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An experimental evaluation of foraging decisions in urban
and natural forest populations of Anolis lizards
Zachary A. Chejanovski
1
&Kevin J. Avilés-Rodríguez
1,2
&Oriol Lapiedra
1,3
&
Evan L. Preisser
1
&Jason J. Kolbe
1
#Springer Science+Business Media New York 2017
Abstract Foraging decisions reflect a trade-off between the
benefits of acquiring food and the costs of movement.
Changes in the biotic and abiotic environment associated with
urbanization can alter this trade-off and modify foraging de-
cisions. We experimentally manipulated foraging opportuni-
ties for two Anolis lizard species –the brown anole (A. sagrei)
in Florida and the crested anole (A. cristatellus)inPuertoRico
–to assess whether foraging behavior differs between habitats
varying in their degree of urbanization. In both urban and
natural forest habitats, we measured the latency of perched
anoles to feed from an experimental feeding tray. We manip-
ulated perch availability and predator presence, while also
taking into account population (e.g., conspecific density) and
individual-level factors (e.g., body temperature) to evaluate
whether and how these contribute to between-habitat differ-
ences in foraging behavior. In both species, urban anoles had
longer latencies to feed and lower overall response rates com-
pared to lizards from forests. Urban anoles were also larger
(i.e., snout-vent length and mass) in both species and urban
A. sagrei were in better body condition than the natural forest
population. We postulate that the observed patterns in forag-
ing behavior are driven by differences in perceived predation
risk, foraging motivation, or neophobia. Although we are un-
able to identify the mechanism(s) driving these differences,
the substantial differences in urban versus forest anole forag-
ing behavior emphasizes the importance of understanding
how urbanization influences animal populations and their per-
sistence in anthropogenically-modified environments.
Keywords Foraging behavior .Motivation .Predation risk .
Structural habitat .Urbanization
Introduction
Animals must feed tosurvive, and theory states that organisms
maximize fitness by matching their foraging decisions to en-
vironmental conditions (Stephens and Krebs 1986;Dalletal.
2005). These decisions reflect a trade-off between the caloric
benefits and potential costs of foraging, such as missed mating
opportunities or greater predation risk (Lima and Bednekoff
1999; Verdolin 2006). Environmental change can, by altering
this cost:benefit ratio, modify foraging behavior.
Urbanization, for instance, produces rapid environmental
change that dramatically transforms the biotic and abiotic
characteristics of populated areas worldwide (Shochat et al.
2006). While these changes are associated with many novel
stressors (e.g., habitat fragmentation, human activity, and
predators) that may alter foraging decisions in urban habitats,
the precise nature of these anthropogenically-driven changes
in foraging behavior is still unclear. Furthermore, the ability to
modify foraging behavior can determine whether or not ani-
mal populations persist in human-modified habitats.
One of the most striking differences between urban and
natural areas is their structural habitat. Urban habitats contain
fewer trees, lower vegetation (e.g., shrubs and lawns) and
more impervious surfaces than natural areas (Blair 1996;
Forman 2014). This decrease in structural complexity may
heighten perceived predation risk via greater exposure to
*Zachary A. Chejanovski
zchejanovski@gmail.com
1
Department of Biological Sciences, University of Rhode Island,
Kingston, RI 02881, USA
2
Present address: Department of Biology, University of Massachusetts
Boston, Boston, MA 02125, USA
3
Present address: Department of Organismic and Evolutionary
Biology, Harvard University, Cambridge, MA 02138, USA
Urban Ecosyst
DOI 10.1007/s11252-017-0654-5
potential predators and fewer refuges for prey (Whittingham
and Evans 2004). Vegetative cover influenced escape behavior
in the lizard Psammodromus algirus, for example, with indi-
viduals fleeing from an approaching predator at greater dis-
tances in more open areas (Martin and López 1995). Animals
may be less willing to forage in urban areas, or may restrict
foraging activity to residual vegetated fragments (i.e., green
spaces) they perceive as safer (Hodgson et al. 2006).
Similarly, small mammals abandoned artificial food patches
more quickly in open areas than when the patches were placed
nearer to and within vegetation (Bowers et al. 1993; Baker
et al. 2015). These studies suggest that habitat structure can
mediate the relationship between foraging activity and per-
ceived predation risk. While this research is useful, many stud-
ies addressing the topic do not separate out the potentially
confounding effects of predation and structural habitat (but
see Bouskila 1995). Experiments that do manipulate both fac-
tors in urban and natural sites, however, permit assessments of
how habitat structure per se influences foraging behavior.
Urban habitats containing abundant or novel predators could
have higher predation risk than natural areas (reviewed by
Fischer et al. 2012). Both feral and domestic cats have been
linked to the decline of various urban taxa (e.g., birds:
Lepczyk 2003; Baker et al. 2005; lizards: Ditchkoff et al.
2006; small mammals: Sims et al. 2008), and some urban hab-
itats have higher densities of generalist avian predators
(Jokimäki and Huhta, 2000;Sorace and Gustin, 2009).
Although increases in perceived predation risk may reduce for-
aging by some urban species, anthropogenic subsidies charac-
teristic of urban areas may decouple the relationship between
predator abundance and actual predation risk (Rodewald et al.
2011). Urban mesopredators such as raccoons, for example,
readily utilize artificial resources (Prange et al. 2004)thatin-
crease their abundance but decrease their need to prey on other
species. The fact that studies comparing anti-predator behavior
in prey from urban versus natural habitats produce inconsistent
results may reflect this decoupling of predator abundance and
predation risk. House finches from urban areas escaped at great-
er distances, suggesting that perceived predation risk is higher
in urban versus natural habitats (Valcarcel and Fernández-
Juricic 2009). A study of 44 European bird species, however,
found shorter escape distances in urban habitats (Møller 2008).
The question of whether prey respond appropriately to preda-
tion risk in urban environments, and how this response influ-
ences foraging behavior, remains unanswered.
Anolis lizards (or anoles) are ideal for research evaluating how
structural habitat and predation risk influence foraging in urban
and natural environments. Anoles are small, diurnal, mostly in-
sectivorous lizards for whom structural habitat –perch height,
diameter and substrate type –isakeynicheaxis(Losos2009).
Perch attributes such as diameter, inclination and roughness,
along with anole morphology, influence locomotor performance
(Losos and Sinervo 1989; Irschick and Losos 1999;Kolbeetal.
2015) and thus the ability of anoles to capture prey and evade
predators. Anoles utilize elevated perches to survey their territory
for potential prey, mating opportunities, and conspecific compet-
itors (Stamps 1977). The fact that perceived risk is inversely
related to perch height in anoles (Cooper 2006; Cooper 2010)
suggests that elevated perches are perceived as safer than ground
perches. For instance, anoles traveling farther on the ground to
feed in an experimental setting used more intermediate perches
compared to when feeding closer to their original perch (Drakeley
et al. 2015). Other studies have also shown that although anoles
are primarily ground foragers (Losos 1990;Lapiedraetal.2017),
they become more arboreal in the presence of ground-dwelling
predators (Schoener et al. 2002; Losos et al. 2004).
In this study, we experimentally manipulated foraging op-
portunities for two Anolis species –the brown anole
(A. sagrei) in Florida and the crested anole (A. cristatellus)
in Puerto Rico –to assess whether foraging decisions differ
between habitats varying in their degree of urbanization.
During these experiments, we manipulated perch availability
and predator presence in each habitat type to determine their
effects on perceived predation risk and foraging decisions. We
also considered how factors such as perch availability, body
temperature, conspecific density and body size, might also
contribute to differences in foraging behavior. Our research
sought to assess the willingness of lizards to forage in urban
and natural forest habitats, and to explore how structural hab-
itat and predator presence influenced foraging decisions.
Methods
Site selection
We examined Anolis foraging behavior in populations occu-
pying both urban and natural habitats. All experiments were
conducted during warm days (>25 °C during trials) between
the hours of 0900 and 1900 when lizards were active.
Foraging trials with A. cristatellus were conducted in
July 2014 in urban and natural forest sites within the San
Juan metropolitan area of Puerto Rico. Trials with A. sagrei
were conducted during April–May 2015 in urban, suburban,
and natural forest sites (each replicated twice) in southeast
Florida (Broward County). Natural forest habitats were sec-
ondary forests characterized by relatively closed canopies,
dense vegetation, and little human disturbance. No humans
or domestic animals were observed in any of our natural sites
throughout the course of these experiments. Urban habitats
consisted of sparse vegetation, more open space (typically
covered by mown lawn or impervious surfaces), and increased
pedestrian traffic compared to natural habitats. Suburban hab-
itats (A. sagrei experiments only) were roadside areas inter-
mediate between urban and natural sites in terms of vegetation
density, open space, and pedestrian disturbance.
Urban Ecosyst
Experimental procedure
We first located male lizards perched in survey posture on a
vertical substrate (e.g., tree or wall). Survey posture –head
downward, hind limbs extended up the vertical surface, and
upper body pushed away from the substrate –indicates an anole
receptive to foraging (Stamps 1977); anoles seem to abandon
this posture when fed to satiation (Drakeley et al. 2015). After
locating an anole, we placed a foraging tray with two meal-
worms directly in front of this focal lizard at a distance of 1 m
from the base of the perch for A. cristatellus and five meal-
worms at a 2-m distance for A. sagrei. Mealworms were larvae
of the darkling beetle, Tenebrio molitor, which have been used
successfully as a food resource in previous studies (Drakeley
et al. 2015;Lapiedraetal.2017). These quantities of meal-
worms elicited the fastest responses for each species in pilot
trials conducted near our study sites. Foraging trays were ini-
tially covered with an opaque material to prevent lizards from
seeing the mealworms before the researcher was able to move
to a distance >3 m from the tray (see Drakeley et al. 2015;
Lapiedra et al. 2017). Lizards were allowed to habituate for
two minutes, after which time the cover was removed by
pulling an attached string, signaling the start of the trial. All
trials were recorded using a digital video camera placed on a
tripod ~1 m from the foraging tray. Latency to feed (in seconds)
was measured from these videos as the time from when the
cover was removed from the foraging tray to when the first
mealworm was captured. Experimental time was limited to
20 min and non-responses were assigned this maximum time.
Half of the foraging trials in each habitat type for each species
were experimentally manipulated to test whether perch availabil-
ity (for A. sagrei) and perceived predation risk (for A. cristatellus)
influenced foraging decisions. For A. sagrei, we placed two
perches directly between the focal lizard and the feeding tray to
increase perch availability in these trials. Perches were ~3 cm in
diameter and 1-m tall and constructed using wood collected from
the study sites. Lizards readily used these perches in pilot trials.
For A. cristatellus, we placed a static model of a bird predator
~30 cm behind the foraging tray to increase perceived predation
risk.Weusedataxidermyspecimenofapearly-eyedthrasher
(Margarops fuscatus), a bird commonly found in both urban and
natural areas of San Juan that has been previously reported to
prey upon anoles (Adolph and Roughgarden 1983).
In addition to these experimental manipulations, we also
measured a number of variables that could potentially influ-
ence latency to feed. Because lizard-accessible perches may
serve as refuges or increase the possibility of detecting predators,
we measured the number of perches within a 1 m radius of the
focal lizard for A. cristatellus and within 0.5 m of the line be-
tween the feeding tray and focal lizard for A. sagrei, not including
experimentally-added perches. We standardized these measures
by calculating perch density (i.e., number of perches per unit
area). Perches were considered as any substrate elevated above
20 cm and >0.5 cm in diameter. We also measured the perch
height of the focal lizard at the start of the trial because lizards
perched higher may be satiated from previous foraging opportu-
nities (Stamps 1977). Higher perches may also enable lizards to
survey a larger area and thus receive more information regarding
predation risk (Scott et al. 1976) prior to foraging.
Foraging decisions can also be influenced by temperature.
As ectotherms, body temperature greatly affects lizard loco-
motor performance (Angilletta 2009) and digestive efficiency
(Harwood 1979). Because urban areas often act as heat islands
(Oke 1973), their higher ambient temperatures relative to
nearby natural areas could increase the body temperatures of
urban lizards. To estimate body temperature, we placed a cop-
per lizard model at the original position of the focal lizard and
allowed temperature readings to stabilize before recording its
internal temperature (Hertz 1992; Gunderson and Leal 2015).
While conspecific presence can dilute predation risk (as
reviewed by Roberts 1996) or provide cues regarding the qual-
ity of a resource patch (Stamps 1987), higher conspecific den-
sities also increase intraspecific competition and the chance of
missing foraging opportunities (Drakeley et al. 2015). We mea-
sured the number of conspecifics within a 5 m radius of the
focal lizard for A. cristatellus and within a 3 m radius of the
focal lizard for A. sagrei.Again,westandardizedthesemea-
sures by calculating conspecific density (i.e., number of con-
specifics per unit area). We also recorded whether one or more
conspecifics approached the foraging tray during the trial. In
laboratory-based staged encounters, larger individuals success-
fully defended preferred perches from smaller anoles (Tokarz
1985). Because similar outcomes could result during competi-
tion for foraging opportunities, we measured body size as
snout-vent length (SVL) and mass from a representative sam-
ple of each lizard population. We also used these measure-
ments to calculate body condition (i.e., scaled mass index
following the methods of Peig and Green 2009)asaproxy
for motivation, given that whether a lizard is hungry or satiated
(i.e., motivational state) can influence the trade-off between
costs and benefits when making a foraging decision. For ex-
ample, a lizard may be willing to accept greater risk in order to
acquire food if it has not fed for an extended period of time or if
prey items are rarely encountered. We also calculated body
condition for a subset of A. sagrei individuals that we were
able to capture following their foraging trial (this was not done
for A. cristatellus). To estimate the original body mass of these
individuals, we measured the average weight of each meal-
worm and subtracted the mass of any mealworms consumed
from the mass of each lizard.
Statistical analysis
We tested for statistical differences in latency to feed by
performing survival analysis. We used a Cox proportional haz-
ards model available in the R-package Bsurvival^(Therneau
Urban Ecosyst
and Lumley 2015). This semi-parametric model is capable of
dealing with right-censored data such as those obtained by
limiting our foraging trials to a maximum of 20 min. Model
selection was based on AICc scores (Burnham and Anderson
2004) and only significant (or marginally non-significant) fac-
tors were retained in the best models. Following Burnham and
Anderson (2004), the model with the fewest factors was
favored when models differed by less than two units from
the best model. Differences in mean SVL, mass, body
condition, estimated body temperature, conspecific density
and perch availability among habitat types were tested using
t-tests or analysis of variance (ANOVA) and Tukey’sHonest
Significant Difference (HSD) post hoc tests when data were
normally distributed (as determined from Shapiro-Wilks test
of normality). When data could not be normalized, differences
were tested using Kruskal-Wallisranksumtests(pairwise)or
Dunn’s test (multiple comparisons; R-package Bdunn.test^;
Dinno 2016) using rank sums with Bonferroni correction. For
the subset of A. sagrei individuals we were able to measure
following their foraging trial, we tested the relationship be-
tween body condition and latency to feed using Pearson’sprod-
uct moment correlation. All analyses were performed using R
statistical software (R Development Core Team 2015).
Results
For A. cristatellus, lizards from forest habitats fed faster than
those from urban habitats (coeff. = −0.82, z=−2.12, p= 0.034,
Fig. 1) and had an overall greater response rate (63% in forest vs.
26% in urban). Similarly, A. sagrei from forests fed faster than
those in either suburban (coeff. = −1.50, z=−2.95, p= 0.003) or
urban habitats (coeff. = −1.67, z=−3.01, p= 0.003). Forest
A. sagrei also had a greater response rate (38%) than those from
urban (10%) or suburban (11%) habitats. However, latency to
feed did not differ between urban and suburban habitats for
A. sagrei (coeff. = −0.17, z=−0.25, p= 0.799, Fig. 2). Habitat
type was the only factor in the best model for A. sagrei,whereas
habitat type, perch height, and conspecifics present at the
foraging tray were significant factors for A. cristatellus
(Table 1). Specifically, higher-perching A. cristatellus individuals
took longer to feed than those perched nearer to the ground
(coeff. = −0.01, z=−3.48, p< 0.001), and focal lizards tended
to have shorter latencies when a conspecific attempted to feed
from the tray (coeff. = 0.74, z=1.87,p= 0.06).
At the habitat level, there were more perches available in
natural forests compared to urban habitats for A. cristatellus
(Kruskal-Wallis rank sum test; X
2
= 20.42, df = 1, p< 0.001;
Tab le 2). The number of available perches for A. sagrei was also
higher in natural habitats compared to both urban (Dunn’stest
using rank sums; z=−4.12, df = 2, p< 0.001) and suburban
(Dunn’s test using rank sums; z=−4.87, df = 2, p< 0.001)
habitats, but urban and suburban habitats did not differ (Dunn’s
test using rank sums; z= 0.71, df = 2, p= 0.720). Forest A. sagrei
were smaller (SVL) and weighed less than suburban and urban
populations (Table 2), but urban and suburban lizards did not
differ. Urban A. sagrei had better body condition compared to
forest lizards (Table 2), but suburban lizards did not differ from
either urban (Dunn’s test using rank sums; z=1.17,df=2,
p= 0.122) or forest populations (Dunn’s test using rank sums;
z= 1.00, df = 2, p= 0.160). The relationship between latency to
feed and body condition for A. sagrei captured following a for-
aging trial was not significant for either the urban/suburban
(Pearson’s product-moment correlation; t=−0.31, df = 56,
p= 0.758) or natural forest habitat (Pearson’s product-moment
correlation; t=−0.39, df = 29, p= 0.708). Forest A. cristatellus
were also smaller (SVL) and weighed less compared to urban
lizards, but body condition did not differ between these popula-
tions (Table 2).
Discussion
Anoles in urban habitats took longer to feed than those in
forest habitats, a result consistent across two species in two
geographically distinct locations. Moreover, a large propor-
tion of urban lizards (80–90%) never responded to foraging
opportunities in our experimental trials. This is contrary to
Fig. 1 Survival analysis
comparing latency to feed of
A. sagrei populations from natural
forest (n= 42), suburban (n=44)
and urban habitats (n=42)
Urban Ecosyst
research on birds and mammals in which greater foraging
activity was observed in experimental food patches placed in
urban habitats compared to natural ones (Bowers and Breland
1996; Shochat et al. 2004). While such studies are rare in
lizards, a recent study on delicate skinks (Lampropholis
delicata) found no differences in foraging-related behaviors
between urban and forest populations (Moulé et al. 2015).
Although our experimental manipulations of perch availabil-
ity and predator presence did not affect anole foraging,
A. cristatellus had shorter latencies to feed when perched low-
er and when conspecifics attempted to forage. The difference
in anole foraging between urban and natural habitats could
result from variation in at least three factors: perceived preda-
tion risk, motivation of lizards to forage, or neophobia.
If anoles perceive greater predation risk in urban versus
forest habitats, this could explain why most urban anoles were
unwilling to forage. Perceived risk could be increased by re-
duced perch availability in urban areas, thereby increasing
exposure to potential predators. Perch density in each of our
urban foraging trials was at least 50% lower than in forest
trials (Table 3). Previous work has linked decreased vegetative
cover to an increase in predation pressure using mesocosms
(Finke and Denno 2002) and clay models (Shepard 2007).
However, perch availability was not a significant factor
influencing latency to feed, even when experimentally in-
creased in A. sagrei foraging trials.
An increase in perceived predation risk could also reflect
higher predator abundance in urban habitats (Sorace 2002).
The extirpation of top predators from urban areas can increase
mesopredator abundance (Soulé et al. 1988; Rogers and Caro
1998;CrooksandSoule1999). Many potential predators of
anoles have successfully colonized urban areas, including
birds (Clergeau et al. 1998; Croci et al. 2008), mammals
(Ordeñana et al. 2010) and other lizards (Smith et al. 2004).
Although this study did not assess predator abundance, we
saw multiple bird species, including great egrets (Ardea alba)
and yellow crowned night-herons (Nyctanassa violacea),
searching for and consuming anoles in urban habitats (Z.
Chejanovski, pers. obs.). Anoles likely detect such predators
via movement; movement of a model snake, for instance,
elicited a deterrent response from anoles in Puerto Rico
(Leal 1999). The lack of any response by A. cristatellus to
our model predator likely reflects the absence of any move-
ment; during one trial, a lizard actually perched on the model’s
head. This lack of response emphasizes the importance of
coupling life-like models with movement to simulate the pres-
ence and hunting strategy of a particular predator.
The urban-forest difference in foraging behavior may also
reflect habitat-linked variation in the motivational state of
each lizard population. Although we attempted to control for
among-individual differences in motivation by only selecting
anoles found in survey posture (see Methods; Drakeley et al.
2015), perch height may also indicate anole foraging motiva-
tion. Perch height negatively influenced willingness to feed
for A. cristatellus (Table 1), and Stamps (1977) observed that
female anoles perched higher after being fed to satiation. If
Fig. 2 Survival analysis
comparing latency to feed of
A. cristatellus populations from
natural forest (n=38)andurban
habitats (n=45)
Tabl e 1 Results of the best Cox
proportional hazards model for
each species summarizing the
effects of each factor on latency to
feed relative to natural habitats
A. sagrei Variable Coeff. Exp(coef) SE(coef) Z P-value
Suburban -1.50 0.22 0.51 -2.95 0.003
Urban -1.67 0.19 0.56 -3.01 0.003
A. cristatellus Urban -0.82 0.44 0.39 -2.12 0.034
Conspecifics Present 0.74 2.10 0.40 1.88 0.061
Perch Height -0.01 0.99 0.01 -3.48 < 0.001
Latency to feed did not differ between urban and suburban habitats for A. sagrei (z=−0.254, p=0.799)
Urban Ecosyst
higher-perching A. cristatellus aremorelikelytobesatiated,
lower-perching lizards may be more receptive to ground-
dwelling prey. Consistent with the Bmotivational state^hy-
pothesis, we found that urban lizards in both species were
larger (SVL and mass) and, for A. sagrei, in better body con-
dition than their forest-dwelling conspecifics (Table 3). Body
condition may represent a measure of the energy stores avail-
able to an organism, acquired from previous foraging oppor-
tunities (Jakob et al. 1996). In ground squirrels (Spermophilus
beldingi), for instance, individuals with lower body condition
spent more time foraging under risky conditions (Bachman
1993). Additionally, Allenby’s gerbils (Gerbillus andersoni
allenbyi) supplemented with food (thus increasing condition
of these individuals) allocated more time surveying for pred-
ators and less time foraging under predation risk (Kotler et al.
2004). If forest anoles are more food-limited, they may choose
to feed on the ground despite the risk. Such Brisky^behavior
occurs when the costs of a missed opportunity exceeds those
caused by predation (Lima and Dill 1990), which is often the
case when food is scarce. Lizards alter their behavior in rela-
tion to food availability, and may take more risks when re-
sources are scarce; anoles, for instance, responded faster to
feeding trays containing less food than to trays with more food
(Drakeley et al. 2015). Podarcis lizards decreased flight-
initiation distance in response to increasing food abundance
(Cooper et al. 2006), highlighting their ability to weigh the
costs of predation risk against the benefits of resource acqui-
sition. Nonetheless, in our study, the relationship between la-
tency to feed and body condition was not significant in either
urban/suburban or natural forest populations of A. sagrei.
Neophobia, the tendency of an animal to avoid novel food
resources or objects, could also explain the response of urban
anoles to our foraging trays. While neophobic behaviors protect
animals from the dangers associated with unfamiliar stimuli
(Greenberg 1990; Greenberg and Mettke-Hofmann 2001), they
can also hinder the ability of animals to exploit novel food
resources, a trait central to the success of some urban species
(Sol et al. 2011). The fact that the mealworms used in this study
are not a common food resource in urban areas may have de-
terred the anoles. In a previous study, however, a majority of
anoles from similar urban habitats responded when mealworms
were presented without a feeding tray (Lapiedra et al. 2017);
this suggests that the feeding tray itself may elicit neophobia in
urban anoles. However, other herpetological studies comparing
urban and natural conspecifics found no differences in
neophobia (Candler and Bernal 2015; Moulé et al. 2015).
Tabl e 2 Summary of statistical
tests comparing mean differences
between urban and natural forest
habitats
A. cristatellus A. sagrei
Variable Statistic df P Statistic df P
Perch Height t=−2.53 75.67 0.013 z=−3.17 2 <0.001
Conspecific Density X
2
= 0.18 1 0.668 z= 2.89 2 0.002
Body Temperature t=−11.21 79.69 <0.001 q = 42.41 2 0.999
Perch Availability X
2
= 20.42 1 <0.001 z=−4.12 2 <0.001
SVL t= 3.89 33.54 <0.001 z=4.43 2 <0.001
Body Mass t= 3.43 37.96 <0.001 z=5.03 2 <0.001
Body Condition X
2
=19 19 0.457 z= 2.27 2 0.012
Because most values for suburban A. sagrei were statistically indistinguishable from those in urban habitats,
comparisons between suburban and forest habitats are not shown
Tabl e 3 Summary of variables
(mean ± SE) hypothesized to
influence latency to feed for each
species in each habitat type
A. cristatellus A. sagrei
Habitat Type Natural Urban Natural Suburban Urban
N3845424442
Perch Height 137.33 ± 9.12 167.39 ± 1.13 116.48 ± 8.03 89.61 ± 7.29 83.79 ± 6.84
Conspecific Density 0.04 ± 0.0006 0.04 ± 0.0004 0.02 ± 0.005 0.05 ± 0.008 0.05 ± 0.006
Body Temperature 30.58 ± 0.02 32.66 ± 0.02 30.87 ± 0.33 30.77 ± 0.44 30.85 ± 0.40
Perch Availability 3.73 ± 0.28 1.82 ± 0.24 3.15 ± 0.32 1.23 ± 0.30 1.36 ± 0.24
N2020312632
SVL 65.4 ± 0.45 68.5 ± 0.66 52.58 ± 0.91 58.23 ± 0.88 58.09 ± 0.65
Body Mass 8.63 ± 0.30 10.12 ± 0.31 3.60 ± 0.20 5.24 ± 0.25 5.37 ± 0.18
Body Condition 9.30 ± 0.41 9.08 ± 0.37 4.98 ± 0.08 5.07 ± 0.11 5.30 ± 0.11
Urban Ecosyst
Our results demonstrate clear differences in foraging be-
havior between anoles from urban and forest habitats. These
patterns could result from differences in perceived predation
risk, motivation to forage, neophobia, or a combination of
these factors. Although selection pressures in urban and natu-
ral habitats likely favor different behavioral strategies (Hendry
et al. 2008; Audet et al. 2016; Lapiedra et al. 2017;reviewed
in Sol et al. 2013), we are far from understanding how urban-
ization alters animal behavior (Shochat et al. 2006).
Furthermore, it is pivotal that future research address whether
changes in foraging and other behaviors can allow animal
populations to persist in urban environments, which is critical
to predict and mitigate potential changes in biodiversity.
Acknowledgements This research was funded by a grant from the
National Science Foundation (DEB-1354897) and funds from the
University of Rhode Island. Protocols for use of vertebrate animals in this
study were approved by the Institutional Animal Care and Use Committee
at the University of Rhode Island (AN11-09-005). Permits were provided
by Broward County Parks and Recreation (Florida) (ES01152015-001).
We thank the University of Puerto Rico for permission to conduct this study
on their property and the staff of the Museum of Zoology at the University
of Puerto Rico for laboratory space and logistical support. Christopher
Thawley provided important suggestions for our body condition analysis.
References
Adolph SC, Roughgarden J (1983) Foraging by passerine birds and
Anolis lizards on St. Eustatius (Neth. Antilles): implications for in-
terclass competition, and predation. Oecologia 56:313–317
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical
synthesis. Oxford University Press
Audet J-N, Ducatez S, Lefebvre L (2016) The town bird and the country
bird: problem solving and immunocompetence vary with urbaniza-
tion. Behav Ecol 27:637–644
Bachman GC (1993) The effect of body condition on the trade-off be-
tween vigilance and foraging in Belding’s ground squirrels. Anim
Behav 46:233–244
Baker PJ, Bentley AJ, Ansell RJ, Harris S (2005) Impact of predation by
domestic cats Felis catus in an urban area. Mamm Rev 35:302–312
Baker MAA, Emerson SE, Brown JS (2015) Foraging and habitat use of
eastern cottontails (Sylvilagus floridanus) in an urban landscape.
Urban Ecosyst 18:977–987
Blair RB (1996) Land use and avian species diversity along an urban
gradient. Ecol Appl 6:506–519
Bouskila A (1995) Interactions between predation risk and competition: a
field study of kangaroo rats and snakes. Ecology 76:165–178
Bowers MA, Breland B (1996) Foraging of gray squirrels on an urban-
rural gradient: use of the GUD to assess anthropogenic impact. Ecol
Appl 6:1135–1142
Bowers MA, Jefferson JL, Kuebler MG (1993) Variation in giving-up
densities of foraging chipmunks (Tamias striatus) and squirrels
(Sciurus carolinensis). Oikos 66:229–236
Burnham KP, Anderson DR (2004) Multimodel inference: understanding
AIC and BIC in model selection. Sociol Methods Res 33:261–304
Candler S, Bernal XE (2015) Differences in neophobia between cane
toads from introduced and native populations. Behav Ecol 26:97–
104
Clergeau P, Savard J-PL, Mennechez G, Falardeau G (1998) Bird abun-
dance and diversity along an urban-rural gradient: a comparative
study between two cities on different continents. Condor 100:413–
425
Cooper WE (2006) Risk factors affecting escape behaviour by Puerto
Rican Anolis lizards. Can J Zool 84:495–504
Cooper WE (2010) Escape tactics and effects of perch height and habit-
uation on flight initiation distance in two Jamaican anoles
(Squamata: Polychrotidae). Rev Biol Trop 58:1199–1209
Cooper WE, Peréz-Mellado V, Hawlena D (2006) Magnitude of food
reward affects escape behavior and acceptable risk in Balearic liz-
ards, Podarcis lilfordi. Behav Ecol 17:554–559
Croci S, Butet A, Clergeau P (2008) Does urbanization filter birds on the
basis of their biological traits? Condor 110:223–240
Crooks KR, Soule ME (1999) Mesopredator release and avifaunal extinc-
tions in a fragmented system. Nature 400:563–566
Dall SRX, Giraldeau L-A, Olsson O et al (2005) Information and its use
by animals in evolutionary ecology. Trends Ecol Evol 20:187–193
Dinno A (2016) Package ‘dunn.test’
Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban
ecosystems: modifications due to human-induced stress. Urban
Ecosyst 9:5–12
Drakeley M, Lapiedra O, Kolbe JJ (2015) Predation risk perception, food
density and conspecific cues shape foraging decisions in a tropical
lizard. PLoS One 10:e0138016
Finke DL, Denno RF (2002) Intraguild predation diminished in complex-
structured vegetation: implications for prey suppression. Ecology
83:643–652
Fischer JD, Cleeton SH, Lyons TP et al (2012) Urbanization and the
predation paradox: the role of trophic dynamics in structuring ver-
tebrate communities. Bioscience 62:809–818
Forman R (2014) Urban ecology: science of cities. Cambridge University
Press
Greenberg R (1990) Feeding neophobia and ecological plasticity: a test of
the hypothesis with captive sparrows. Anim Behav 39:375–379
Greenberg R, Mettke-Hofmann C (2001) Ecological aspects of
neophobia and neophilia in birds. Curr Ornithol 16:119–178
Gunderson AR, Leal M (2015) Patterns of thermal constraint on ecto-
therm activity. Am Nat 185:653–664
Harwood RH (1979) The effect of temperature on the digestive efficiency
of three species of lizards, Cnemidophorus tigris,Rrhonotus
multicarinatus,andSceloporus occidentalis. Comp Biochem
Physiol Part A Physiol 63:417–433
Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates
of phenotypic change in wild animal populations. Mol Ecol 17:20–
29
Hertz PE (1992) Temperature regulation in Puerto Rican Anolis lizards: a
field test using null hypotheses. Ecology 73:1405–1417
Hodgson P, French K, Major RE (2006) Comparison of foraging behav-
iour of small, urban-sensitive insectivores in continuous woodland
and woodland remnants in a suburban landscape. Wildl Res 33:591–
603
Irschick DJ, Losos JB (1999) Do lizards avoid habitats in which perfor-
mance is submaximal? The relationship between sprinting capabil-
ities and structural habitat use in Caribbean anoles. Am Nat 154:
293–305
Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a compar-
ison of body condition indices. Oikos 77:61–67
Jokimäki J, Huhta E (2000) Artificial nest predation and abundance of
birds along an urban gradient. Condor 102:838–847
Kolbe JJ, Battles AC, Avilés-Rodríguez KJ (2015) City slickers: poor
performance does not deter Anolis lizards from using artificial sub-
strates in human-modified habitats. Funct Ecol doi. doi:10.1111
/1365-2435.12607
Kotler BP, Brown JS, Bouskila A (2004) Apprehension and time alloca-
tion in gerbils: the effects of predatory risk and energetic state.
Ecology 85:917–922
Urban Ecosyst
Lapiedra O, Chejanovski ZA, Kolbe JJ (2017) Urbanization and biolog-
ical invasionshape animal personalities. Glob Change Biol 23:592–
603. doi:10.1111/gcb.13395
Leal M (1999) Honest signalling during prey–predator interactions in the
lizard Anolis cristatellus. Anim Behav 58:521–526
Lepczyk C (2003) Landowners and cat predation across rural-to-urban
landscapes. Biol Conserv 115:191–201
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives an-
tipredator behavior: the predation risk allocation hypothesis. Am
Nat 153:649–659
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of
predation: a review and prospectus. Can J Zool 68:619–640
Losos JB (1990) Ecomorphology, performance capability, and scaling of
west Indian Anolis lizards: an evolutionary analysis. Ecol Monogr
60:369–388
Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive
radiation of anoles. University of California Press
Losos JB, Sinervo B (1989) The effects of morphology and perch diam-
eter on sprint performance of Anolis lizards. J Exp Biol 145:23–30
Losos JB, Schoener TW, Spiller DA (2004) Predator-induced behaviour
shifts and natural selection in field-experimental lizard populations.
Nature 432:505–508
Martin J, López P (1995) Influence of habitat structure on the escape
tactics of the lizard Psammodromus algirus.CanJZool73:129–132
Møller AP (2008) Flight distance of urban birds, predation, and selection
for urban life. Behav Ecol Sociobiol 63:63–75
Moulé H, Michelangeli M, Thompson MB, Chapple DG (2015) The
influence of urbanization on the behaviour of an Australian lizard
and the presence of an activity-exploratory behavioural syndrome. J
Zool 298:103–111
Oke TR (1973) City size and the urban heat island. Atmos Environ 7:
769–779
Ordeñana MA, Crooks KR, Boydston EE et al (2010) Effects of urban-
ization on carnivore species distribution and richness. J Mammal 91:
1322–1331
Peig J, Green AJ (2009) New perspectives for estimating body condition
from mass/length data: the scaled mass index as an alternative
method. Oikos 118:1883–1891
Prange S, Gehrt SD, Wiggers EP (2004) Influences of anthropogenic
resources on raccoon (Procyon lotor) movements and spatial distri-
bution. J Mammal 85:483–490
R Development Core Team (2015) R: A language and environment for
statistical computing.
Roberts G (1996) Why individual vigilance declines as group size in-
creases. Anim Behav 51:1077–1086
Rodewald AD, Kearns LJ, Shustack DP (2011) Anthropogenic resource
subsidies decouple predator–prey relationships. Ecol Appl 21:936–
943
Rogers CM, Caro MJ (1998) Song sparrows, top carnivores and nest
predation: a test of the mesopredator release hypothesis. Oecologia
116:227–233
Schoener TW, Spiller DA, Losos JB (2002) Predation on a common
Anolis lizard: can the food-web effects of a devastating predator be
reversed? Ecol Monogr 72:383–407
Scott NJ, Wilson DE, Jones C, Andrews RM (1976) The choice of perch
dimensions by lizards of the genus Anolis (Reptilia, Lacertilia,
Iguanidae). J Herpetol 10:75–84
Shepard DB (2007) Habitat but not body shape affects predator attack
frequency on lizard models in the Brazilian Cerrado. Herpetologica
63:193–202
Shochat E, Lerman SB, Katti M, Lewis DB (2004) Linking optimal
foraging behavior to bird community structure in an urban-desert
landscape: field experiments with artificial food patches. Am Nat
164:232–243
Shochat E, Warren PS, Faeth SH et al (2006) From patterns to emerging
processes in mechanistic urban ecology. Trends Ecol Evol 21:186–
191
Sims V, Evans KL, Newson SE et al (2008) Avian assemblage structure
and domestic cat densities in urban environments. Divers Distrib 14:
387–399
Smith MM, Smith HT, Engeman RM (2004) Extensive contiguous
north–south range expansion of the original population of an inva-
sive lizard in Florida. Int Biodeterior Biodegradation 54:261–264
Sol D, Griffin AS, Bartomeus I, Boyce H (2011) Exploring or avoiding
novel food resources? The novelty conflict in an invasive bird. PLoS
One 6:e19535
Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments
for a life in the city. Anim Behav 85:1101–1112
Sorace A (2002) High density of bird and pest species in urban habitats
and the role of predator abundance. Ornis Fenn 79:60–71
Sorace A, Gustin M (2009) Distribution of generalist and specialist pred-
ators along urban gradients. Landsc Urban Plan 90:111–118
Soulé ME, Bolger DT, Alberts AC et al (1988) Reconstructed dynamics
of rapid extinctions of chaparral-requiring birds in urban habitat
islands. Conserv Biol 2:75–92
Stamps JA (1977) The function of the survey posture in Anolis lizards.
Copeia 1977:756–758
Stamps JA (1987) Conspecifics as cues to territory quality: a preference
of juvenile lizards (Anolis aeneus) for previously used territories.
Am Nat 129:629–642
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University
Press
Therneau TM, Lumley T (2015) Package 'survival'
Tokarz RR (1985) Body size as a factor determining dominance in staged
agonistic encounters between male brown anoles (Anolis sagrei).
Anim Behav 33:746–753
Valcarcel A, Fernández-Juricic E (2009) Antipredator strategies of house
finches: are urban habitats safe spots from predators even when
humans are around? Behav Ecol Sociobiol 63:673–685
Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-
offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464
Whittingham MJ, Evans KL (2004) The effects of habitat structure on
predation risk of birds in agricultural landscapes. Ibis 146:210–220
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