Predator presence and recent climatic warming raise body
temperatures of island lizards
Félix Landry Yuana*1, Shun
Itob1, Toby P. N. Tsanga, Takeo
Kuriyamac, Kaede Yamazakid, Timothy
C. Bonebrakea and Masami Hasegawad
Short running title: Snakes and climate raise lizard temperatures
aSchool of Biological Sciences, The University of Hong
Kong, Hong Kong SAR, China
bGraduate School of Life Science, Tohoku University,
Aoba-ku, Sendai, Japan
cInstitute of Natural and Environmental Sciences,
University of Hyogo, Tamba, Japan
dDepartment of Biology, Faculty of Science, Toho
University, Funabashi, Chiba, Japan
*Corresponding author. E-mail address:
flyuan@connect.hku.hk. Telephone number: +852 5649
2201. Mailing address: School of Biological Sciences, Kadoorie
Biological Sciences Building, The University of Hong Kong, Pok Fu Lam
Road, Hong Kong SAR, China.
1These authors contributed equally to the manuscript.
Statement of authorship: FLY, SI, MH and TCB designed the study. FLY,
TK, KY, YK and MH collected the data, while FLY, TPNT and SI performed
the analyses. FLY and SI wrote the manuscript, and all authors
significantly contributed to revisions.
Data accessibility statement: Data supporting the results will be
archived in Dryad should the manuscript be accepted.
Keywords: prey-predator, interspecific interactions, body temperature,
thermal performance, ectotherm, climate change, japan, lizard, snake
Type of article: Letters
Words in abstract: 147
Words in main text: 4965
Number of references: 56
Number of figures: 5
Number of tables: 0
Number of text boxes: 0
ABSTRACT
In ectothermic predator-prey relationships, evasion of predation by prey
depends on physiological and behavioural responses relating to both
players’ thermal biology. On Japan’s Izu Islands, we investigated a prey
lizard’s physiological and thermal responses to the presence of a snake
predator over evolutionary time in addition to recent climatic warming.
Foraging lizard body temperatures have increased by 1.0°C from 1981 to
2019 overall, yet were 3.4°C warmer on snake islands relative to
snake-free islands. We also detected snake predator-induced selection on
hind leg length, which in turn is a major determinant for sprint speed
only in lizard populations exposed to predation by snakes. Accordingly,
we found that warmer prey body temperatures result in faster sprint
speeds by the prey at temperatures suboptimal for the snake predator,
and therefore contribute to escaping predation. Given recent climatic
change, further warming could irrevocably alter this and other
ectothermic predator-prey relationships.
INTRODUCTION
In ectotherms, where body temperatures and physiological processes are
dependent on immediate thermal environments, the prey’s survival under
predation is tied to the accessibility of body temperatures to achieve
their thermal optimum for escaping by rapid movement (Hertz et al. 1983;
Chai and Srygley 1990; Cooper 2000). To successfully evade predation
when chased, a prey’s thermal optimum for escape, in addition to its
locomotory speed at that temperature, should surpass that of the
predator for chasing (Grigaltchik et al. 2012; Dell et al. 2014; Öhlund
et al. 2015; Figueira et al. 2019). Ectothermic prey-predator dynamics
become increasingly complex when we consider how recent climate change
has and will foreseeably continue to impact both players (Grigaltchik et
al. 2012; Laws 2017). In a warming world, changes in the available
thermal landscapes can manifest at the order of microhabitats, which is
especially challenging for lizards because of their dependency on
thermoregulation to reach body temperatures adequate for behaviours
supporting survival and reproduction (Sinervo et al. 2010). Considering
the thermally dependent nature of predator evasion, the evolution of a
prey species’ thermal physiology and behaviour should be strongly
affected by both their predators and changes in environmental
temperatures.
Within the Galapagos Archipelago on Santa Fe Island, Christian and Tracy
(1981) found that the success of predation by Galapagos hawks
(Buteo galapagoensis ) on hatchling land iguanas (Conolophus
pallidus ) is highest at times of the day when iguana body temperatures
are suboptimal for sprinting. Conversely, at times when iguanas were
capable of attaining body temperatures optimal for reaching maximal
sprint speeds, predation success by the hawks was much lower. Similarly,
on Isla Plaza Sur, Snell et al. (1988) found that lava lizards
(Tropidurus albemarlensis ) run faster on the side of the island
with less vegetation and greater exposure to predators. Oceanic island
systems such as the Galapagos Islands are ideal for studying ecological
processes shaping life history because they formed in isolation with no
prior connection to other landmasses. Once colonized by limited overseas
dispersal, the flora and fauna on each island develops along unique
evolutionary trajectories shaping each island’s present-day diversity
(Whittaker et al. 2017). In the case where multiple populations of a
single species remain isolated across an archipelago over evolutionary
time, it allows for an untangling of the effects of different selective
pressures (Kuriyama et al. 2011; Brandley et al. 2014).
Located off the southeastern coast of Japan’s mainland, the volcanic Izu
Islands formed independently less than a million years ago, rendering
them completely vacant for colonization by species occupying adjacent
land (Kaneoka et al. 1970). The low number of reptile species in the Izu
Islands relative to tropical or other less-isolated regions (Hasegawa
2003) provides an opportunity to single out the selection pressures of
prey-predator relationships on thermal physiology and behaviour.
Notably, one endemic lizard species, Okada’s five-lined skink
(Plestiodon latiscutatus ), is dominant and distributed across all
of the system’s major islands, while one of its major predators, the
Japanese four-lined rat snake (Elaphe quadrivirgata ), is also
found on most, but not all of these islands (Hasegawa and Moriguchi
1989), resulting in a number of insular skink populations free from
snake predation. Therefore, taking into account the thermal dependency
of both predator and prey in this system, we can expect adaptions in the
thermal physiology and behaviour of P. latiscutatus in order to
escape predation by E. quadrivirgata across space and
time.
With our study spanning nearly 40 years, we investigated variations in
the foraging body temperature of P. latiscutatus as a function of
snake predator presence as well as climatic warming over the study
period. We also follow the sequence through which field-active body
temperatures matter in this prey-predator relationship by quantifying
the physiological and morphological components of the thermal dependency
of locomotion and its overall role in the evasion of the snake predator
by the prey lizard.
METHODS