchier M, Waller CL (2011) Recent Schermann-Legionnet A, Hennion F, Vernon P, Atlan A (2007)
range expansions in non-native predatory beetles on sub- Breeding system of the sub-Antarctic plant species Pringlea
Antarctic South Georgia. Polar Biol 34:597–602 antiscorbutica R. Br. and search for potential insect pollinators
in the Kerguelen Islands. Polar Biol 30:1183–1193

Thorpe WH, Crisp DJ (1949) Studies on plastron respiration. Part IV.
Plastron respiration in the Coleoptera. J Exp Biol 26:219–260

Topp W, Ring RA (1988) Adaptations of Coleoptera to the marine
environment. II. Observations on rove beetles (Staphylinidae)
from rocky shores. Can J Zool 66:2469–2474

Whinam J, Chilcott N, Bergstrom DM (2005) Subantarctic hitchhik-
ers: expeditioners as vectors for the introduction of alien
organisms. Biol Cons 121:207–219

123