Abstract
Populations of snakes and other reptiles are declining worldwide. Habitat loss and degradation is thought to be a significant factor in these declines, so to improve management strategies it is important to increase our understanding of reptilian habitat requirements. Modern agriculture is abandoning the tradition of gathering compost and manure in large heaps. Consequently these unusually warm environments are disappearing from the landscape. This may imperil populations of grass snakes (Natrix natrix) that rely on these anthropogenic heat sources to incubate their eggs. We conducted a relocation experiment to examine if eggs can develop successfully in other more natural environments that grass snakes potentially could utilize in the absence of manure heaps and compost piles. We found that hatching success was high (71 %) when we placed eggs in manure heaps and non-existent (0 %) when we placed them in potential ‘natural’ nests. Placement in compost piles resulted in intermediate (43 %) hatching success. Eggs in manure heaps hatched earlier than eggs in compost piles and thermal data from the nests showed that temperatures were higher and more stable in manure heaps than in compost piles and potential ‘natural’ nests. Jointly these results suggest that manure heaps generally provide a better nesting habitat than compost piles, attributable to thermal differences between the environments. Our findings facilitate improvement of current management strategies and have implications for conservation of oviparous reptiles in general.
Similar content being viewed by others
References
Ahlén I, Andrén A, Nilson G (2001) Sveriges grodor, ödlor och ormar: fältguide och faktasamling. Naturskyddsföreningen, Stockholm
Alford RA, Dixon PM, Pechmann JHK (2001) Global amphibian population declines. Nature 412:499–500
Beebee T, Griffiths R (2000) Amphibians and reptiles. A natural history of the British herpetofauna. Harper Collins Publishers, London
Beutler A, Assman O, Drobny M, Schilling D (1993) Die ringelnatter (Natrix natrix natrix Linnaeus, 1758) in Sudbayern-Bestandssituiation, Gefahrdung und Schutz. Mertensiella 3:171–180
Birchard GF (2004) Effects of incubation temperature. In: Deeming DC (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 103–123
Blouin-Demers G, Weatherhead PJ, Row JR (2004) Phenotypic consequences of nest-site selection in black rat snakes (Elaphe obsoleta). Can J Zool 82:449–456
Booth DT (2004) Artificial incubation. In: Deeming DC (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 253–263
Brown GP, Shine R (2005) Nesting snakes (Tropidonophis mairii, Colubridae) selectively oviposit in sites that provide evidence of previous successful hatching. Can J Zool 83:1134–1137
Brown GP, Shine R (2007) Like mother, like daughter: inheritance of nest site location in snakes. Biol Lett 3:131–133
Burger J, Zappalorti RT (1991) Nesting behavior of pine snakes (Pithuopis m. melanoleucus) in the New Jersey Pine Barrens. J Herpetol 25:152–160
Burghardt GM, Murphy JB, Chiszar D, Hutchins M (2009) Combating ophiophobia: origins, treatments, education, and conservation tools. In: Mullin SJ, Seigel RA (eds) Snakes: ecology and conservation. Cornell University Press, Ithaca, pp 262–280
Caughley G, Grice R, Barker B, Brown B (1988) The edge of the range. J Anim Ecol 57:771–785
Cedhagen T, Nilson G (1991) Grod-och kräldjur i Norden. Fältbiologerna, Sollentuna
Cox NA, Temple HJ (2009) European red list of reptiles. Office for official publications of the European communities, Luxembourg
Curry-Lindahl K (1975) Groddjur och kräldjur i färg: alla Europas arter. Almqvist och Wiksell Förlag AB, Stockholm
Dorcas ME, Willson JD (2009) Innovative methods for studies of snake ecology and conservation. In: Mullin SJ, Seigel RA (eds) Snakes: ecology and conservation. Cornell University Press, Ithaca, pp 5–37
Eckstein HP (1992) Die bedeutung von pferdemisthaufen für die ringelnatter. Bufo Express 1:3–4
Feyrer F, Nobriga ML, Sommer TR (2007) Multidecadal trends for three declining fish species: habitat patterns and mechanisms in the San Fransisco estuary, California, USA. Can J Fish Aquat Sci 64:723–734
Flatt T, Shine R, Borges-Landaez PA, Downes SJ (2001) Phenotypic variation in an oviparous montane lizard (Bassiana duperreyi): the effects of thermal and hydric incubation environments. Biol J Linn Soc 74:339–350
Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjà vu amphibians. Bioscience 50:653–666
Glandt D (2010) Taschenlexikon der amphibien und reptilien Europas. Quelle & Meyer, Wiebelsheim
Goldsmith SK (1984) Aspects of the natural history of the rough green snake, Opheodrys aestivus (COLUBRIDAE). Southwest Nat 29:445–452
Günther R (1996) Die amphibien und reptilien Deutschlands. Gustav Fischer, Jena
Hagman M, Elmberg J, Kärvemo S, Löwenborg K (2012) Grass snakes (Natrix natrix) in Sweden decline together with their anthropogenic nesting-environments. Herpetol J 22:199–202
Harshbarger JC, Coffey MJ, Young MY (2000) Intersexes in Mississippi River shovelnose sturgeon sampled below Saint Louis, Missouri, USA. Mar Environ Res 50:247–250
Isaac LA, Gregory PT (2004) Thermoregulatory behaviour of gravid and non-gravid female grass snakes (Natrix natrix) in a thermally limiting high-latitude environment. J Zool 264:403–409
King DI, Lambert JD, Buonaccorsi JP, Prout LS (2008) Avian population trends in the vulnerable montane forests of the northern Appalachians, USA. Biodivers Conserv 17:2691–2700
Köhler G (2005) Incubation of reptile eggs. Krieger Publishing Company, Malabar
LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710–714
Light T, Marchetti MP (2007) Distinguishing between invasions and habitat changes as drivers of diversity loss among California’s freshwater fishes. Conserv Biol 21:434–446
Löwenborg K, Shine R, Kärvemo S, Hagman M (2010) Grass snakes exploit anthropogenic heat sources to overcome distributional limits imposed by oviparity. Func Ecol 24:1095–1102
Löwenborg K, Shine R, Hagman M (2011) Fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by female grass snakes, Natrix natrix (Colubridae). J Evol Biol 24:177–183
Luiselli L, Filippi E, Capula M (2005) Geographic variation in diet composition of the grass snake (Natrix natrix) along the mainland and an island of Italy: the effects of habitat type and interference with potential competitors. Herpetol J 15:221–230
Madsen T (1983) Growth rates, maturation and sexual size dimorphism in a population of grass snakes, Natrix natrix in southern Sweden. Oikos 40:277–282
Madsen T (1984) Movements, home range size and habitat use of radio-tracked grass snakes (Natrix natrix) in southern Sweden. Copeia 1984:707–713
Madsen T, Shine R (1999) Life history consequences of nest-site variation in tropical pythons (Liasis fuscus). Ecology 80:989–997
Mattison C (2007) The new encyclopedia of snakes. Princeton University Press, New York
McLoughlin PD, Dzus E, Wynes B, Boutin S (2003) Declines in populations of woodland caribou. J Wildl Manage 67:755–761
Mertens D (1995) Population structure and abundance of grass snakes, Natrix natrix in central Germany. J Herpetol 29:454–456
Packard GC, Packard MJ, Miller K, Boardman TJ (1987) Influence of moisture, temperature and substrate on snapping turtle eggs and embryos. Ecology 68:983–993
Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sánchez- Azofeifa GA, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167
Reading CJ (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151:125–131
Reading CJ, Jofre GM (2009) Habitat selection and range size of grass snakes Natrix natrix in an agricultural landscape in southern England. Amphibia Reptilia 30:379–388
Reading CJ, Luiselli LM, Akani GC, Bonnet X, Amori G, Ballouard JM, Filippi E, Naulleau G, Pearson D, Rugiero L (2010) Are snake populations in widespread decline? Biol Lett 7:777–780
Ritter A, Nollert A (1993) Beobachtungen an einem winterquartier der ringelnatter, Natrix n. natrix (Linnaeus 1758), in ostlichen Mecklenberg/Vorpoomern. Mertensiella 3:189–198
Shine R (1995) A new hypothesis for the evolution of viviparity in reptiles. Am Nat 145:809–823
Shine R (2004) Adaptive consequences of developmental plasticity. In: Deeming DC (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 187–210
Shine R, Bonnet X (2009) Reproductive biology, population viability, and options for field management. In: Mullin SJ, Seigel RA (eds) Snakes: ecology and conservation. Cornell University Press, Ithaca, pp 172–200
Shine R, Elphick MJ, Harlow PS (1997) The influence of natural incubation environments on the phenotypic traits of hatchling lizards. Ecology 78:2559–2568
Smith MA (1954) The British amphibians and reptiles. Collins, London
Stamps JA, Krishnan VV (1998) Territory acquisition in lizards IV. Obtaining high status and exclusive home ranges. Anim Behav 55:461–472
Steward JW (1971) The snakes of Europe. Fairleigh Dickinson University Press, Rutherford
Street D (1979) The reptiles of northern and central Europe. BT Batsford, London
Svedberg U, Andersen M, Feilberg J (2004) Svenska djur och växter. Prisma Norstedts Förlagsgrupp, Stockholm
Thorpe RS (1975) Quantitative handling of characters useful in snake systematics with particular reference to intraspecific variation in the ringed snake Natrix natrix (L.). Biol J Linn Soc 7:27–43
Townson S (1990) Incubation of grass snake (Natrix natrix helvetica) eggs. B Herpetol Soc Bull 34:13–15
Van Wijngaarden-Bakker LH, Troostheide KD (2003) Bones and eggs. The archaeological presence of the grass snake Natrix natrix (L.) in The Netherlands. Environ Archaeol 8:111–118
Wake DB (1991) Declining amphibian populations. Science 253:860
Warner DA, Shine R (2007) Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154:65–73
Weatherhead PJ, Madsen T (2009) Linking behavioral ecology to conservation objectives. In: Mullin SJ, Seigel RA (eds) Snakes: ecology and conservation. Cornell University Press, Ithaca, pp 149–171
Winne CT, Willson JD, Todd BD, Andrews KM, Gibbons JW (2007) Enigmatic decline of a protected population of eastern kingsnakes, Lampropeltis getula, in South Carolina. Copeia 2007:507–519
Wretenberg J, Lindström Å, Svensson S, Thierfelder T, Pärt T (2006) Population trends of farmland birds in Sweden and England—similar trends but different patterns of agricultural intensification. J App Ecol 43:1110–1120
Zuiderwijk A, Smit G, Van Den Bogert H (1993) Man-made hatcheries for grass snakes (Natrix natrix L 1758): a simple method for grass snake conservation. Mertensiella 3:227–234
Acknowledgments
We thank E. Di Marino for help with technical engineering and P. Dahlin and K. Eklund for providing equipment. Our gratitude also goes to the many farmers and landowners who kindly provided access to their compost piles and manure heaps. Two anonymous reviewers provided helpful comments on an earlier version of the manuscript. Snakes were collected under permits from Länsstyrelsen in Stockholm and Uppsala. Stockholms Norra Djurförsöksetiska Nämnd approved experimental procedures (ethics approval number N43/09). Funding was provided by Stiftelsen Oscar och Lili Lamms Minne, Helge Axelsson Johnssons Minnesfond, Lars Hiertas Minnesfond, Längmanska Kulturfonden, Magnus Bergvalls Stiftelse, the Royal Swedish Academy of Sciences, the Swedish Research Council, and the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Löwenborg, K., Kärvemo, S., Tiwe, A. et al. Agricultural by-products provide critical habitat components for cold-climate populations of an oviparous snake (Natrix natrix). Biodivers Conserv 21, 2477–2488 (2012). https://doi.org/10.1007/s10531-012-0308-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-012-0308-0