Microgeographic variation in locomotor traits among lizards in a human-built environment Colin Donihue School of Forestry and Environmental Studies, Yale University, New Haven, CT, USA
ABSTRACT Microgeographic variation in fitness-relevant traits may be more common than previously appreciated. The fitness of many vertebrates is directly related to their locomotor capacity, a whole-organism trait integrating behavior, morphology, and physiology. Because locomotion is inextricably related to context, I hypothesized that it might vary with habitat structure in a wide-ranging lizard, Podarcis erhardii, found in the Greek Cyclade Islands. I compared lizard populations living on humanbuilt rock walls, a novel habitat with complex vertical structure, with nearby lizard populations that are naive to human-built infrastructure and live in flat, loose-substrate habitat. I tested for differences in morphology, behavior, and performance. Lizards from built sites were larger and had significantly (and relatively) longer forelimbs and hindlimbs. The differences in hindlimb morphology were especially pronounced for distal components—the foot and longest toe. These morphologies facilitated a significant behavioral shift in jumping propensity across a rocky experimental substrate. I found no difference in maximum velocity between these populations; however, females originating from wall sites potentially accelerated faster over the rocky experimental substrate. The variation between these closely neighboring populations suggests that the lizards inhabiting walls have experienced a suite of trait changes enabling them to take advantage of the novel habitat structure created by humans. Submitted 30 September 2015 Accepted 18 February 2016 Published 10 March 2016 Corresponding author Colin Donihue,
[email protected] Academic editor James Roper Additional Information and Declarations can be found on page 8 DOI 10.7717/peerj.1776 Copyright 2016 Donihue Distributed under Creative Commons CC-BY 4.0 OPEN ACCESS
Subjects Animal Behavior, Conservation Biology, Ecology, Coupled Natural and Human Systems Keywords Locomotion, Morphometrics, Context-dependence, Lizard, Podarcis erhardii, Local
adaptation, Sprint speed
INTRODUCTION Animal locomotion integrates a suite of morphological, behavioral, and physiological attributes and impacts an individual’s fitness (Irschick & Garland, 2001; Calsbeek & Irschick, 2007; Irschick et al., 2008). Furthermore, locomotor behavior and performance is of necessity closely tied to an individual’s immediate ecological setting (Losos, 1990; Toro, Herrel & Irschick, 2004; Kohlsdorf & Navas, 2007). While traits associated with locomotion are often considered typological for a species, emerging evidence suggests that microgeographic variability in ecological context can result in considerably more intraspecific variation in fitness-relevant traits than previously appreciated (Richardson et al., 2014). Other studies have demonstrated that the substrate and structure of a habitat are consistently related to a lizard species’ behavior, morphology, and performance
How to cite this article Donihue (2016), Microgeographic variation in locomotor traits among lizards in a human-built environment. PeerJ 4:e1776; DOI 10.7717/peerj.1776
(Vanhooydonck & Van Damme, 2003; Calsbeek & Irschick, 2007; Kohlsdorf & Navas, 2007; Losos, 2011). Lizards in more complex habitats tend to more often jump from branchto-branch or rock-to-rock (Kohlsdorf & Navas, 2007; Harrison, Revell & Losos, 2015). Additionally, jumping performance in lizards is often associated with longer hind limbs, particularly in the distal segments between the ankle and the tip of the longest toe (Moermond, 1979; Losos, 1990; Toro, Herrel & Irschick, 2004). Laboratory tests of lizard locomotion typically employ a single experimental substrate. Moreover, the types of substrates used may (e.g., sand) or may not (e.g., cork or sandpaper) reflect naturally occurring substrates that have given rise to different adaptations for locomotion. Comparing lizard locomotion across multiple substrates is increasingly the focus of new studies (Tulli, Abdala & Cruz, 2012; Vanhooydonck et al., 2015), but these studies have yet to investigate performance of conspecifics living in different habitats and test predictions of associated morphological and behavioral differences according to those habitats. Humans are ecosystem engineers, creating novel habitat structure across landscapes and exerting strong adaptive pressure on the organisms in those landscapes (Jones, Lawton & Shachak, 1994; Donihue & Lambert, 2014). In the Greek islands, stone walls and terraces crisscross the landscape, and the eponymous Aegean Wall Lizard, Podarcis erhardii, can readily be found throughout (Valakos et al., 2008). However, P. erhardii, can also commonly be found dashing between bushes in nearby wall-less habitats with sand or loose-soil substrates. Podarcis erhardii living on stone walls experience a more structurally complex habitat than their conspecifics in non-wall habitats (Fig. 1). Based on other research showing that lizard traits change to accommodate new demands for locomotor performance in rocky habitats (Goodman, 2007; Kohlsdorf & Navas, 2007; Revell et al., 2007), I hypothesized that human alteration of the landscape should affect behavioral and morphological traits associated with locomotion. I tested for differences in jumping behavior, limb morphology, and sprinting performance between lizards living in areas with walls and areas without walls. The research demonstrates that human alteration of the environment can result in considerable microgeographic variation in important whole-organism traits such as locomotion.
METHODS I collected 324 adult P. erhardii from 10, 50 m by 50 m sites within 15 km of each other on Naxos, a large island in the Greek Cyclade Islands. Five sites had stone walls, the other five were characterized by sandy substrate with interspersed Juniperus oxycedrus shrubs or a loose jumble of soil and Mediterranean phrygana (Fig. 1). All sites were selected for having a high density of lizards, and non-wall sites for being more than 200 m from the nearest built stone structure. While P. erhardii home range has not been investigated, sister species have reported home ranges no larger than 120 m2 (Brown, Gist & Taylor 1995; Swallow & Castilla, 1996) suggesting it is highly unlikely lizards from non-wall sites had originated on walls. For all lizards, I recorded sex and measured snout-to-vent length (SVL), and the length of each segment of the right fore and hind limb using digital calipers (Frankford Arsenal 672060).
Donihue (2016), PeerJ, DOI 10.7717/peerj.1776
2/11
n=94 n=76
5 Wall Sites NAXOS
0
5
62.40 ± 0.62 59.23 ± 0.74
43.38 ± 3.35 37.25 ± 2.31
14.87 ± 0.12 12.69 ± 0.10
Snout to Vent Length
Total Leg Length
Ankle to Toe Tip
58.13 ± 0.44 55.02 ± 0.59
40.31 ± 2.41 35.09 ± 1.69
13.63 ± 0.10 11.86 ± 0.08
p=0.0015 p=0.0294
p=0.0019 p
