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Facultative Thermogenesis During Brooding Is Not the Norm Among Pythons

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Facultative Thermogenesis During Brooding Is Not the Norm Among Pythons Facultative thermogenesis during brooding is not the norm among pythons Jake Brashears & Dale F. DeNardo Journal of Comparative Physiology A Neuroethology, Sensory, Neural, and Behavioral Physiology ISSN 0340-7594 Volume 201 Number 8 J Comp Physiol A (2015) 201:817-825 DOI 10.1007/s00359-015-1025-4 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag Berlin Heidelberg. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy J Comp Physiol A (2015) 201:817–825 DOI 10.1007/s00359-015-1025-4 ORIGINAL PAPER Facultative thermogenesis during brooding is not the norm among pythons Jake Brashears1,2 · Dale F. DeNardo1 Received: 8 February 2015 / Revised: 2 May 2015 / Accepted: 12 June 2015 / Published online: 27 June 2015 © Springer-Verlag Berlin Heidelberg 2015 Abstract Facultative thermogenesis is often attributed to our data combined with existing literature demonstrate pythons in general despite limited comparative data avail- that facultative thermogenesis is not as widespread among able for the family. While all species within Pythonidae pythons as previously thought. brood their eggs, only two species are known to produce heat to enhance embryonic thermal regulation. By contrast, Keywords Evolution of endothermy · Metabolic rate · a few python species have been reported to have insig- Parental care · Reptile · Snake nificant thermogenic capabilities. To provide insight into potential phylogenetic, morphological, and ecological fac- tors influencing thermogenic capability among pythons, Introduction we measured metabolic rates and clutch-environment temperature differentials at two environmental tempera- Although it often requires a substantial expenditure of tures—python preferred brooding temperature (31.5 °C) resources on the part of the parent, parental care is wide- and a sub-optimal temperature (25.5 °C)—in six species spread because it confers numerous fitness benefits to off- of pythons, including members of two major phylogenetic spring (e.g., increased survival and growth) (Clutton-Brock branches currently devoid of data on the subject. We found 1991). A common benefit of parental care is thermoregula- no evidence of facultative thermogenesis in five species: tion of the developing offspring (Shine and Harlow 1996; Aspidites melanocephalus, A. ramsayi, Morelia viridis, M. Ashmore and Janzen 2003). In fact, thermoregulation of the spilota cheynei, and Python regius. However, we found that developmental environment has been proposed as an ini- Bothrochilus boa had a thermal metabolic sensitivity indic- tial driving factor in the evolution of endothermy (Farmer ative of facultative thermogenesis (i.e., a higher metabolic 2000). rate at the lower temperature). However, its metabolic rate Pythons (Squamata: Pythonidae) are rare among reptiles was quite low and technical challenges prevented us from in providing ubiquitous parental care that provides ther- measuring temperature differential to make conclusions mal, hydric, and predator defense benefits (Shine 2004; about facultative endothermy in this species. Regardless, Stahlschmidt and DeNardo 2010). Pythons are ectothermic throughout most of life, but during brooding the females of some species are known to increase their metabolic rate and * Jake Brashears exhibit muscular twitching, termed facultative thermogen- [email protected] esis. While widely accepted as a trait of pythons in general, Dale F. DeNardo of the 44 extant python species (Barker et al. 2015), facul- [email protected] tative thermogenesis has been confirmed in only two spe- cies: the Burmese python (Python molurus) (Vinegar et al. 1 School of Life Sciences, Arizona State University, PO Box 874501, Tempe, AZ 85281‑4501, USA 1970), which has since been broken into two species (P. molurus and P. bivitattus, Jacobs et al. 2009) and two sub- 2 Present Address: Department of Life Sciences, San Diego City College, 1313 Park Boulevard, San Diego, species of the carpet python (Morelia spilota spilota) (Slip CA 92101‑4787, USA and Shine 1988); (M. s. imbricata) (Pearson et al. 2003). In 1 3 Author's personal copy 818 J Comp Physiol A (2015) 201:817–825 these species, facultative thermogenesis provides substan- species as the diamond python (M. s. spilota) and the tial heat to the clutch, supplementing the insulatory benefits southwestern carpet python (M. s. imbricata), both of associated with coiling around the eggs (Stahlschmidt et al. which have been shown to use facultative thermogenesis 2008). Female heat production is inversely proportional to (Slip and Shine 1988; Pearson et al. 2003). Morelia spilota environmental temperature (Tenv), with metabolic rate and is widely distributed throughout Australia and thus experi- muscular twitching increasing as temperature decreases ences a great range with considerable variation in environ- below optimal developmental temperature (approximately mental temperature. Morelia s. spilota and M. s. imbricata 31.5 °C for most species) (Brashears and DeNardo 2013). are both from high latitudes, while M. s. cheynei is more In P. molurus, maximum heat production occurs when Tenv tropical in distribution. Examining M. s. cheynei provides approaches 24 °C (Van Mierop and Barnard 1978). insight into environmental influences on facultative ther- Currently, the occurrence of facultative thermogenesis mogenesis. Lastly, we examined the ball pythons (Python within the Pythonidae remains unclear (Stahlschmidt and regius) to clarify somewhat ambiguous prior results from DeNardo 2010). This limitation compromises our under- this species. Together, these species combined with the pre- standing of the factors that have shaped its evolution within vious species studied provide a considerable variation in the pythons and, as a result, decreases the utility of python adult size and thus may reveal any influence that size may facultative endothermy in evaluating the driving forces have on the use of endothermy. behind the evolution of endothermy. More complete knowl- edge of the existence of facultative endothermy among pythons would provide for a better understanding of the rel- Materials and methods ative importance of phylogenetic constraints, morphologi- cal limitations, and environmental conditions on the exist- Animals ence of facultative endothermy, and thus provide insight into driving forces (and constraints) of endothermic capa- Over two breeding seasons (2007 and 2008), data were col- bility in general. lected from 18 brooding females representing six species of The Pythonidae is divided between two primary phylo- python: 3 A. melanocephalus, 3 A. ramsayi, 2 B. boa, 3 M. genetic clades, an Afro-Asian clade with two major line- spilota cheynei, 1 M. viridis, and 6 P. regius. Snakes were ages and an Indo-Australian clade with eight major lineages either borrowed from private breeders and housed at Ari- (Reynolds et al. 2014; for recent review, see Barker et al. zona State University (ASU) during the two-year period or 2015). The two species with confirmed facultative thermo- were part of a long-term captive breeding colony at ASU. genesis are in the different clades—P. molurus within the Animals were housed individually in temperature-con- Afro-Asian group and M. spilota within the Indo-Austral- trolled rooms (27 1 °C) under a 12:12 h photoperiod ± ian group. Conversely, both primary clades are also known with supplemental heat provided at one of the cage by a to contain species where the absence of facultative thermo- subsurface heating element (Flexwatt, Flexwatt Corp., genesis has been confirmed—the rock python (P. sebae) Wareham, MA, USA). During the non-breeding season (Vinegar et al. 1970) and the ball python (P. regius) (Ellis (June to November), animals were fed weekly and pro- and Chappell 1987) within the Afro-Asian clade and the vided water ad libitum. In November, animals underwent reticulated python (P. reticulatus) (Vinegar et al. 1970), the a 6-week cooling period in which we turned off the sub- water python (Liasis fuscus) (Stahlschmidt et al. 2012), and surface heating elements and ceased feeding. In January, the Children’s python (Antaresia childreni) (Stahlschmidt subsurface heating and feeding resumed. After 2 weeks, we and DeNardo 2009) in the Indo-Australian clade (Fig. 1). began rotating males through the females’ cages. In Feb- Brooding metabolic data are currently absent for all other ruary, we began weekly ultrasound scans (Concept/MCV, species, including no representation from four of the ten Dynamic Imaging, Livingston, Scotland) of females to major lineages. assess their reproductive progress. The aim of this study was to assess the presence of We weighed gravid females 1 week prior to oviposition. brooding facultative thermogenesis in four previously For three of the species (M. viridis, M. s. cheynei, P. regius), unstudied species of python, including representatives from pre-oviposition females were
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