Skip to main content

Food supplementation affects the foraging ecology of a low-energy, ambush-foraging snake

Behavioral Ecology and Sociobiology volume 71, Article number: 5 (2017) Cite this article

Abstract

The effect of food availability on the spatial ecology of animals varies within and across study systems because a multitude of factors can affect the spatial activity of organisms. Low-energy specialists, such as ambush-foraging snakes, feed infrequently and can endure long periods without food. Because they have low-energy requirements, one possible tactic for feeding may be to simply ambush for longer periods when prey availability is low, thereby decreasing the potential costs associated with locating new ambush sites. We used radiotelemetry, supplemental feeding, and remote video cameras on free-ranging male puff adders (Bitis arietans) in South Africa to test the hypothesis that food intake affects the foraging ecology of extreme low-energy, ambush foragers and to quantify their natural feeding rates. Supplementally fed puff adders improved their body condition, spent less time foraging, and decreased distance traveled compared to control snakes. However, movement frequency and home range size did not differ between the two groups. These findings indicate that control snakes traveled farther within similar-sized home ranges compared to fed snakes and did so at no survival cost. Further, naturally foraging puff adders successfully caught a prey of small size once every 10 days on average. Hence, despite their “sit-and-wait” foraging strategy and their low-energy intake/requirements, underfed puff adders travel widely to presumably find appropriate ambush sites that maximize prey capture. Our research provides the first strong evidence that the spatial activity of a terrestrial vertebrate species with extremely low energetic demands is significantly affected by food intake.

Significance statement

Because animals travel their home range partly to forage, their space use can be affected by the amount of food available in nature. We show that, despite a low-energy lifestyle, the movement level of an ambush-foraging snake that feed infrequently is linked to the amount of food they eat. Underfed snakes traveled greater distances in search of prey, within similar-sized home ranges, compared to well-fed snakes, and they did so at no survival cost. Hence, our research adds to our understanding of the effect of food on the spatial ecology of animals, by providing conclusive evidence that the spatial response of an organism with extremely low-energy demands can be affected by food.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Adams ES (2001) Approaches to the study of territory size and shape. Annu Rev Ecol Syst 32:277–303

    Article  Google Scholar 

  • Aleksiuk M, Gregory PT (1974) Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. Copeia 1974:681–689

    Article  Google Scholar 

  • Alexander GJ (2007) Thermal biology of the southern African python (Python natalensis): does temperature limit its distribution. In: Henderson RW, Powell R (eds) Biology of the boas and pythons. Eagle Mountain Publishing, Eagle Mountain, pp. 50–75

    Google Scholar 

  • Alexander GJ, Marais J (2007) A guide to the reptiles of southern Africa. Struik Publishers, Cape Town

    Google Scholar 

  • Alexander GJ, Maritz B (2015) Sampling interval affects the estimation of movement parameters in four species of African snakes. J Zool 297:309–318

    Article  Google Scholar 

  • Beaupre SJ (2002) Modeling time-energy allocation in vipers: individual responses to environmental variation and implications for populations. In: Schuett GW, Höggren M, Douglas ME, Greene HW (eds) Biology of the vipers. Eagle Mountain Publishing, Eagle Mountain, pp. 463–482

    Google Scholar 

  • Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can J Zool 68:203–220

    Article  Google Scholar 

  • Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519

    Article  Google Scholar 

  • Clark RW (2006) The use of fixed videography in studying the predation behavior of ambush foraging snakes. Copeia 2006:181–187

    Article  Google Scholar 

  • Clark RW, Tangco S, Barbour MA (2012) Field recordings reveal factors that influence predatory strike success of free-ranging rattlesnakes (Crotalus spp.). Anim Behav 84:183–190

    Article  Google Scholar 

  • Cundall D, Deufel A, MacGregor G, Pattishall A, Richter M (2016) Effects of size, condition, measurer, and time on measurements of snakes. Herpetologica 72:227–234

    Article  Google Scholar 

  • Desy EA, Batzli GO, Liu J (1990) Effects of food and predation on behaviour of prairie voles: a field experiment. Oikos 58:159–168

    Article  Google Scholar 

  • Driver A, Maze K, Rouget M et al. (2005) National spatial biodiversity assessment 2004: priorities for biodiversity conservation in South Africa. Strelitzia 17, Pretoria

  • Duvall D, Goode MJ, Hayes WK, Leonhardt JK, Brown DG (1990) Prairie rattlesnake vernal migration: field experimental analyses and survival value. Natl Geogr Res 6:457–469

    Google Scholar 

  • Fortier GM, Tamarin RH (1998) Movement of meadow voles in response to food and density manipulations: a test of the food-defense and pup-defense hypotheses. J Mammal 79:337–345

    Article  Google Scholar 

  • Gaulin SJC, FitzGerald RW (1988) Home range size as a predictor of mating systems in Microtus. J Mammal 69:311–319

    Article  Google Scholar 

  • Gibbons JW, Semlitsch RD (1987) Activity patterns. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. McGraw-Hill, New York, pp. 396–421

    Google Scholar 

  • Glaudas X, Rodríguez-Robles JA (2011a) A two-level problem: habitat selection in relation to prey abundance in an ambush predator, the speckled rattlesnake (Crotalus mitchellii). Behaviour 148:1491–1524

    Article  Google Scholar 

  • Glaudas X, Rodríguez-Robles JA (2011b) Vagabond males and sedentary females: spatial ecology and mating system of the speckled rattlesnake (Crotalus mitchellii). Biol J Linn Soc 103:681–695

    Article  Google Scholar 

  • Greene HW (1992) The ecological and behavioral context for pitviper evolution. In: Campbell JA, Brodie Jr ED (eds) Biology of the pitvipers. Selva Press, Tyler, pp. 107–117

    Google Scholar 

  • Greene HW (1997) Snakes: the evolution of mystery in nature. University of California Press, Berkeley

    Google Scholar 

  • Gregory PT (2009) Northern lights and seasonal sex: the reproductive ecology of cool-climate snakes. Herpetologica 65:1–13

    Article  Google Scholar 

  • Gregory PT (2011) Temporal dynamics of relative-mass variation of red-sided garter snakes (Thamnophis sirtalis parietalis) at a communal hibernaculum in Manitoba. Ecoscience 18:1–8

    Article  Google Scholar 

  • Haapakoski M, Ylönen H (2010) Effects of fragmented breeding habitat and resource distribution on behavior and survival of the bank vole (Myodes glareolus). Popul Ecol 52:427–435

    Article  Google Scholar 

  • IBM Corp. (2015) IBM SPSS Statistics for Windows, Version 23.0., www.ibm.com/analytics/us/en/technology/spss/

  • Ims RA (1987) Male spacing systems in microtine rodents. Am Nat 130:475–484

    Article  Google Scholar 

  • Ims RA (1988) Spatial clumping of sexually receptive females induces space sharing among male voles. Nature 335:541–543

    Article  CAS  PubMed  Google Scholar 

  • Jellen BC, Shepard DB, Dreslik MJ, Phillips CA (2007) Male movement and body size affect mate acquisition in the eastern massasauga (Sistrurus catenatus). J Herpetol 41:451–457

    Article  Google Scholar 

  • Jones M, Mandelik Y, Dayan T (2001) Coexistence of temporally partitioned spiny mice: roles of habitat structure and foraging behavior. Ecology 82:2164–2176

    Article  Google Scholar 

  • Lagos VO, Contreras LC, Meserve PL, Gutiérrez JR, Jaksic JM (1995) Effect of predation risk on space use in small mammals: a field experiment with a Neotropical rodent. Oikos 74:259–264

    Article  Google Scholar 

  • Lindell LE (2011) Annual variation in growth rate and body condition of adders, Vipera berus: effects of food availability and weather. Can J Zool 75:261–270

    Article  Google Scholar 

  • Madsen T, Shine R (1996) Seasonal migration of predators end prey—a study of pythons and rats in tropical Australia. Ecology 77:149–156

    Article  Google Scholar 

  • Madsen T, Shine R (2000) Rain, fish and snakes: climatically driven population dynamics of Arafura filesnakes in tropical Australia. Oecologia 124:208–215

    Article  CAS  PubMed  Google Scholar 

  • McCue MD (2007) Snakes survive starvation by employing supply- and demand-side economic strategies. Zoology 110:318–327

    Article  PubMed  Google Scholar 

  • McCue MD, Lillywhite HB, Beaupre SJ (2012) Physiological responses to starvation: low energy specialists. In: McCue MD (ed) Comparative physiology of fasting, starvation and food limitation. Springer-Verlag, Berlin, pp. 103–131

    Chapter  Google Scholar 

  • Myers JP, Connors PG, Pitelka FA (1979) Territory size in wintering sanderlings: the effects of prey abundance and intruder density. Auk 96:551–561

    Google Scholar 

  • Nowak EM, Theimer TC, Schuett GW (2008) Functional and numerical responses of predators: where do vipers fit in the traditional paradigms? Biol Rev 83:601–620

    Article  PubMed  Google Scholar 

  • Nowak EM, Schuett GW, Theimer TC, Sisk TD, Nishikawa K (2015) Does short-term provisioning of resources to prey result in behavioral shifts by rattlesnakes? J Wildlife Manage 79:357–372

    Article  Google Scholar 

  • Pough FH (1980) The advantages of ectothermy for tetrapods. Am Nat 115:92–112

    Article  Google Scholar 

  • Prestt I (1971) An ecological study of the viper Vipera berus in southern Britain. J Zool 164:373–418

    Article  Google Scholar 

  • Punzo F (2005) Chemosensory recognition by males of the desert pocket mouse, Chaetodipus pencillatus to odors of various species of snakes. Ethol Ecol Evol 17:83–89

    Article  Google Scholar 

  • Putnam BJ, Barbour MA, Clark RW (2016) The foraging behavior of free-ranging rattlesnakes (Crotalus oreganus) in California ground squirrel (Otospermophilus beecheyi) colonies. Herpetologica 72:55–63

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna www.r-project.org

    Google Scholar 

  • Reinert HK (1992) Radiotelemetric field studies of pitvipers: data acquisition and analysis. In: Campbell JA, Brodie Jr ED (eds) Biology of the pitvipers. Selva Press, Tyler, pp. 185–198

    Google Scholar 

  • Reinert HK, Cundall D (1982) An improved surgical implantation method for radio-tracking snakes. Copeia 1982:702–705

    Article  Google Scholar 

  • Row JR, Blouin-Demers G (2006) Kernels are not accurate estimators of home-range size for herpetofauna. Copeia 2006:797–802

    Article  Google Scholar 

  • Schoener TW (1968) Sizes of feeding territories among birds. Ecology 49:123–141

    Article  Google Scholar 

  • Secor SM, Diamond J (1998) A vertebrate model of extreme physiological regulation. Nature 395:659–662

    Article  CAS  PubMed  Google Scholar 

  • Secor SM, Diamond J (2000) Evolution of regulatory responses to feeding in snakes. Physiol Biochem Zool 73:123–141

    Article  CAS  PubMed  Google Scholar 

  • Secor SM, Jayne BC, Bennett AF (1992) Locomotor performance and energetic cost of sidewinding by the snake Crotalus cerastes. J Exp Biol 163:1–14

    Article  Google Scholar 

  • Secor SM, Nagy KA (1994) Bioenergetic correlates of foraging mode for the snakes Crotalus cerastes and Masticophis flagellum. Ecology 75:1600–1614

    Article  Google Scholar 

  • Setser K (2007) Use of anesthesia increases precision of snake length measurement. Herpetol Rev 38:409–411

    Google Scholar 

  • Shine R, Bonnet X (2000) Snakes: a new ‘model organism’ in ecological research? Trends Ecol Evol 15:221–222

    Article  CAS  PubMed  Google Scholar 

  • Shulze RE (1997) South African atlas of agrohydrology and climatology. Water Research Commission, Pretoria

    Google Scholar 

  • Slip DJ, Shine R (1988) Feeding habits of the diamond python, Morelia s. spilota: ambush predation by a boid snake. J Herpetol 22:323–330

    Article  Google Scholar 

  • Smith CF, Schuett GW, Earley RL, Schwenk K (2009) The spatial and reproductive ecology of the copperhead (Agkistrodon contortrix) at the northeastern extreme of its range. Herpetol Monogr 23:45–73

    Article  Google Scholar 

  • Spotila JR, Standora EA (1985) Energy budgets of ectothermic vertebrates. Am Zool 25:973–986

    Article  Google Scholar 

  • StatSoft Inc. (2014) STATISTICA (data analysis software system), version 12, www.statsoft.com

  • Stenger J (1958) Food habits and available food of ovenbirds in relation to territory size. Auk 75:335–346

    Article  Google Scholar 

  • Taitt MJ, Krebs CJ (1981) The effect of extra food on small rodent populations: II. Voles (Microtus towndendii). J Anim Ecol 50:125–137

    Article  Google Scholar 

  • Taylor EN, Malawy MA, Browning DM, Lemar SV, DeNardo DF (2005) Effects of food supplementation on the physiological ecology of female western diamond-backed rattlesnakes (Crotalus atrox). Oecologia 144:206–214

    Article  PubMed  Google Scholar 

  • Tetzlaff SJ (2015) To forage, mate or thermoregulate? Influence of food supplementation on behavior of the rattlesnake Sistrurus catenatus. Master thesis, Department of Biology, Purdue University, Fort Wayne, Indiana, USA

  • Tetzlaff SJ, Ravesi M, Parker J, Forzley M, Kingsbury B (2015) Feeding and breeding: a northern population of massasauga rattlesnakes, Sistrurus catenatus (Rafinesque 1818), continues to hunt during the mating season. Herpetol Notes 8:277–280

    Google Scholar 

  • Ujvari B, Shine R, Madsen T (2011) How well do predators adjust to climate-mediated shifts in prey distribution? A study on Australian water pythons. Ecology 92:777–783

    Article  PubMed  Google Scholar 

  • Walton M, Jayne BC, Bennett AF (1990) The energetic cost of limbless locomotion. Science 249:524–527

    Article  CAS  PubMed  Google Scholar 

  • Wasko DK, Sasa M (2012) Food resources influence spatial ecology, habitat selection, and foraging behavior in an ambush-hunting snake (Viperidae: Bothrops asper): an experimental study. Zoology 115:179–187

    Article  PubMed  Google Scholar 

  • Waye HL, Mason RT (2008) A combination of body condition measurements is more informative than conventional condition indices: temporal variation in body condition and corticosterone in brown tree snakes (Boiga irregularis). Gen Comp Endocr 155:607–612

    Article  CAS  PubMed  Google Scholar 

  • Weatherhead PJ, Brown GP (1996) Measurement versus estimation of condition in snakes. Can J Zool 74:1617–1621

    Article  Google Scholar 

  • Webber MM, Glaudas X, Rodríguez-Robles JA (2012) Do sidewinder rattlesnakes (Crotalus cerastes) cease feeding during the breeding season? Copeia 2012:100–105

    Article  Google Scholar 

Download references

Acknowledgments

We thank two anonymous reviewers for providing their helpful comments on earlier drafts of this manuscript; K. Erlwanger, M.A. Costello, and K. Thambu and the central animal service staff at the University of Witwatersrand for assisting with the surgical procedures; G. Sauthier and H. Van Der Vyver for their field assistance; L. Traill for the analytical advice; and the landowners of the Dinokeng Game Reserve that granted us access to their properties to track snakes, specifically the Graf, Engelbrecht, Keith, Leroux, and Pretorius families; G. and T. Anderson; and F. Erasmus. Last but not least, Gerd and Tienie Graf at Ikhaya lamaDube Game Lodge greatly facilitated this study by providing free accommodation and good company for more than 3 years.

Author information

Authors and Affiliations

  1. School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, P.O. Wits, Johannesburg, 2050, South Africa

    X. Glaudas & G.J. Alexander

Authors
  1. X. Glaudas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G.J. Alexander
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to X. Glaudas.

Ethics declarations

Funding

This study was partly supported by a research grant from the Committee for Research and Exploration at the National Geographic Society (#9443–14) to XG and GJA and by postdoctoral fellowships from the Claude Leon Foundation and the University of the Witwatersrand’s research office to XG.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (University of the Witwatersrand, animal protocol #2012–42-04). Specimens were collected under scientific research permits CPF6–0167 and CPF6–0024, issued by the Gauteng Department of Agriculture and Rural Development.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Communicated by S. J. Downes

Appendix

Appendix

Prey captured by naturally foraging male puff adders: amphibians (n = 7; 3 Schismaderma carens, 1 Amietophrynus gutturalis, 1 Amietophrynus sp., 1 bufonid, 1 unknown amphibian), aves (n = 2; 1 Passer diffusus, 1 Phylloscopus trochilus), mammals (n = 2; 1 Rattus sp., 1 soricid), and reptiles (n = 2; 1 Acanthocercus atricollis, 1 Gerrhosaurus flavigularis).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Glaudas, X., Alexander, G. Food supplementation affects the foraging ecology of a low-energy, ambush-foraging snake. Behav Ecol Sociobiol 71, 5 (2017). https://doi.org/10.1007/s00265-016-2239-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-016-2239-3

Keywords

  • Feeding rate
  • Movement
  • Predator-prey relationship
  • Puff adder
  • Spatial ecology