Town and Country Reptiles: A Review of Reptilian Responses To Urbanization

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Town and Country Reptiles: A Review of Reptilian Responses to Urbanization
Article in Integrative and Comparative Biology · June 2018

DOI: 10.1093/icb/icy052
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Integrative and Comparative Biology
Integrative and Comparative Biology, pp. 1–19
doi:10.1093/icb/icy052 Society for Integrative and Comparative Biology
SYMPOSIUM
Town and Country Reptiles: A Review of Reptilian

Responses to Urbanization
Susannah S. French,1 Alison C. Webb, Spencer B. Hudson and Emily E. Virgin
Department of Biology, Utah State University, Logan, UT 84322, USA and Ecology Center, Utah State University, Logan,
UT 84322, USA
From the symposium “Behavioral and Physiological Adaptation to Urban Environments” presented at the annual
meeting of the Society for Integrative and Comparative Biology, January 3–7, 2018 at San Francisco, California.
All authors contributed equally to this manuscript.
1
E-mail: susannah.french@usu.edu
Synopsis The majority of the world population is now inhabiting urban areas, and with staggering population growth,
urbanization is also increasing. While the work studying the effects of changing landscapes and specific urban pressures
on wildlife is beginning to amass, the majority of this work focuses on avian or mammalian species. However, the effects
of urbanization likely vary substantially across taxonomic groups due to differences in habitat requirements and life
history. The current article aims first to broaden the review of urban effects across reptilian species; second, to sum-
marize the responses of reptilian fauna to specific urban features; and third, to assess the directionality of individual and
population level responses to urbanization in reptile species. Based on our findings, urban research in reptilian taxa is
lacking in the following areas: (1) investigating interactive or additive urban factors, (2) measuring multiple morpho-
logical, behavioral, and physiological endpoints within an animal, (3) linking individual to population-level responses,
and (4) testing genetic/genomic differences across an urban environment as evidence for selective pressures.
Overview areas (e.g., passerines in different cities across the

Increasing human population growth necessitates the United States and Europe), but the results are often
development and expansion of urban areas. The urban conflicting. This discrepancy is due in part to the
environment poses novel and diverse challenges for spe- heterogeneity of urban landscapes, to the large num-
cies that inhabit the landscape. Abiotic factors such as ber of interacting and coinciding stressors in an ur-
noise, artificial light, hydrology, and temperature ban landscape, but perhaps most significantly to the
changes (e.g., urban heat island) can cause stress, alter fact that species responses vary considerably. While
timing of life history events, and affect behavior and most work has focused on avian and mammalian
basic physiological functioning. Human-built struc- responses to urbanization, there are a growing num-
tures can also provide habitat options for reptile species. ber of studies investigating other taxonomic groups
Biotic factors, such as invasive species, can also alter (Mitchell et al. 2008), although much of the urban
community and trophic interactions as well as patho- work in amphibians and reptiles is investigating the
gen exposure. Thus, the potential number of urban abundance and spread of invasive species (Gibbon
effectors for native species is large. et al. 2000). Assessing the impacts on multiple tax-
While the general consensus is that urbanization onomic groups and a diversity of ecosystems is crit-
reduces species richness, the mechanisms for that ical due to differences in dispersal, habitat, ecology,
reduction are unclear (McKinney 2008). Studies physiology, and life history of species inhabiting ur-
have documented responses of wildlife to specific ban landscapes as well as those that are unable to
urban areas (e.g., changes within one municipality inhabit these areas (McKinney 2008; Allen et al.
over time), or specific species to different urban 2017). The current review is poised to accomplish
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2 S. S. French et al.
three main aims. First, is to broaden the review of (Ackley et al. 2015b). Whereas, when identifying spe-
urban effects across reptilian species. It is critical to cies factors of impact on herpetofauna in northern
assess a diversity of taxonomic groups and not solely Italy, litter and direct disturbance are negatively re-
focus on a few models species for the health of the lated to species richness (Ficetola et al. 2007).
overall ecosystem. Second, it is critical to summarize Habitat fragmentation also plays an important
the responses of reptilian fauna to specific urban role in species richness of herpetofauna (Dickman
features. This is necessary because the majority of 1987; Irwin et al. 2010). Patch size in particular
the research on urban reptiles to date assesses pres- has repeatedly been shown as an important predictor
ence or abundance, which is important, but under- of reptile species richness in many different environ-
standing how animals respond to specific features ments (Dickman 1987; Garden et al. 2007; 2010) and
(e.g., contaminants, invasive species, light, noise, of species evenness (i.e., species diversity) in others
etc.) will allow for better management moving for- (Sullivan et al. 2014). For example, remnants in met-
ward. Third, it is essential for researchers to assess ropolitan Perth, Australia were found to be an im-
the directionality of behavioral, physiological, and portant predictor of species richness with bigger
population level responses to urbanization in rep- remnants having more reptile species (How and
tiles. By doing so, we will gain a better understand- Dell 2000). Similarly, by using specialized habitats
ing of the directionality of responses, both individual in NJ, USA (i.e., Pine Barrens) some species of
and population level, providing mechanisms for the snakes are able to thrive (Zappalorti and Mitchell
effects of urban features on wildlife. This is critical as 2008). Importantly, many of these studies show
there is surmounting evidence that reptiles are de- that maintaining structural complexity and remnant
clining worldwide for a number of reasons including habitat patches can help protect some species
urbanization (Gibbon et al. 2000; Mitchell et al. (Hamer and McDonnell 2008). The effects of patch
2008; Todd et al. 2010). size appear to be species dependent, whereby habitat
fragmentation in the Midwestern United States ad-
versely effects some species of turtles (red-eared
Responses to specific urban features
sliders, Trachemys scripta elegans) more than other
Largescale landscape changes and habitat species (e.g., midland painted turtles, Chrysemys picta
fragmentation marginata, eastern spiny softshells, Apalone spinifera
The majority of research available regarding the spinifera, common snapping turtles, Chelydra serpen-
effects of urbanization on reptiles focuses primarily tina serpentina) (Rizkalla and Swihart 2006; Ryan
on species richness or presence/absence data et al. 2014).
(Table 1A). While most work demonstrates a de- The vast majority of work, however, demonstrates
crease in population size or species richness with a negative impact of urbanization on reptiles. For
urbanization, a few studies instead find the opposite example, Lowe found that encroaching urbanization
relationship. Rodda and Tyrrell (2008) review life was associated with altered riparian habitat and the
history characteristics of invasive, urban, and pet extinction of several reptiles (e.g., Thamnophis spe-
herpetofauna and found that many invasive species cies) in the American southwest (1985). These effects
thrive in urban settings. However, some native spe- are seen worldwide, as for example, reptile species
cies such as snakes also persist and even thrive in richness in Bulgaria was found to be highest in rural
urban environments (Schlauch 1978). Moreno- zones and followed by urban and suburban zones
Rueda and Pizarro (2007) found that reptile species (Mollov et al. 2009; Mollov 2011). Many other stud-
richness is positively correlated with human popula- ies also document apparent adverse effects of urban-
tions, although their focus was primarily on agricul- ization on reptile abundance and species richness
tural landscapes associated with urban environments. (Table 1; Ackley et al. 2009; Banville and Bateman
Similarly, Barrett and Guyer (2008) found that un- 2012; Hunt et al. 2013; Sullivan et al. 2017), whereby
like amphibian species, reptile species significantly development beyond moderate levels leads to de-
increased in urban watersheds in western Georgia creased number of species and abundance for those
USA, likely because of changes in canopy cover. that remain (Germaine and Wakeling 2001).
Ackley et al. (2015b) have taken this one step further Modification of aquatic habitat in IN, USA, also
and looked at microhabitat differences in Phoenix, led to declines in both turtles and snakes from the
AZ, USA. The authors did find a negative impact of area (Minton 1968). Finally, by comparing wildlife
building cover, and also found that affluent areas databases of herpetofauna, researchers demonstrated
including patches of desert remnants still retained that reptiles are negatively impacted by urbanization
relatively high lizard diversity and abundance (Hamer and McDonnell 2008). While distribution

on 23 July 2018
Reptilian responses to urbanization 3
Table 1 Reptilian responses to urban features and general outcomes
General response Urban factor

measured Species measured Outcome Reference
(A) Abundance Green anole (A. carolinensis) Cats Cats ate a lot of lizards Loyd et al. (2013)
and diversity
Crested anole (A. cristatellus) Urbanization Decreased presence and Kolbe et al. (2016b)
abundance
Lesser Antillean iguana Urbanization Decreased abundance and local Knapp and Perez-
(I. delicatissima) extirpations, similar density Heydrich (2012)
Dunes sagebrush lizard Urbanization Decreased abundance Smolensky and
(S. arenicolus) Fitzgerald (2011)
Desert grassland Urbanization Decreased abundance coincided Audsley et al. (2006)
whiptail (Aspidoscelis with increased roadrunner
uniparens) and Lesser earless abundance
lizard (Holbrookia maculata)
Fence lizard (S. occidentalis) Urbanization More frequent tonic immobility Sparkman et al. (2018)
and lower sprint speeds;
Significantly shorter limbs in
females.
Common chuckwalla (S. ater) Urbanization Similar abundance Sullivan and Sullivan
(2008)
Common chuckwalla (S. ater) Urbanization Similar abundance Sullivan and Williams
(2010)
Northern watersnake Urbanization Altered habitat use and Pattishall and Cundall
(N. sipedon) abundance (2009)
Eastern long-necked turtle Urbanization dur- Increased abundance Roe et al. (2011)
(C. longicollis) ing dry period
Eastern long-necked turtle Urbanization Similar abundance Stokeld et al. (2014)
(C. longicollis)
Reptile species in southeastern Population density Increased species richness Moreno-Rueda and
Spain Pizarro (2007)
Reptile species in western Watershed Increased species richness Barrett
Georgia, USA development and Guyer (2008)
Reptile species in Oxford, UK Urbanization and Species richness decreased with Dickman (1987)
habitat increasing distance from per-
fragmentation manent water and increased
with patch size.
Reptile species in Australia Urbanization Vegetation remnant size corre- How and Dell (2000)
lated positively with species
number
Reptile species in South Bulgaria Urbanization Reptile species richness was Mollov et al. (2009)
highest in rural zone,
2nd highest was the urban
zone, and last was the subur-
ban zone.
Riparian reptile species Damming Decreased species richness and Hunt et al. (2013)
occupancy
Reptile species in Brisbane, Urbanization Landscape structure and local Garden et al. (2010)
Australia scale habitat were most im-
portant for species
assemblages
Lizard species in Phoenix, AZ, Socioeconomic Building cover negatively af- Ackley et al. (2015b)
USA status and land fected diversity
cover
Reptile species in Indianapolis, Altered Turtles disappeared and snakes Minton (1968)
IN, USA waterways decreased
(continued)

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Table 1 Continued

Reptile species in Melbourne, Urbanization Decreased presence Hamer and McDonnell
Australia (2009)
Snake species in NJ, USA Urbanization Species-dependent effects Zappalorti and Mitchell
(2008)
(B) Diet Coastal horned lizard Invasive ants Altered prey selection in areas Suarez et al. (2000)
(P. coronatum) invaded by non-native ants
Dugite (P. affinis) Urbanization Smaller in mass and less likely to Wolfe et al. (2017)
have food in stomach
(C) Behavior Side-blotched lizard (U. stans- Temperature Urban vegetation allowed for Ackley et al. (2015a)
buriana) and ornate tree lizard extended lizard activity
(U. ornatus)
Puerto Rican crested anole Predation Increased tail autonomy and Tyler et al. (2016)
(A. cristatellus) regrowth
Anoles (A. sagrei and Urbanization Increased body size, longer la- Chejanovski et al.
A. cristatellus) tency to feeding when offered (2017)
food, and lower overall re-
sponse rates
Anoles (A. cristatellus and Artifical Artificial substrates slowed run- Kolbe et al. (2016a)
A. stratulus) substrates ning speed but were still used
frequently
Brown anole (A. sagrei) Urbanization More tolerant to humans, less Lapiedra et al. (2017)
aggressive, and spent more
time exploring new habitat
Common wall lizard (P. muralis) Urbanization More asymmetric traits Lazic et al. (2015)
Aegean wall lizard (P. erhardii) Human built Switched foraging mode in new Donihue (2016)
structures environment
Dalmatian wall lizard Urbanization Similar risk-taking and neophobia De Meester et al.
(P. melisellensis) of foraging behavior (2018)
Delicate skink (L. delicata) Urbanization No differences in learning Kang et al. (2018)
metrics
Delicate skink (L. delicata) Urbanization Similar activity, exploratory, and Moule et al. (2016)
foraging behaviors
Garden skink (L. guichenoti) Urbanization Greater flight initiation distance, Prosser et al. (2006)
approach distance, and sprint
speed
Side-blotched lizard Human presence Shorter flight initiation Keehn and Feldman
(U. stansburiana) (2018)
South Indian rock agama Urbanization Better body condition, less di- Balakrishna et al.
(P. dorsalis) verse diet, and altered hunting (2016)
strategies
Peninsular rock agama Urbanization Shorter flight initiation distance Batabyal et al. (2017)
(P. dorsalis)
Gila monster (H. suspectum) Urbanization No difference in home range Kwiatkowski et al.
size and movement parame- (2008)
ters; Population sex ratio was
female-biased.
Blue-tongued skinks (Tiliqua spp.) Noise (decible Altered movement behavior Alarcon and Fabiola
frequency) (2016)
Sleepy lizard (T. rugosa) Human presence Increases stride frequency for up Kerr et al. (2004)
and handling to an hour
Liolaemus lizards Human presence Shorter approach distance Labra and Leonard
(1999)
(continued)

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Table 1 Continued

Snake species in TN, USA Urbanization and Higher fecal parasite counts Davis et al. (2012)
habitat
fragmentation
Australian freshwater turtle Urbanization and Less aestivation due to increased Rees et al. (2009)
(C. longicollis) drought water
(D) Physiology Eastern fence lizard Cadmium tire Acute mortality and altered Brasfield et al. (2004)
(S. undulatus) byproduct thyroid hormone
Ornate tree lizard (U. ornatus) Urbanization Lower baseline and stress-in- French et al. (2008)
duced CORT levels and al-
tered leukocyte counts
Side-blotched lizard Urbanization Higher CORT response, repro- Lucas and French
(U. stansburiana) ductive investment, and oxi- (2012)
dative stress; lower survival,
innate immunity, and
antioxidants
Anoles (A. sagrei and Temperature Higher urban temperatures ac- Tiatragul et al. (2017)
A. cristatellus) celerated development of
non-native anole embryos
Eurpoean wall lizard (P. muralis) Urbanization Increased parasite loads and re- Lazic et al. (2017)
duced body condition
Lesser Antillean iguana Urbanization No change in growth rate or Knapp and Perez-
(I. delicatissima) body condition; asymptotic Heydrich (2012)
body condition
Galapagos marine iguana Human develop- Higher oxidative stress, lower French et al. 2017)
(A. cristatus) ment and tour- immunity, and sex-dependent
ism (including responses in CORT and sex
urban) hormones
Common gartersnake (T. sirtalis) Indoxocarb Acute increase in CORT and Neuman-Lee et al.
pesticide immunity (2016)
Western terrestrial gartersnake Polybrominated Altered thyroid morphology and Neuman-Lee et al.
(T. elegans) diphenyl ethers increased body size of repro- (2015)
(PBDEs) flame ductive females and offspring
retardants
Copperhead (A. contortrix) Roads and traffic Reduced CORT response and no Owen et al. 2014)
difference in baseline CORT
Eastern long-necked turtle Urbanization dur- Similar reproductive output and Ferronato et al. (2017)
(C. longicollis) ing wet period growth rate
Eastern long-necked turtle Urbanization dur- Increased growth rate Roe et al. (2011)
(C. longicollis) ing dry period
Yellow-bellied slider (T. scripta Trace elements of Increased bactericidal ability and Haskins et al. (2017)
scripta) coal combus- no change in PHA response or
tion (cadmium, parasitism
copper, and
arsenic)
Painted turtle (C. picta) Roads and traffic No differences in baseline or Polich (2016)
stress-induced CORT levels
Painted turtle (C. picta) Roads and traffic No differences in baseline or Baxter-Gilbert et al.
stress-induced CORT levels (2014)
Common snapping turtles Mercury exposure Reduced hatching success Hopkins et al. (2013)
(C. serpentina)
(continued)

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Table 1 Continued

American Alligator Chemicals from Thyroid and sex steroid hor- Crain et al. (1998);
(A. mississippiensis) pristine and mone abnormalities in con- Guillette et al.
contaminated taminated lakes; Smaller (1999)
lakes phallus sizes
(E) Survival Common blue-tongued skink Domestic pets Increased injury and mortality Koenig et al. (2002)
(T. scincoides) and habitat loss with increased domestic pets
and habitat loss
Green anole (A. carolinensis) Interaction of Temperature and dose of pesti- Talent (2005)
temperature cide interact to affect
and pyrethrin mortality
pesticide
Texas horned lizard (P. cornutum) Urbanization Increased survival Endriss et al. (2007)
Texas horned Lizard Urbanization Decreased survival Wolf et al. (2013)
(P. cornutum)
Salt marsh snake (N. clarkii Herbicide Decreased survival Ackley and Meylan
compressicauda) (2010)
Spiny softshell turtle (A. spinifera) Urbanization Decreased survival Plummer and Mills
(2008)
Eastern long-necked turtle Urbanization dur- Similar abundance and survival Ferronato et al. (2017)
(C. longicollis) ing wet period
Semi-aquatic turtle species in Urbanization Species dependent survival Eskew et al. (2010)
NC, USA
Reptile species in the Urbanization and Species dependent extinctions Lowe (1985)
Southwestern USA altered riparian and declines
habitat
Lacertid lizard species in Poland Cats Cats killed more lizards in rural Krauze-Gryz et al.
areas (2017)
Skink species in Australia Habitat Increased bird predation on the Anderson and Burgin
fragmentation edge of fragmented remnants (2008)
Painted turtles (C. picta) and Roads Sex-dependent mortality on Steen and Gibbs
common snapping turtles roads changes population (2004); Steen et al.
(C. serpentine) structure to male biased (2006)
(F) Genetic Crested anole (A. cristatellus) Urbanization Phenotypic shifts Winchell et al. (2016)
responses
Common wall lizard (P. muralis) Urbanization Decreased gene flow Beninde et al. (2016)
West coast laterite ctenotus Urbanization Decreased gene flow, similar Krawiec et al. (2015)
(C. fallens) genetic diversity, and no ge-
netic differentiation
Florida sand skink (Plestiodon Urbanization Decreased gene flow and similar Richmond et al. (2009)
reynoldsi) genetic diversity
California legless lizard (Anniella Urbanization Similar genetic diversity Parham and Papenfuss
pulchra) (2009)
Reticulated velvet gecko Urbanization Increased genetic differentiation Hoehn et al. 2007)
(Hesperoedura reticulata) Tree
Dtella (Gehyra variegata)
Alameda striped racer (Coluber Urbanization Decreased gene flow Richmond et al. (2016)
lateralis euryxanthus)
Mexican dusky rattlesnake Urbanization Increased genetic differentiation Sunny et al. (2015)
(Crotalus triseriatus) and normal gene flow
Blanding’s turtle (Emydoidea Urbanization Decreased gene flow and ge- Rubin et al. (2001)
blandingii) netic diversity
(continued)

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Table 1 Continued

Ornate box turtle (Terrapene Urbanization Decreased gene flow, similar Cureton et al. (2014)
ornata) genetic diversity, and no ge-
netic differentiation
Tuatara (Sphenodon punctatus) Urbanization Increased genetic differentiation Moore et al. (2008)
Lizard species in Southern Urbanization Decreased gene flow, decreased Delaney et al. (2010)
California, USA genetic diversity, and increased
genetic differentiation
Lizard species in Southern Urbanization Decreased gene flow and similar Thomassen et al.
California, USA genetic diversity (2018)
Notes: An organized look at original research investigating reptilian responses to urban features organized by (A) abundance and diversity, (B)
diet, (C) behavior, (D) physiology, (E) survival, and (F) genetic. Within each subsection of the table, studies are ordered by taxonomic group and
then followed by multispecies studies.
studies are a critical first step in determining what intensity of exposure, including elevated stress reac-
species are most impacted, an important next step is tivity, oxidative stress, and suppressed immunity
to begin investigating specific factors within the ur- (French et al. 2010; 2017). Another study found
ban environment that may be influencing reptile spe- that lizards which have been observed, briefly han-
cies using a combination of field and controlled dled, or extensively handled all increased stride fre-
laboratory studies. quency following exposure to humans (Kerr et al.
2004). While allowing humans to get closer before
running away could be a result of habituation to
Biotic factors
human presence, increased stride frequency would
Human presence and invasive species suggest an increased cost of movement associated
In general, urbanization tends to decrease native spe- with human presence. While humans are the leading
cies richness but promotes diversity of exotic and/or factor altering environments for native species, the
non-native species (McKinney 2006; 2008). Because introduction of other invasive species can also alter
urbanization can promote the establishment of non- the landscape and ecology, having significant impli-
native and generalist species, there is the potential cations for native species.
for urbanization to influence species interactions There is evidence of increased predation for rep-
through the introduction of novel predators, prey, tiles in urbanized areas primarily by invasive species
and parasites. The number of invasive species is sig- and pets (Fischer et al. 2012). Household pets, such
nificantly increasing and thought to be one of the as domestic cats, are known to prey upon local
predominate risks for native species (Pimentel et al. fauna. For example, video monitoring of free-
2005). For example, the presence of native crested roaming cats in southeastern United States showed
anoles (Anolis cristatellus) is negatively associated that 33% of prey recovered from outdoor cats were
with the presence of a non-native competitor species, reptiles, specifically the green anoles (Anolis caroli-
brown anoles (Anolis sagrei). Here, brown anoles not nensis) (Loyd et al. 2013). Similarly, Koenig et al.
only reduced the abundance of crested anoles, but (2002) found that blue-tongued skinks (Tiliqua scin-
also caused a shift in their use of perches (Kolbe coides) were more likely to be attacked by household
et al. 2016b). pets in suburban areas compared to urban areas.
Humans are one of the predominant invasive spe- However, Krauze-Gryz et al. (2017) found that rep-
cies present in urban environments that have been tiles in Poland were more likely to be predated by
shown to alter reptilian behavior and movement pat- cats in rural areas. With native predators, skinks
terns. Lizards from areas of high human density have were more likely to be predated by birds on the
shorter approach distances before initiating flight edge of fragmented remnants compared to the core
compared to lizards from areas of low human den- (Anderson and Burgin 2008). Similarly, in southeast
sity (Labra and Leonard 1999). Marine iguanas close Arizona, terrestrial lizard abundance decreased in ur-
to towns come in more frequent contact with people ban areas along with an increase in roadrunners
including tourists in the Galapagos Islands and also abundance, a common natural predator (Audsley
show behavioral and physiological responses to et al. 2006), suggesting a causal link. These results

on 23 July 2018
provide evidence to suggest that urbanization gener- general ecology, including habitat size and fragmen-
ally increases chances of predation from both native tation, can also alter disease transmission in urban
and non-native predators. habitats (Riley et al. 2014b). For example, Davis
et al. (2012) found that more snakes had fecal para-
Diet sites near the outer edges of an urban forest com-
Urbanization can affect reptile diet composition and fre- pared to snakes near the core of the forest. Similarly,
quency of feeding by altering the availability of native food Lazic et al. (2017) found that wall lizards (Podarcis
sources and introducing non-native prey species muralis) had higher parasite loads and reduced body
(Table 1B), which, in some instances, can be beneficial. condition in urban areas compared to rural areas.
In the case of the threatened Lake Erie Water Snake These studies suggest that urbanization can poten-
(Nerodia sipedon insularum), the invasive round goby tially influence pathogen transmission among reptiles
(Neogobius melanostomus) is an important food source occupying previously natural habitat and adjacent
allowing for increased growth rates and body size which areas. However, more studies are needed to further
can reduce predation risk during vulnerable developmen- elucidate how urban cover influences transmission of
tal stages (King et al. 2006). Similarly, Balakrishna et al. parasites and susceptibility to reptile species.
(2016) found that Indian rock agamas (Psammophilus
dorsalis) in urban environments had better body condi-
Abiotic factors
tion, had a less diverse diet, and even altered their foraging
strategy compared to rural conspecifics. Temperature, light, and noise
Not all species perform better on urban diets or with Urbanization can alter abiotic features of an environ-
novel diet sources. For example, a study comparing diet ment, such as temperature, light, and noise, but the
of road-killed and museum-collected specimens direct impacts of these changes on animals is not
showed that dugites (Pseudonaja affinis) occupying ur- well understood. Temperature is a dominant ecolog-
ban areas in Australia were less likely to contain a meal ical variable for all animals that can be altered in
and were smaller in mass compared to their rural coun- urban environments. The majority of studies on
terparts (Wolfe et al. 2017). Suarez et al. (2000) found temperature changes in urban environments have fo-
that invasive Argentine ants (Linepithema humile) orig- cused on endothermic species. However, known
inating from urban areas displaced native ant species temperature changes in urban areas likely render
and significantly altered the diet composition for ectotherms even more susceptible to urbanization.
coastal horned lizard (Phrynosoma coronatum). Decreased shade cover from plants can cause reptiles
Furthermore, ontogenetic differences in diet suggest to be less active due to intense heat. Ackley et al.
the need for a diverse ant community to sustain pop- (2015a) demonstrated that irrigated and non-native
ulations, and raise concern that the documented decline shade planting increased lizard activity time in urban
in native ant species and diversity through displacement desert relative to native landscaping. Tiatragul et al.
by the Argentine ant could potentially affect survival (2017) found that urban temperatures not only ac-
and population persistence of many ant predator spe- celerated development of non-native anole embryos,
cies. Feeding behaviors may also differ for lizards in but that non-native embryos were robust and sur-
urban versus forested environments. Anolis lizards in vived well under urban temperatures. Temperature
urban environments of Puerto Rico have been observed also has the potential to exacerbate other environ-
to be larger and to have longer latency to feeding when mental stressors. For example, Talent (2005) found
offered food (Chejanovski et al. 2017). Some lizards that temperature influenced the sensitivity of lizards
have even switched foraging modes in response to hab- to pyrethrin pesticides. Similar to temperature, light
itat changes occurring with human presence. Aegean and photoperiod are critical for the timing of im-
wall lizards (Podarcis erhardii) which utilized rock walls portant life history events. Artificial light has also
were more sedentary, exhibited morphological changes, become a ubiquitous factor for most urban environ-
and ate less sedentary prey compared to non-wall liz- ments and while several studies have focused on
ards (Donihue 2016). birds (da Silva et al. 2014; Ouyang et al. 2017), the
studies for reptile species are largely inconclusive or
Parasites lacking (Perry et al. 2008).
Urbanization has the potential to influence immu- It has been suggested that no site in the continen-
nity and host–pathogen dynamics of urban-dwelling tal United States is free from anthropogenic noise
animals via the introduction of non-native parasites exposure, including remote protected areas such as
and pathogens along with other larger invasive spe- national parks (Barber et al. 2011). Several studies
cies (Martin et al. 2010). Furthermore, changes in have directly tested the effects of human noise on

on 23 July 2018
bird behavior and physiology (Rheindt 2003; and are less likely to aestivate because the water sup-
Swaddle and Page 2007; Francis et al. 2009; ply does not seasonally dry up in urban areas.
Slabbekoorn 2013; Davies et al. 2017) and male However, damming, which greatly alters riparian
tree frog (Hyla arborea) calling (Lengagne 2008) landscapes, reduces reptile occupancy and richness
but few other animals have been studied this exten- for many species, not only aquatic (Hunt et al.
sively. Alarcon and Fabiola (2016) tested different 2013). Perhaps most significantly, soil moisture in
decibels and frequencies on behavior in blue- all habitats is critical for the development of reptile
tongued skinks (T. scincoides) and found that loud, embryos of oviparous species, which constitutes the
especially high frequency, noises resulted in animals vast majority of reptile species (Ackerman 1991).
spending more time freezing, a typical stress re- Roads are a notable abiotic factor associated with
sponse in reptiles. urban environments that introduce changes in sub-
strate, noise, and disturbance rates, which may in
Substrates and roads themselves also be a direct source of mortality
Some abiotic urban features may actually be benefi- (Ashley and Robinson 1996; Jochimsen et al. 2004;
cial to animal inhabitants, by providing access to Andrews and Gibbons 2005; Andrews et al. 2008;
more diverse substrates (e.g., greater refuge and Andrews et al. 2015). A synthesis of studies investi-
perching options) and resources, allowing reptiles gating the impact of roads on reptile abundance
to persist under anthropogenic disturbances. demonstrates generally negative impacts, as does a
Evidence for this has emerged through early work meta-analysis of life history traits and population
on comparative habitat preferences across the ur- responses to roads (Fahrig and Rytwinski 2009;
ban–rural landscape. For example, northern water- Rytwinski and Fahrig 2012). Among snake species,
snakes (N. sipedon) occupying urbanized stream those of smaller sizes such as ring-necked snakes
areas exhibit significantly greater site fidelity than (Diadophis punctatus), southeastern crown snakes
those found in natural stream areas (Pattishall and (Tantilla coronata), and eastern hognose snakes
Cundall 2008). Snakes in natural areas selected hab- (Heterodon platirhinos) more often avoid the pres-
itat with wide riparian zones and dense canopy ence of roads and traffic (Andrews and Gibbons
cover, whereas snakes in urban areas more often oc- 2005; Andrews et al. 2008; Robson and Blouin-
cupied artificial substrates (e.g. piles of scrap metal, Demers 2013). However, larger species such as gar-
concrete, or holes in a railroad bed adjacent to tersnakes (Thamnophis sirtalis parietalis), coachwhips
streams) and areas with high human density (Masticophis flagellum), and brown tree snakes
(Pattishall and Cundall 2009). Artificial structures (Boiga irregularis) can exhibit alternative movement
(e.g. broader and smoother substrates) are exten- activities and pathways to avoid exposure and re-
sively utilized for perching and refuge among lizard main in natural habitats (Shine et al. 2004;
species such as garden skinks (Lampropholis guiche- Mitrovich et al. 2009; Siers et al. 2014). Similarly,
noti), blue-tongued skinks (T. scincoides), crested turtle species including common snapping turtles
anoles (A. cristatellus), and Gila monsters and eastern painted turtles (Chrysemys picta picta)
(Heloderma suspectum) (Koenig et al. 2001; Prosser disperse into urbanized habitat less often than natu-
et al. 2006; Winchell et al. 2016), whereas other spe- ral habitat, as they also exhibit avoidance behaviors
cies such as barred anoles (Anolis stratulus) tend to toward areas with higher densities of roads (Patrick
use more natural aspects of the urban environment and Gibbs 2010). However, some species (Chrysemys
(i.e., trees and other cultivated vegetation; (Winchell picta and Chelydra serpentine) show sex-dependent
et al. 2018)). Artificial substrates also tend to be differences in road mortality so much so that there
smoother than natural substrates for arboreal species are changes in population structure (Steen and Gibbs
which can impact running velocity as was demon- 2004). The sex-biased effect of roads seems to be
strated in two species of Anolis lizards (Kolbe et al. driven by females nesting migrations that make
2016a). This may in part explain why lizards display them more likely to cross roads and be killed
differing flight initiation distances, escape strategies, (Steen et al. 2006).
and performance levels from rural counterparts Lizard species including blue-tongued skinks
(Koenig et al. 2001; Prosser et al. 2006; Aviles- (T. scincoides), western fence lizards (Sceloporus occi-
Rodriguez 2015; Winchell et al. 2016). dentalis), orange-throated whiptails (Aspidoscelis
As would be expected, urban changes in hydrology hyperythra), and dunes sagebrush lizards (Sceloporus
most significantly impact aquatic or riparian species, arenicolus) have been found to actively avoid cross-
especially turtles. Rees et al. (2009) found that ing roads and instead utilize vegetation and other
Australian freshwater turtles alter their behavior natural substrates for movement (Koenig et al. 2001;

on 23 July 2018
Brehme et al. 2013; Hibbitts et al. 2017). While the footprint itself. American alligators (Alligator missis-
risk of mortality is reduced by road and traffic avoid- sippiensis) from lakes contaminated with municipal
ance, changes in movement patterns and spatial and agricultural runoff show altered thyroid and sex
distributions can contribute to genetic isolation and steroid hormone levels and smaller phalluses (Crain
population sinks for reptiles (Forman and Alexander et al. 1998; Guillette et al. 1999). Western pond tur-
1998; Shepard et al. 2008). However, the field of road tles (Emys marmorata) from protected areas in
ecology is growing and working to provide new plan- California still show signs of both current- and
ning strategies to mitigate the impacts on animals historic-use pesticides in their blood (Meyer et al.
(Langen et al. 2012; Riley et al. 2014a). 2016). Turtles in southwest VA, USA also show ev-
idence of higher blood mercury levels when sampled
Pollution at contaminated sites and depending on their feeding
In many urban landscapes and adjacent developed strategy (Bergeron et al. 2007). In common snapping
areas, environmental toxin levels and air particulates turtles (C. serpentina), mercury levels were associated
are higher than surrounding rural areas (Cohen et al. with reduced hatching success (Hopkins et al. 2013).
2004; Wei and Yang 2010). The few studies that test This contamination in aquatic settings can also pass
ecotoxicological outcomes of urban pollutants in to species that prey upon aquatic animals, as ob-
reptiles demonstrate that the effects are not necessar- served in a viperine snake (Natrix maura) that preys
ily harmful. For example, yellow-bellied sliders on fish in France and has high mercury levels as a
(Trachemys scripta scripta) accumulate trace elements result (Lemaire et al. 2018). Yet, the overall evidence
from coal combustion such as cadmium, copper, and as to the effects of urban and anthropogenic pollu-
arsenic as they grow, but these elements do not seem tants on reptiles is limited and more research is
to adversely impact their immune systems measured needed (Croteau et al. 2008). In particular, research-
via parasitism and responses to phytohemagglutinin, ers suggest that major ecotoxicological gaps for rep-
although bacterial killing ability was elevated in tur- tiles include better understanding the magnitude and
tles from contaminated sites (Haskins et al. 2017). In mechanism of contaminant exposure (Weir et al.
gartersnakes (T. sirtalis), exposure to the pesticide 2010; Riley et al. 2014b).
indoxocarb induced an acute stress increase in cor-
ticosterone and immunity, whereas exposure to a Directionality of responses
similar natural toxin to which the gartersnakes
Individual responses
have evolved resistance (i.e., tetrodoxin) did not in-
duce a physiological response (Neuman-Lee et al. In order to estimate the impact of urbanization on
2016). Moreover, exposure to polybrominated reptiles, understanding the directionality of how dif-
diphenyl ethers (PBDEs) which are used as flame ferent species respond to the stressors of environ-
retardants and are persistent contaminants found mental change is pivotal. Measuring individual level
in practically every environment and organism responses can effectively provide real-time informa-
tested, resulted in altered thyroid follicular height tion concerning organismal viability in a particular
in female gartersnakes (Thamnophis elegans), suggest- environment, whereas population-level censuses may
ing thyroid dysfunction (Neuman-Lee et al. 2015). require long periods of time to yield insight. A large
Neuman-Lee et al. (2017) also found an increase in body of work has amassed in assessing individual
body size of pregnant female gartersnakes exposed to responses to urbanization across several taxa, yet
PBDEs as well as their resulting offspring. Brasfield few studies thus far have included reptiles.
et al. (2004) demonstrated that exposure to cad- Emerging findings suggest the impact of anthropo-
mium, a byproduct of tire ware that is likely high genic disturbance likely depends on habitat require-
in urban settings, could result in acute mortality and ments and life history, whereby directionality for
thyroid dysfunction in developing Eastern fence liz- individual responses is either relatively consistent
ards (Sceloporus undulatus). Talent (2005) demon- or species-specific.
strated that temperature influenced the sensitivity
of green anoles to pyrethrin pesticides. Given that Behavior and morphology
urbanization is known to alter ambient temperature One of the main mechanisms through which animals
and there are more pesticides in use in human- respond to changing environmental conditions is by
altered landscapes, this has important implications adjusting modes of behavior (Reale et al. 2007;
for urban reptiles. Miranda et al. 2013; Sol et al. 2013). Differences in
It is important to note that the effects of urban behavioral traits among urban and rural environ-
pollution can be wider reaching that just the urban ments can either result from individual behavioral

on 23 July 2018
plasticity or microevolutionary changes (Miranda Greenberg and Holekamp 2017). Directionality of

et al. 2013). Whether behavioral responses to urban- temperament shifts to urbanization may thus depend
ization rely on acclimation or adaptation in reptiles on whether anthropogenic conditions are beneficial,
remains largely undetermined (Kang et al. 2018). innocuous, or detrimental to the habitat require-
Regardless, the directionality of behavioral responses ments of a given reptile species.
to urbanization may be associated with life history Assessments of habitat selection and use have
strategies most appropriate for coping with changing yielded preliminary evidence of how urban environ-
environmental conditions (Huey et al. 2003; Sol and ments may meet the habitat requirements of some
Maspons 2016; Sol et al. 2018). Across avian and species, but may fail to do so for others (also see
mammalian taxa, urban and rural conspecifics gen- “Substrates and Roads” section above). For example,
erally vary in temperament, whereby behaviors in- in the same urban environment, the barred anole (A.
volving neophobia or neophilia, exploration, stratulus) utilizes more natural habitat compared to
aggression, and risk perception tend to differ the crested anole (A. cristatellus), which utilizes more
(Miranda et al. 2013; Sol et al. 2013). Behavioral anthropogenic structures (Winchell et al. 2018).
comparisons of urban and rural reptiles have so far Additional work has demonstrated that urban
been limited, but relatively consistent patterns of crested anoles jump from perch to perch less than
temperament shifts may be applicable to reptile spe- rural conspecifics, which instead move around more
cies with similar habitat requirements and life histo- frequently on a given perch (Aviles-Rodriguez 2015).
ries (Table 1C). Such preferences likely depend on the degree of sim-
Of critical importance is understanding whether ilarity in environmental conditions between both
behavioral adjustments are occurring within a species habitat types as this is predicted to determine the
and if such changes are beneficial in terms of sur- magnitude of selective pressures for behavioral dif-
vival and reproduction. Emerging studies suggest ferences that may be associated with urbanization.
that at least some reptiles are more tolerant of par- Lastly, it is important to consider that some of
ticular anthropogenic factors. For example, brown these behavioral changes may be the result of mor-
anoles (A. sagrei) and crested anoles (A. cristatellus) phological shifts in response to urbanization, espe-
from urban areas exhibit prolonged exploratory and cially in species with short generation times. A recent
foraging behaviors of new environments, as well as study on the effects of urbanization on antipredator
decreased risk perception and response rates towards behaviors of fence lizards found urban environments
predator and to human presence (Chejanovski et al. to be associated with shorter limbs, lowered sprint
2017; Lapiedra et al. 2017). Increased tolerance to speed, and more frequent tonic immobility
urbanization is also evident in Indian rock agamas (Sparkman et al. 2018). Interestingly, certain aspects
(P. dorsalis) and side-blotched lizards (Uta stansburi- of morphology have been found to be overall smaller
ana) which exhibit decreased flight initiation distan- (e.g., head size) and more asymmetric in urban com-
ces or risk perception to anthropogenic stimuli mon wall lizards, suggesting divergent size–shape
(Batabyal et al. 2017; Keehn and Feldman 2018). allometries from those in rural environments (Lazic
However, Prosser et al. (2006) found that urban gar- et al. 2013; 2015). However, other morphological
den skinks (L. guichenoti) instead flee at a greater components have been found to be larger, including
approach distance and exhibit greater sprint speed limb length in urban agamid lizards (Lophognathus
than conspecifics from natural habitats. Meanwhile, temporalis) and crested anoles, and greater subdigital
other studies yielded no behavioral response to ur- lamellae (i.e., footpad scales) in urban crested anoles
banization including movement, exploratory, and (Iglesias et al. 2012; Winchell et al. 2016). Urban
foraging behaviors of delicate skinks (Lampropholis brown anoles and crested anoles both tend to exhibit
delicata) in the Sydney region (Moule et al. 2016). greater body sizes (i.e., snout-vent lengths and
Overall activity of Gila monsters (H. suspectum) did masses) and body condition than those in natural
not differ among rural and urban areas (Kwiatkowski environments (Chejanovski et al. 2017; Hall and
et al. 2008). Similarly, risk-taking and neophobia Warner 2017). Yet others find no difference in
of foraging behavior was not affected by urbanization body condition or growth rates, such as the lesser
in Dalmatian wall lizards (Podarcis melisellensis). Antillean iguanas (Iguana delicatissima) (Knapp and
Collectively, these findings are relatively in line with Perez-Heydrich 2012). Finally, Tyler et al. (2016)
avian and mammal species that exhibit temperaments found greater rates of tail autonomy and regrowth
with more neophilic, exploratory, aggressive, and in urban anoles than their rural counterparts. In the
risk-taking behaviors in urban areas than in rural case of all of these morphological changes, there is
areas (Miranda et al. 2013; Sol et al. 2013; the potential for downstream effects on behavior or

on 23 July 2018
locomotion, and for the animal to incur inherent (bacterial killing ability) and higher reproductive in-
costs. vestment relative to rural side-blotched lizards.
Laboratory studies on these same urban lizards dem-
Physiology onstrated that there is direct competition for protein
Just as with behavioral research, studies investigating resources between the eggs and immunity in repro-
physiological responses to urbanization also yield ductive females (Durso and French 2018), and that
mixed results (Table 1D). One common metric uti- immune-challenged lizards alter their energetic strat-
lized across studies is the endocrine stress response egy by down-regulating metabolism (Smith et al.
involving activation of the hypothalamic–pituitary– 2017). Taken together these results suggest urbaniza-
adrenal axis (Saplosky 1992) and ultimately the re- tion may be causing a life history shift in investment
lease of glucocorticoids (i.e., corticosterone in the from self-maintenance to reproduction, a viable
case of reptiles; CORT) (Moore and Jessop 2003). strategy in a short-lived reptile (Smith and French
As compared to reptiles occurring in natural habitat, 2017).
those residing in urbanized areas have been found to Finally, in this context, the degree to which phe-
exhibit either similar or contrasting levels of baseline notypic plasticity, genetic evolution, or a combina-
stress and stress reactivity. When considering stress tion thereof may underlie differences in physiology,
physiology in snakes, no difference in baseline levels behavior, and morphology among populations across
of CORT is evident in copperheads (Agkistrodon con- the urban–rural landscape remains unclear.
tortrix) residing in forests compared to urbanized Regardless, significant changes in physiology, behav-
habitat (i.e., road development and traffic) (Owen ior, and morphology in urban reptiles should yield
et al. 2014). Similarly, northwestern garter snakes the potential to induce long-lasting effects on popu-
(Thamnophis ordinoides) generally do not exhibit lation size and performance over time.
blood heterophil-lymphocyte ratios, indicative of
chronic stress, in urbanized habitat (i.e., increased
human and predator presence) (Bell 2013). Further, Population responses
urban snakes, such as copperheads, exhibit reduced Although aspects of urbanization are known to place
stress-induced CORT levels compared to forest con- reptile populations directly at risk, whether individ-
specifics (Owen et al. 2014). However, copperheads ual responses result in additional threats to popula-
in urbanized areas demonstrate a negative associa- tion viability is largely undetermined. Changes in
tion between anthropogenic activity and baseline, individual physiology and behavior in response to
stress-induced, and magnitude of CORT response urbanization can affect survival and reproduction,
(Owen et al. 2014). Similar trends are evident in and thus ultimately affect populations. Linking phys-
turtles, as no differences in baseline or stress- iological and behavioral measures to demographic
induced CORT levels were found in painted turtles parameters may elucidate undetected effects of ur-
exposed to urban features (i.e., road development banization, yet few studies have pursued such
and traffic) as compared to those in natural areas endeavors (e.g., Lucas and French 2012). Of upmost
(Baxter-Gilbert et al. 2014; Polich 2016). concern thus far has been the abundance of reptile
Stress physiology in lizard species, however, exhib- populations, as individual survival and reproduction
its dissimilarities in response to urbanized areas. For often vary with respect to biotic and abiotic factors
example, tree lizards (Urosaurus ornatus) inhabiting of the urban-rural landscape (Table 1A, 1E).
Phoenix, AZ, USA have lower baseline and stress- Anthropogenic impacts generally appear to have
induced levels of corticosterone than their rural neutral effects, and in some cases, positive effects
counterparts, suggesting they have habituated to ur- on the population dynamics of semi-aquatic reptiles,
ban living (French et al. 2008). These same animals although detrimental effects may arise under severe
also show evidence of elevated immunity (i.e., higher cases of habitat disturbance. Despite close proxim-
leukocyte counts) perhaps to deal with increased in- ities to anthropogenic activity, abundances of north-
cidence of wounding in the city (2008). However, ern water snake populations were similar to those in
side-blotched lizards (U. stansburiana), a not too rural environments (Pattishall and Cundall 2009).
distant relative of the tree lizard, show differential Such findings are thought to be due to variable ref-
responses to city life in Saint George, UT, USA. uge and thermal opportunities provided by both ter-
Lucas and French (2012) found both increased cor- restrial and aquatic features of the urban
ticosterone response to a stressor and elevated oxi- environment. Greater complexity and stability in ur-
dative stress in urban side-blotched lizards. However, ban habitats may also explain how eastern long-
these same urban animals also have lower immunity necked turtles (Chelodina longicollis) maintain and

on 23 July 2018
even increase survival, reproductive output, and differences in the selective pressures of an environ-
population abundance in spite of temporal fluctua- ment and the resulting physiological and population-
tions in environmental conditions (Roe et al. 2011; level changes could potentially lead to genetic
Stokeld et al. 2014; Ferronato et al. 2017). This seems differentiation.
to be congruent with high survival estimates for other
turtles, such as yellowbelly sliders, common snapping Genetic
turtles, and spiny softshell turtles (A. spinifera), al- Urbanization may have genetic consequences among
though eastern mud turtles (Kinosternon subrubrum) reptile populations, as land-use changes can lead to
tend to exhibit lower survival estimates (Eskew et al. intense forms of habitat alteration (Table 1F).
2010; Plummer and Mills 2008). Populations of man- Herpetofauna that are particularly sensitive to habi-
grove salt marsh snakes (Nerodia clarkii compressi- tat degradation can rapidly become extirpated from
cauda) in St. Petersburg, FL, USA were also higher urban locales (Gibbon et al. 2000; Cushman 2006;
in abundance in anthropogenic habitats until their Hamer and McDonnell 2009). For those that persist
decline after severe disturbance (Ackley and Meylan across fragmented urban landscapes, connectivity
2010). Interestingly terrestrial and aquatic populations and gene flow between populations may be hindered
tend to differ in their responses. or inhibited, which can ultimately lead to reductions
Populations of terrestrial reptiles instead seem to in genetic diversity, inbreeding depression, and even
be more variable in their sensitivity to anthropogenic local extinction (Reed et al. 2002; Reed et al. 2003;
perturbations compared to semi-aquatic species. This Reed 2004; Cushman 2006; Frankham 2006).
may be due to relative differences in the urban mod- Degraded and fragmented habitats are also less likely
ifications of aquatic versus terrestrial habitats (e.g., to be recolonized by extinguished species.
varying facets, intensities, and frequencies) or differ- Additionally, the loss of genetic diversity in remain-
ences in survey methods and species detection rates. ing populations can reduce adaptive potential in re-
For example, population abundance is often related sponse to environmental changes.
to the degree of fragmentation, size, and quality of Although there are population and behavioral
habitat. However, different species have particular studies to document thriving and mobile urban rep-
ecological requirements in habitats that determine tiles species, preliminary genetic data provides little
the directionality of response. Urban disturbance in evidence of continuous gene flow for various reptile
the form of increasingly fragmented landscapes often species located along fragmented urban landscapes
causes fast declines and local extirpations in reptile (e.g., Delaney et al. 2010; Krawiec et al. 2015;
populations, such as in the lesser Antillean iguana (I. Beninde et al. 2016; Richmond et al. 2016;
delicatissima) (Knapp and Perez-Heydrich 2012). In Thomassen et al. 2018). Inhibited or decreased
the case of Texas horned lizards (Phrynosoma cornu- gene flow, in turn, seems to either reduce genetic
tum) in central Oklahoma, urban development diversity levels (Rubin et al. 2001; Delaney et al.
caused declines in the abundance due to increased 2010) or yield no effect (Parham and Papenfuss
mortality despite moderate reproductive output 2009; Richmond et al. 2009; Cureton et al. 2014;
(Endriss et al. 2007; Wolf et al. 2013). Populations Krawiec et al. 2015; Sunny et al. 2015). There are
of dunes sagebrush lizards vary significantly in abun- often remarkable amounts of genetic divergence of
dance and this variation could be explained by hab- populations across the urban–rural landscape, which
itat patch size and quality, which are affected by may be occurring over relatively short geographic
human development, oil, and gas industry and temporal scales (Hoehn et al. 2007; Moore
(Smolensky and Fitzgerald 2011). Similarly, declines et al. 2008; Delaney et al. 2010; Sunny et al. 2015).
in population abundance for the invasive crested Implications for population genetics may thus de-
anole (A. cristatellus) in Miami, FL, USA are strongly pend on the size, configuration, age, and isolation
associated with losses in habitat size and quality of habitat fragments. Studies are revealing evidence
(Kolbe et al. 2016b). In other urban habitats with of selection for divergent phenotypes and suggest a
limited refuge and plant food density, population potential for reptile populations to adapt to urban
abundance of common chuckwallas (Sauromalus environments (Winchell et al. 2016; 2018).
ater) is dependent on the availability of plant food
diversity (Sullivan and Sullivan 2008; Sullivan and
Williams 2010). Collectively, these studies suggest Conclusions
that urbanization can lead to population level Overall, this review has identified complex and di-
changes but that some species, and perhaps environ- verse results that are variable both within and among
ments, are more sensitive. Over multiple generations, all scales of ecological organization. There is

on 23 July 2018
variability in the directionality of the responses to MWJ, editors. Egg incubation: its effects on embryonic de-
urbanization, whereby some studies find inert or velopment in birds and reptiles. Cambridge, UK:
even positive effects of urbanization, while others Cambridge University Press. p. 193–211.
Ackley J, Muelleman P, Carter R, Henderson R, Powell R.
show the opposite. This discrepancy is due in part
2009. A rapid assessment of herpetofaunal diversity in vari-
to the heterogeneity of urban landscapes and to the ously altered habitats on Dominica. Appl Herpetol 6:171–84.
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important factor leading to inconsistencies in study 2015a. Urban heat island mitigation strategies and lizard
outcomes is that urbanization includes many differ- thermal ecology: landscaping can quadruple potential ac-
ent factors interacting simultaneously. While there tivity time in an arid city. Urban Ecosyst 18:1447–59.
are a handful of studies testing the interactive effects Ackley JW, Meylan PA. 2010. Watersnake Eden: use of storm-
water retention ponds by mangrove salt marsh snakes
of urban qualities, most are focused on non-reptile
(Nerodia clarkii compressicauda) in urban Florida.
taxonomic groups (Isaksson 2015). With a growing Herpetol Conserv Biol 5:17–22.
body of studies investigating specific urban features Ackley JW, Wu J, Angilletta MJ, Myint SW, Sullivan B.
or stressors, it is becoming increasingly important to 2015b. Rich lizards: how affluence and land cover influence
measure interactive effects (Talent 2005), physiolog- the diversity and abundance of desert reptiles persisting in
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misleading results due to tradeoffs which can occur on the behaviour, physiological traits and welfare of two
animal models: wild mice (Mus musculus) and Eastern
between physiological systems (Lucas and French
blue tongued lizard (Tiliqua scincoides) [Thesis]: The
2012). Also, the large number of different University of Queensland.
approaches used in these studies make it difficult Allen WL, Street SE, Capellini I. 2017. Fast life history traits
to compare outcomes and to assess directionality promote invasion success in amphibians and reptiles. Ecol
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north-western Sydney, Australia. Landscape Ecol
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given effect. Andrews KM, Gibbons JW. 2005. How do highways influence
To conclude, based on our findings there is an snake movement? Behavioral responses to roads and
apparent lack of urban research in reptilian species vehicles. Copeia 2005:772–82.
(1) investigating interactive or additive urban factors Andrews KM, Gibbons JW, Jochimsen DM, Mitchell J. 2008.
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reptiles and other wildlife on the Long Point Causeway,
the near future as urbanization and animal popula-
Lake Erie, Ontario. Can Field Nat 110:403–12.
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need for better community outreach, involvement, Lizard abundance in an exurban Southwestern savanna,
and education to make conservation of all species and the possible importance of Roadrunner predation.
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Aviles-Rodriguez K. 2015. Do urban environments influence
Funding antipredator and foraging behavior of the lizard Anolis
cristatellus? [ProQuest Dissertations Publishing]:
This work was supported by the National Science University of Rhode Island.
Foundation [(IOS)-1350070 to S.S.F.]. Balakrishna S, Batabyal A, Thaker M. 2016. Dining in the
city: dietary shifts in Indian rock agamas across an
urban–rural landscape. J Herpetol 50:423–8.
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Town and Country Reptiles: A Review of Reptilian Responses to Urbanization

Article in Integrative and Comparative Biology · June 2018

Susannah French Alison C. Webb

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Spencer Hudson Emily E. Virgin

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Physiological ecology of Side-blotched Lizards View project

Amphibian Salt Tolerance and Adaptation View project

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Town and Country Reptiles: A Review of Reptilian

Overview areas (e.g., passerines in different cities across the

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Table 1 Reptilian responses to urban features and general outcomes

General response Urban factor

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General response Urban factor

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General response Urban factor

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General response Urban factor

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General response Urban factor

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plasticity or microevolutionary changes (Miranda Greenberg and Holekamp 2017). Directionality of

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