Kleptothermy: an additional category of thermoregulation, and a possible example in sea kraits (Laticauda laticaudata, Serpentes).

Abstract

Lacking the capacity for thermogenesis, most ectotherms inhabiting thermally heterogeneous environments rely instead upon exploiting that ambient heterogeneity. In many cases they maintain body temperatures within a narrow range despite massive spatial and temporal variation in ambient conditions. Reliance on diverse thermal opportunities is reflected in specific terms for organisms that bask in sunlight to regulate their temperature (heliotherms), or that press their bodies against warm substrates to facilitate heat flow (thigmotherms), or that rely on large body mass to maintain thermal constancy (gigantothermy). We propose an additional category of thermoregulators: kleptotherms, which regulate their own temperature by 'stealing' heat from other organisms. This concept involves two major conditions: the thermal heterogeneity created by the presence of a warm organism in a cool environment and the selective use of that heterogeneity by another animal to maintain body temperatures at higher (and more stable) levels than would be possible elsewhere in the local area. Kleptothermy occurs in endotherms also, but is usually reciprocal (rather than unilateral as in ectotherms). Thermal monitoring on a small tropical island documents a possible example of kleptothermy, based on high stable temperatures of a sea snake (Laticauda laticaudata) inside a burrow occupied by seabirds.

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Animal behaviour
Opinion piece
Kleptothermy: an
additional category of
thermoregulation, and
a possible example
in sea kraits (Laticauda
laticaudata, Serpentes)
Lacking the capacity for thermogenesis, most
ectotherms inhabiting thermally heterogeneous
environments rely instead upon exploiting that
ambient heterogeneity. In many cases they main-
tain body temperatures within a narrow range
despite massive spatial and temporal variation
in ambient conditions. Reliance on diverse ther-
mal opportunities is reflected in specific terms
for organisms that bask in sunlight to regulate
their temperature (heliotherms), or that press
their bodies against warm substrates to facilitate
heat flow (thigmotherms), or that rely on large
bodymasstomaintain
(gigantothermy).Wepropose
categoryofthermoregulators:
which regulate their own temperature by ‘steal-
ing’ heat from other organisms. This concept
involves two major conditions:
heterogeneity created by the presence of a warm
organism in a cool environment and the selective
use of that heterogeneity by another animal to
maintain body temperatures at higher (and
more stable) levels than would be possible
elsewhereinthelocal
occurs in endotherms also, but is usually recipro-
cal (rather than unilateral as in ectotherms).
Thermal monitoring on a small tropical island
documents a possible example of kleptothermy,
based on high stable temperatures of a sea
snake (Laticauda laticaudata) inside a burrow
occupied by seabirds.
thermalconstancy
additional
kleptotherms,
an
the thermal
area. Kleptothermy
Keywords: ectothermy; thermoregulation;
thigmothermy; reptile; snake
Reliance on other animals to create the thermal hetero-
geneity exploited by behavioural thermoregulation is
widespread. In some cases, conspecifics are exploited
to increase effective mass (as in tightly clustered
groups of lizards (Shah et al. 2003) and snakes
(Myres & Eells 1968; Aubret & Shine 2009)). Similar
clustering (or huddling) behaviour is also widespread
in gregarious endotherms (e.g. Brown & Foster 1992;
Arends et al. 1995; Ancel et al. 1997). Such behaviour
enables a group of individuals to increase its thermal
inertia, retard heat loss and/or reduce the per capita
metabolic expenditure needed to maintain stable
body temperatures (Myres & Eells 1968; Canals et al.
1989, 1998). In other cases, physical contact with
warmer conspecifics enables cold animals to achieve
higher temperatures; such an advantage may explain
the phenomenon of female mimicry in Canadian
garter snakes, Thamnophis sirtalis (Shine et al. 2001).
In this system, males that have recently emerged
from hibernation attract courtship from other males,
gaining significant heat transfer in the process (Shine
et al. 2001).
The most dramatic examples of kleptothermy
(heat-stealing), however, should come from cases
where ectotherms regulate their own temperatures by
exploiting the high and constant body temperatures
exhibited by endothermic species. Especially if the
endotherm is ensconced within a well-insulated site
(such as a nest or a burrow), any animal sharing that
habitat probably will experience higher and/or con-
stant ambient temperatures than would otherwise be
the case. The endotherms involved are not only mam-
mals and birds; termites maintain high and constant
temperatures within their mounds, providing other-
wise-unavailable thermal regimes that are exploited
by a wide array of lizards, snakes and crocodilians
(Vanzolini 1948; Leloup 1984; Magnusson et al.
1985; Ehmann et al. 1991). However, many cases of
kleptothermy involve ectotherms sheltering inside the
burrows used by endotherms. For example, seabird
burrows are common retreat-sites for reptiles as diverse
as Australian tiger snakes (Notechis scutatus, Worrell
1958) and New Zealand tuatara (Sphenodon punctatus,
Newman 1987), and mammal burrows are used by
geckos (Finlayson 1941).
While conducting ecological studies on amphibious
sea snakes (blue-banded sea kraits, Laticauda laticau-
data) in New Caledonia, we documented a possible
example of the thermal benefits of kleptothermy
(figure 1). One adult male snake (snout-vent length
94.5 cm, mass 217 g), to which we had attached a
time-depth recorder (that also records temperature,
TDRLTD-1110,Lotek
sampling rate 450s, +0.18C; see Brischoux et al.
2007 for implantation methodology), spent three
days within a burrow occupied by a pair of seabirds
(wedge-tailed shearwater, Puffinus pacificus) that were
incubating their chick. The snake’s body temperature
over this period was higher and more constant
(37.5+0.28C, range 37.1–37.98C, figure 1) than at
any other time during the period we monitored the
animal (or during periods when we have monitored
other sea kraits), and very different from the thermal
regimes available in any other microhabitat available
to the snake on this small island (figure 1). In particular,
the diel range of body temperatures of this snake was
more stable (coefficient of variation (CV) ¼ 0.005)
during the period it occupied the shearwater burrow,
compared with 31.7+3.78C (CV ¼ 0.117) when in
other available microhabitats (figure 1). The critical
role of the birds in maintaining the high burrow
temperature is evident from the low, stable temperature
ofan unoccupiedburrow
27.0–28.58C, figure 1).
Althoughseveral authors
co-habitation of ectothermic vertebrateswith endother-
mic organisms within well-insulated sites (see above),
our dataset appears to be the first to quantify the
potential thermal benefits of this phenomenon in a
free-ranging ectotherm. Our data are unreplicated
WirelessInc.Canada,
(28.1+0.48C,range
have reported
Biol. Lett. (2009) 5, 729–731
doi:10.1098/rsbl.2009.0550
Published online 5 August 2009
Received 8 July 2009
Accepted 13 July 2009
729
This journal is q 2009 The Royal Society
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and preliminary, and do not tell us whether or not the
snakes actively select occupied bird burrows, or
whether such occupancy conveys any fitness benefits
(or, indeed, costs). Nonetheless, the data do confirm
that the presence of an endotherm can create thermal
heterogeneity at a spatial and temporal scale relevant
to a mobile ectotherm in the same area, and can do
so in a way that is potentially exploitable by the
ectotherm. If such conditions are frequently satisfied,
thentheabilitytoexploit
‘hotspots’ may well be significant for some species.
Kleptothermy may be distinctive not only in the
source of heat involved (the byproduct of another
organism’s metabolism
behaviour) but also in the magnitude and stability of
the thermal regimes potentially achievable; alternative
tactics such as heliothermy and other types of thig-
mothermy typically function only during daylight
hours, and do not provide as much thermostability.
Given the thermal dependence of locomotor and
physiological processes in ectotherms (Dawson 1975;
Bennett 1990; Dorcas et al. 1997), the fitness benefits
ofkleptothermyfor such
considerable.
As with almost any definitional problem in biology,
the boundaries of kleptothermy are unlikely to be
clearcut and will require debate and discussion.
endotherm-derived
and/orthermoregulatory
animals couldbe
However, the phenomenon relies upon two major
conditions: (i) thermal heterogeneity created by the
presence of a warm organism in a cool environment;
and (ii) the selective use of that heterogeneity by
another animal to maintain body temperatures at
higher and more stable levels than would be possible
elsewhere in the local area. Importantly, the source of
heat in kleptothermy involves the metabolic thermo-
genesis of another animal, rather than solar radiation,
volcanically warmed soil, or any other non-biotic
source. Kleptothermy is widespread in endotherms as
well as ectotherms (huddling behaviour of juvenile
endotherms or microchiropterans are clear examples)
but typically is reciprocal. By contrast, kleptothermy
in ectotherms generally will be unilateral. Clustering
together to retard heat loss thus constitutes klep-
tothermy in endotherms (because the slower cooling
rate is partially owing to heat production by members
of the group) but not in ectotherms (because slower
cooling is entirely owing to thermal inertia (i.e. gigan-
tothermy)).Endoparasites(includingoviductalembryos)
are not kleptotherms, because they cannot actively
move about to select specific thermal regimes within
a heterogeneous environment. Future research could
usefully explore the occurrence, forms, and potential
fitness consequences, of this putative thermoregulatory
tactic.
time (days)
3 Jan 2006
4 Jan 2006
5 Jan 2006
6 Jan 2006
7 Jan 2006
8 Jan 2006
9 Jan 2006
10 Jan 2006
temperature (°C)
20
25
30
35
40
55
60
Figure 1. Ambient temperatures on a small island (Signal Islet, New Caledonia) and body temperatures of a male sea krait
(Laticauda laticaudata) on that island over a seven-day period in January 2006. Thermal regimes were monitored with data-
loggers (ACR SmartButton data Loggers: +0.58C, sampling rate 5 min excepted for the snake, see text); all sites other
than the occupied shearwater burrow provided cooler and/or more variable temperatures than did the burrow used by the
snake from 5 to 8 January (open: 35.3+13.48C, ‘dry’ beach rock: 29.1+3.68C, intertidal beach rock: 26.5+2.08C,
vacant sea bird burrow: 28.1+0.48C). Beach rocks and vacant bird burrows are frequently used as shelters by L. laticaudata
(Bonnet et al. 2009). Thin black line indicates open; thick grey line indicates ‘dry’ beach rock; thin grey line indicates intertidal
beachrock; thick broken black dashes indicate vacant seabird burrow; thick black line indicates L. laticaudata (adult male); thin
broken grey dashes indicate constant 37.58C temperature).
730F. Brischoux et al. Opinion piece. Kleptothermy as a thermal tactic
Biol. Lett. (2009)
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The study was carried out under permits no. 6024-179/
DRN/ENV and no. 6024-3601/DRN/ENV.
S. Lorioux and M. De Crignis helped during fieldwork, and
C. Chevillon and D. Ponton (DRN Province Sud, IRD) gave
logistical support.Twoanonymous
insightfulcomments on
manuscript. We thank the Center National de la Recherche
Scientifique, the Australian Research Council and the
Australian Government (Endeavour Awards) for funding.
referees
versions
provided
ofpreviousthis
Franc ¸ois Brischoux1,*, Xavier Bonnet2and
Richard Shine1
1Biological Sciences A08, University of Sydney, Sydney,
NSW 2006, Australia
2Centre d’Etudes Biologiques de Chize ´, CEBC-CNRS
UPR1934 79360, Villiers en Bois, France
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