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Nesting ecology of the grass snake (Natrix natrix) and its implications for conservation
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0001-7630-544X
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The onset of agriculture about 12,000 years ago has had a major influence on the biodiversity of plants and animals. Unfortunately, the rapid changes in agricultural practices that has occurred in recent times has negatively affected many farmland species. One such species is the grass snake (Natrix natrix), which has been reported to decline in many parts of Europe, including Sweden. The grass snake is unique, not only in that it is the most northerly distributed oviparous reptile in the world, but also because of its habit of using anthropogenic heat sources such as manure heaps and composts as nesting-sites. Unfortunately changes in manure management and abandonment of farmlands have resulted in a decline and fragmentation of these environments. This may pose a threat for the northernmost populations of the grass snake, because natural nests in these areas may not provide sufficient heat for the eggs to hatch. The eggs and embryos of reptiles are highly sensitive to incubation temperatures, which can influence not only hatching success but also many phenotypic traits in the hatchlings. In this thesis I used a series of laboratory and field experiments to investigate the importance of anthropogenic heat sources for the reproductive ecology of cold-climate populations of grass snakes.  More specifically, I aimed to investigate thermal regimes of nests and how they influence embryonic development and offspring traits associated with survival and fitness. The results showed that manure heaps and composts are significantly warmer than potential natural nests and that natural nests do not provide sufficient heat to sustain embryonic development. Further, manure heaps were warmer and more constant in temperature than composts, resulting in higher hatching success and earlier hatching in manure heaps. The higher thermal variability in composts increased the frequency of abnormalities that are likely to negatively affect survival and fitness. In conclusion, this thesis shows that the use of anthropogenic heat sources has enabled grass snakes to expand their range farther north than any other oviparous reptile and that the thermal dichotomy in the primary nesting environments used by grass snakes contribute to important life-history variation in this species. These findings have important implications for conservation of reptile populations in general and grass snakes in particular.  

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2016.
Keyword [en]
agriculture, anthropogenic, climate, embryonic development, incubation
National Category
Ecology
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-125524ISBN: 978-91-7649-307-6 (print)OAI: oai:DiVA.org:su-125524DiVA: diva2:894177
Public defence
2016-02-19, Vivi Täckholmsalen, Svante Arrhenius väg 20 A, Stockholm, 10:00 (English)
Opponent
Supervisors
Available from: 2016-01-27 Created: 2016-01-13 Last updated: 2017-02-23Bibliographically approved
List of papers
1. Grass snakes exploit anthropogenic heat sources to overcome distributional limits imposed by oviparity
Open this publication in new window or tab >>Grass snakes exploit anthropogenic heat sources to overcome distributional limits imposed by oviparity
2010 (English)In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 24, no 5, 1095-1102 p.Article in journal (Refereed) Published
Abstract [en]

P>1. A lack of warm nest-sites prevents oviparous reptile species from reproducing in cool climates; such areas are dominated by viviparous species because sun-seeking pregnant females can maintain high temperatures for their developing offspring. 2. Our field and laboratory studies show that one oviparous species (the grass snake, Natrix natrix) escapes this cold-climate constraint (and hence, extends much further north in Europe than do other oviparous taxa) by ovipositing in a thermally distinctive man-made microhabitat (manure heaps on farms). 3. In the field, temperatures inside manure heaps averaged 30 center dot 7 degrees C, much higher than compost heaps (20 center dot 6 degrees C) or potential natural nest-sites under logs and rocks (15 center dot 5 degrees C). 4. In the laboratory, higher incubation temperatures not only hastened hatching, but also increased hatching success and modified the body sizes, colours, and locomotor abilities of hatchlings. Incubation temperatures typical of manure heaps (rather than alternative nest-sites) resulted in larger, faster offspring that hatched earlier in the season. 5. Thus, anthropogenic activities have generated potential nest-sites offering thermal regimes not naturally available in the region; and grass snakes have exploited that opportunity to escape the thermal limits that restrict geographic distributions of other oviparous reptile taxa.

Keyword
geographic distribution, maternal manipulation hypothesis, natricine, reproductive mode, thermoregulation, viviparity
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-50179 (URN)10.1111/j.1365-2435.2010.01730.x (DOI)000281895800018 ()
Note

4

Available from: 2010-12-29 Created: 2010-12-21 Last updated: 2017-12-11Bibliographically approved
2. How a thermal dichotomy in nesting environments influences offspring of the world's most northerly oviparous snake, Natrix natrix (Colubridae)
Open this publication in new window or tab >>How a thermal dichotomy in nesting environments influences offspring of the world's most northerly oviparous snake, Natrix natrix (Colubridae)
2012 (English)In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 107, no 4, 833-844 p.Article in journal (Refereed) Published
Abstract [en]

Temperature has a major influence on the rate of embryonic development in ectothermic organisms. While incubation experiments unambiguously show that constant high temperature accelerates development and shortens embryonic life, studies on the effect of fluctuating temperatures have generated contradictory results. Grass snakes (Natrix natrix) occur at latitudes and altitudes that are unusually cool for an oviparous reptile. In these cool climates females typically lay their eggs in heat-generating anthropogenic microhabitats that provide either a highly fluctuating (compost piles) or a relatively constant (manure heaps) thermal nesting environment. A laboratory experiment with fluctuating and constant incubation temperatures mimicking those recorded in such nests in the field showed that this nest-site dichotomy influences the development of the embryos, and the morphology and locomotor performance of the hatchlings. The incubation period increased at fluctuating temperatures and the fact that the rate of embryonic development showed a decelerating pattern with temperature suggests that periods of low temperature had a relatively larger influence on average development than periods of high temperature. Our study demonstrates how a dichotomy in the nesting environments available to female grass snakes in cool climates can affect variation in the duration of the incubation period and offspring phenotypes in ways that may have consequences for fitness.

Keyword
compost, development, embryo, incubation, manure heap, phenotype, reptiles, thermal fluctuation
National Category
Zoology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-84804 (URN)10.1111/j.1095-8312.2012.01972.x (DOI)000311404100009 ()
Funder
A multiscale, cross‐disciplinary approach to the study of climate change effect on ecosystem services and biodiversitySwedish Research CouncilSwedish Research Council Formas
Note

AuthorCount:3;

Available from: 2013-01-02 Created: 2013-01-02 Last updated: 2017-12-06Bibliographically approved
3. Fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by female grass snakes, Natrix natrix (Colubridae)
Open this publication in new window or tab >>Fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by female grass snakes, Natrix natrix (Colubridae)
2011 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 24, no 1, 177-183 p.Article in journal (Refereed) Published
Abstract [en]

Phenotypic traits of hatchling reptiles are strongly influenced by incubation regimes (e.g. of temperature and moisture), suggesting that maternal choice of suitable nest-sites should be under intense selection. Our laboratory incubation of 209 eggs (17 clutches) from wild-caught Swedish grass snakes (Natrix natrix) showed that scale abnormalities (half-scales on one side of the body, often reflecting lateral asymmetry in the number of ribs) occurred more frequently if eggs were incubated under cooler conditions. Especially at low incubation temperatures, individuals with scale asymmetries took longer to hatch than did symmetric conspecifics, were smaller in body length at hatching and were slower in trials of locomotor speed. Anti-predator tactics also covaried with scale asymmetry. These patterns suggest that individuals with asymmetric scales should have lower fitness and hence should rarely survive to adulthood in the wild. We tested this prediction by examining 201 field-collected snakes from museum collections. As predicted, scale asymmetries were seen primarily in small snakes, and rarely in larger animals. We interpret these data to suggest that scale asymmetries in this species offer an index of developmental instability and that fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by females.

Keyword
asymmetry, development, embryo, oviparity, phenotypic
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-69708 (URN)10.1111/j.1420-9101.2010.02153.x (DOI)000285418500017 ()
Note

authorCount :3

Available from: 2012-01-15 Created: 2012-01-15 Last updated: 2017-12-08Bibliographically approved
4. Agricultural by-products provide critical habitat components for cold-climate populations of an oviparous snake (Natrix natrix)
Open this publication in new window or tab >>Agricultural by-products provide critical habitat components for cold-climate populations of an oviparous snake (Natrix natrix)
2012 (English)In: Biodiversity and Conservation, ISSN 0960-3115, E-ISSN 1572-9710, Vol. 21, no 10, 2477-2488 p.Article in journal (Refereed) Published
Abstract [en]

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.

Keyword
Anthropogenic, Developmental plasticity, Incubation, Nesting-sites, Phenotype, Reptile
National Category
Ecology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-76917 (URN)10.1007/s10531-012-0308-0 (DOI)000307533100004 ()
Available from: 2012-05-24 Created: 2012-05-24 Last updated: 2017-12-07Bibliographically approved

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