Thermal ecology and activity patterns of six species of tropical night lizards (Squamata: Xantusiidae: Lepidophyma) from Mexico

doi:10.1016/j.jtherbio.2018.06.001

Journal of Thermal Biology

Volume 75, July 2018, Pages 97-105

https://doi.org/10.1016/j.jtherbio.2018.06.001 Get rights and content

Highlights

•
First records of different thermal parameters (T_b, T_set, CT_min and CT_max) of some lizards of the genus Lepidophyma.
•
Evaluation of thermoregulatory strategies, as well as thermal qualities of the environment, of the species.
•
Formulation of a hypothesis linking thermal quality of the environment and daily activity period in Lepidophyma.
•
Facultative shift to diurnality in species from thermally homogenous environments.
•
Thermally imposed diurnality in the high elevation species, L. gaigeae.

Abstract

Activity patterns in ectotherms rely on the structure of the thermal environment and thermoregulatory opportunities during activity periods. A dichotomy between diurnal and nocturnal ectotherms is not clear in every case, and temperature can directly affect the daily activity period in these organisms during both photophase and scotophase. In the present study we evaluate the thermal ecology of six tropical night lizards (genus Lepidophyma) from Mexico. Our results indicate a thermoconformer strategy in most of the studied species. In these species, thermal tolerances are associated with environmental temperatures to which they are exposed. Furthermore, thermal quality of the environment directly determines the daily activity period. Therefore, we argue that diurnal activity in Lepidophyma species is determined by local thermal conditions.

Introduction

Due to the thermal dependence of physiological processes and the need for external heat sources, ectotherms must behaviorally regulate their body temperature (T_b) near or within the range of preferred (selected) temperatures (T_set) to carry out their daily biological activities optimally (Kaufmann and Bennett, 1989, Autumn and Denardo, 1995, Autumn et al., 1999). To maintain T_b within these intervals, ectotherms can use both physiological and behavioral mechanisms (Shine and Kearney, 2001; Gvoždík, 2002; Lara-Resendiz et al., 2013; Clusella-Trullas and Chown, 2014). Despite this, the thermal environment imposes spatial and temporal limitations that determine how the activity patterns of these organisms vary at both local and macrogeographic scales.

Activity periods in ectotherms use to be related to thermal quality of the environment (Mautz and Case, 1974, Gvoždík, 2002, García-De la Peña et al., 2007). Nocturnal species rely mainly on night temperatures to attain a T_b near T_set. If they cannot reach T_set at night (scotophase), however, they might compensate by means of daytime (photophase) behaviors and physiological processes, such as maintaining T_b close to the T_set within their shelters or selecting refuges with more suitable thermal qualities for passive physiological processes (e.g. digestion). This strategy has been found mainly in environments where thermal regimes at night are lower than T_set (Mautz and Case, 1974; Angilletta and Werner, 1998; Kearney and Predavec, 2000; Aguilar and Cruz, 2010).

The above explanation does not seem to apply generally in all cases, however, and the mechanisms used to compensate for suboptimal temperatures at night are not at all clear for most nocturnal taxa (Autumn et al., 1999, Kearney and Predavec, 2000, Hitchcock and McBrayer, 2006). Moreover, in thermally homogenous environments, such as tropical rain forests, nocturnal ectotherms do not need to thermoregulate during photophase, since their thermal requirements usually coincide with environmental temperatures during scotophase (Angilletta and Werner, 1998; Huey et al., 2009; Muñoz and Losos, 2018).

The genus Lepidophyma comprises 19 currently recognized species and represents the largest group in the family Xantusiidae (Savage, 1964; Noonan et al., 2013). Its members are distributed from Nuevo León, in northeastern Mexico, and Michoacán, in the west, to Panama, but its populations are most often highly isolated from each other (Bezy and Camarillo, 2002). Species of this family are commonly called “tropical night lizards”, as they mainly inhabit thermally homogenous tropical habitats and generally have been observed active at night (Mautz and Lopez-Foment, 1978; Bezy and Camarillo, 2002). Nevertheless, there are also species associated with thermally heterogeneous environments, such as temperate forests or xeric habitats, where the thermal quality at night can be low; in such circumstances, these lizards must use strategies to compensate for suboptimal night temperatures (Mautz, 1979, Bezy and Camarillo, 2002). The variety of occupied vegetation types, as well as their varied daily activity patterns, make the species of the genus Lepidophyma an appropriate model system to examine thermoregulatory strategies that tropical ectotherms can use in both thermally stable and fluctuating environments. Therefore, the aim of this work was to document the thermal ecology of six species of Lepidophyma inhabiting different environments, in addition to determining their thermoregulatory strategies, and to explore the relationship between their activity period and thermal quality of the environment.

Section snippets

Study organisms and sites

During the rainy season (June–October) 2015–2016, we collected lizards during daytime (photophase, 0900–1800 h) and nighttime (scotophase, 1900–0400 h) during 10 days in six localities in Mexico, including one population at the northern latitudinal limit of the genus and another near the upper elevational limit (Bezy and Camarillo, 2002):

1)
Lepidophyma flavimaculatum Duméril, 1859 is found in tropical rainforest and tropical deciduous forest from Veracruz and Oaxaca, Mexico, to Panama, at 0–750 m

Results

We collected a total of 171 individuals: 16 L. flavimaculatum from Tenosique, Tabasco, and 14 from the Parque Nacional Palenque, Chiapas; 30 L. gaigeae; 33 L. pajapanense; 13 L. smithii; 25 L. sylvaticum, and 40 L. tuxtlae. Thermal parameters obtained from all species are summarized in Table 1.

Species associated with tropical forests presented a primarily nocturnal activity pattern, whereas L. gaigeae, which inhabits a temperate forest, and L. sylvaticum, associated with riparian vegetation in

Discussion

Although in some lizards body and selected temperatures tend to be similar in phylogenetically related species (Huey and Bennett, 1987, Grigg and Buckley, 2013, Clusella-Trullas and Chown, 2014), the observed differences in thermal parameters (T_b, T_set, CT_min and CT_max) among some of the species studied seem to be given due to thermal conditions of the habitat and, in the case of T_b, to different patterns of heat transfer (conduction vs. convection). However, some of these parameters, such as T_b

Acknowledgments

This research was funded by the “Cátedra José Sarukhán Kermez”, awarded to DMAM, by the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT; IN 210116) and by the Centro del Cambio Global y la Sustentabilidad en el Sureste A.C. DMAM, RSB and FJMN were funded by CONACYT posgraduate scolarships (CVU 412744, 774550 and 775920, respectively). DMAM, RSB and FJMN thank to Posgrado en Ciencias Biológicas de la Universidad Nacional Autónoma de México. This article is a

Author contributions

DMAM posed and designed the research and experiments. DMAM, RSB and FJMN collected and analyzed the field and laboratory data. All authors contributed with the interpretation of the results and the redaction of the manuscript.

Interests statement

No author declares conflict of interests.

Diego Miguel-Arenas Moreno: (July 1st, 1985, Mexico City) is a Ph.D. student of the Posgrado en Ciencias Biológicas at the Universidad Nacional Autónoma de México (UNAM). He has been working on the thermal ecology of night lizards (Xantusiidae), and some species of horned lizards, geckos, spiny lizards and anoles. His main topics of interest are the relationship between the thermal quality of the environment and activity time of lizards, as well as the effects of the climate change. He has

References (52)

E.M. Dzialowski
Use of operative temperature and standard operative temperature models in thermal biology
J. Therm. Biol.
(2005)
B.P. Noonan et al.
Phylogenetic relationships within the lizard clade Xantusiidae: using trees and divergence times to address evolutionary questions at multiple levels
Mol. Phylogenet. Evol.
(2013)
S. Valenzuela-Ceballos et al.
Variation in the thermal ecology of an endemic iguana from Mexico reduces its vulnerability to global warming
J. Therm. Biol.
(2015)
R. Aguilar et al.
Refuge use in a patagonian nocturnal lizard, Homonota darwini: the role of temperature
J. Herpetol.
(2010)
M.J. Angilletta et al.
Australian geckos do not display diel variation in thermoregulatory behavior
Copeia
(1998)
K. Autumn et al.
Behavioral thermoregulation increases growth-rate in a nocturnal lizard
J. Herpetol.
(1995)
K. Autumn et al.
Locomotor performance at low temperature and the evolution of nocturnality in geckos
Evolution
(1999)
R.L. Bezy et al.
Systematics of xantusid lizards of the genus Lepidophyma
Contrib. Sci.
(2002)
G. Blouin-Demers et al.
Thermal ecology of black rat snakes (Elaphe obsoleta) in a thermally challenging environment
Ecology
(2001)
B.H. Brattstrom
Body temperatures of reptiles
Am. Midl. Nat.
(1965)

G.A. Brusch et al.

Turn up the heat: thermal tolerances of lizards at La Selva, Costa Rica

Oecologia

(2016)

L. Canseco-Márquez et al.

New herpetofaunal records for the state of Oaxaca, Mexico

Mesoam. Herpetol.

(2015)

S. Clusella-Trullas et al.

Lizard thermal trait variation at multiple scales: a review

J. Comp. Physiol. B

(2014)

C. Dytham

Choosing and Using Statistics: A Biologist’s Guide

Third ed.

(2011)

A.R. Estrada et al.

Apuntes ecológicos sobre Cricosaura typica (Sauria: Xantusiidae) de Cuba

Caribb. J. Sci.

(1998)

S.E. Fick et al.

Worldclim 2: New 1-km spatial resolution climate surfaces for global land areas

Int. J. Clim.

(2017)

L.I. Florentino-Melchor

Ecología térmica de la lagartija microendémica Anolis gadovii (Sauria: dactyloidae)

(2015)

C. García-De la Peña et al.

Ciclos de actividad diaria y estacional de un gremio de saurios en las dunas de arena de Viesca, Coahuila, México

Rev. Mex. Biodivers.

(2007)

S.R. Goldberg

Reproduction in the yellow-spotted night lizard, Lepidophyma flavimaculatum (Squamata, Xantusiidae), from Costa Rica

Phyllomedusa

(2009)

S.R. Goldberg et al.

Lepidophyma gaigeae (Gaige's tropical night lizard) reproduction

Herpetol. Rev.

(2003)

H.W. Greene

Reproduction in a Mexican xantusiid lizard, Lepidophyma tuxtlae

J. Herpetol.

(1970)

J.W. Grigg et al.

Conservatism of lizard thermal tolerances and body temperatures across evolutionary history and geography

Biol. Lett.

(2013)

L. Gvoždík

To heat or to save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: Lacertidae) in different thermal environments along an altitudinal gradient

Can. J. Zool.

(2002)

P.S. Harlow

A harmless technique for sexing hatchling lizards

Herpetol. Rev.

(1996)

P.E. Hertz et al.

Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question

Am. Nat.

(1993)

M.A. Hitchcock et al.

Thermoregulation in nocturnal ecthotherms: seasonal and intraspecific variation in the mediterranean gecko (Hemidactylus turcicus)

J. Herpetol.

(2006)

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Rufino Santos-Bibiano: (June 23rd, 1991) is a Master's student of the Posgrado en Ciencias Biológicas at the Universidad Nacional Autónoma de México (UNAM). His main topics of interest are the phenology of reproduction, thermal ecophysiology and diversity of lizards and snakes from Mexico. He has participated in several research projects on these topics in central and southern Mexico. He has published several scientific contributions on distribution and natural history, as well as descriptions of new species of reptiles from Mexico.

Francisco Javier Muñoz-Nolasco: (June 3rd, 1991) is a Master's student of the Posgrado en Ciencias Biológicas at the Universidad Nacional Autónoma de México (UNAM). He is currently working on aspects of thermal ecology, evaporative water loss, and locomotor performance of skinks (Scincella and Plestiodon), as well as of some habitat-restricted lizards from Mexico. He has published a number of works on the herpetofauna of his natal state, Jalisco. His primary interests include physiological and evolutionary ecology of amphibians and reptiles.

Pierre Charruau: is a full researcher in ecology of reptiles and amphibians at the Centro del Cambio Global y la Sustentabilidad en el Sureste A.C., Villahermosa, Tabasco, Mexico. He received his Doctorate in Ecology from El Colegio de la Frontera Sur, Chetumal, Quintana Roo, Mexico. He realized a Postdoctoral stay at the Instituto de Biología of the Universidad Nacional Autónoma de México, Mexico. His research interests include effects of climate on reptile populations, conservation, ecology, diversity and health of reptiles and amphibians, with a principal focus on crocodiles.

Fausto Roberto Méndez-de la Cruz: (September 6, 1957) he obtained his Ph.D. (1989) at UNAM. He conducted a postdoctoral year at the University of Florida, USA, and a sabbatical year at the Virginia Polytechnic Institute and State University. He is a full professor at the Instituto de Biología, UNAM. His main Research topics are the evolution of viviparity, parthenogenesis, and the vulnerability of amphibians and reptiles to global warming. He was president of the Sociedad Herpetológica Mexicana and Sociedad Latinoamericana de Herpetología. Méndez-de la Cruz has more than 100 publications.

View full text

Thermal ecology and activity patterns of six species of tropical night lizards (Squamata: Xantusiidae: Lepidophyma) from Mexico

Highlights

Abstract

Introduction

Section snippets

Study organisms and sites

Results

Discussion

Acknowledgments

Author contributions

Interests statement

J. Therm. Biol.

Mol. Phylogenet. Evol.

J. Therm. Biol.

Refuge use in a patagonian nocturnal lizard, Homonota darwini: the role of temperature

J. Herpetol.

Australian geckos do not display diel variation in thermoregulatory behavior

Copeia

Behavioral thermoregulation increases growth-rate in a nocturnal lizard

J. Herpetol.

Locomotor performance at low temperature and the evolution of nocturnality in geckos

Evolution

Systematics of xantusid lizards of the genus Lepidophyma

Contrib. Sci.

Thermal ecology of black rat snakes (Elaphe obsoleta) in a thermally challenging environment

Ecology

Body temperatures of reptiles

Am. Midl. Nat.

Turn up the heat: thermal tolerances of lizards at La Selva, Costa Rica

Oecologia

New herpetofaunal records for the state of Oaxaca, Mexico

Mesoam. Herpetol.

Lizard thermal trait variation at multiple scales: a review

J. Comp. Physiol. B

Choosing and Using Statistics: A Biologist’s Guide

Third ed.

Apuntes ecológicos sobre Cricosaura typica (Sauria: Xantusiidae) de Cuba

Caribb. J. Sci.

Worldclim 2: New 1-km spatial resolution climate surfaces for global land areas

Int. J. Clim.

Ecología térmica de la lagartija microendémica Anolis gadovii (Sauria: dactyloidae)

Ciclos de actividad diaria y estacional de un gremio de saurios en las dunas de arena de Viesca, Coahuila, México

Rev. Mex. Biodivers.

Reproduction in the yellow-spotted night lizard, Lepidophyma flavimaculatum (Squamata, Xantusiidae), from Costa Rica

Phyllomedusa

Lepidophyma gaigeae (Gaige's tropical night lizard) reproduction

Herpetol. Rev.

Reproduction in a Mexican xantusiid lizard, Lepidophyma tuxtlae

J. Herpetol.

Conservatism of lizard thermal tolerances and body temperatures across evolutionary history and geography

Biol. Lett.

To heat or to save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: Lacertidae) in different thermal environments along an altitudinal gradient

Can. J. Zool.

A harmless technique for sexing hatchling lizards

Herpetol. Rev.

Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question

Am. Nat.

Thermoregulation in nocturnal ecthotherms: seasonal and intraspecific variation in the mediterranean gecko (Hemidactylus turcicus)

J. Herpetol.