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  • 1. Elmberg, Johan
    et al.
    Hagman, Mattias
    Stockholm University, Faculty of Science, Department of Zoology.
    Löwenborg, Kristin
    Stockholm University, Faculty of Science, Department of Zoology.
    Pettersson, Gustav
    Voisin, Anais
    Stockholm University, Faculty of Science, Department of Zoology.
    Kärvemo, Simon
    Movements and habitat choice of resident and translocated adult female Grass Snakes (Natrix natrix) during the egg-laying period2019In: Herpetological Journal, ISSN 0268-0130, Vol. 29, no 4, p. 245-251Article in journal (Refereed)
    Abstract [en]

    We used externally applied transmitters to study movements of female grass snakes (Natrix natrix) during the egg-laying period in a near-urban landscape in Sweden. Half of the studied snakes were residents while the other half were translocated individuals with no previous experience of the area. As predicted, resident females moved more goal-oriented and shorter distances than did translocated individuals. Habitat use did not differ between resident and translocated snakes; they were typically found in bushes, reeds, and tall vegetation. Habitat preference (use in relation to availability) showed that bushy habitats, tall grassy vegetation and reedbeds were over-used in proportion to availability, whereas forest and open grass lawns were used less than expected based on availability. Our study highlights the importance of preserving and restoring linear habitat components providing shelter and connectivity in conservation of grass snakes. We suggest that externally applied transmitters are a better option than surgically implanted ones in movement studies of grass snakes, and that translocation as a conservation method for snakes has drawbacks.

  • 2.
    Hagman, Mattias
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Elmberg, Johan
    Kärvemo, Simon
    Löwenborg, Kristin
    Stockholm University, Faculty of Science, Department of Zoology.
    Grass snakes (Natrix natrix) in Sweden decline together with their anthropogenic nesting-environments2012In: Herpetological Journal, ISSN 0268-0130, Vol. 22, no 3, p. 199-202Article in journal (Refereed)
    Abstract [en]

    In this paper we show that the number of grass snake (Natrix natrix L.) specimens deposited in Swedish museum collections has declined in the last eighty years, and that this is correlated with a dramatic national decrease in the number of livestock holdings. These results support the hypothesis that Swedish grass snakes are declining and that this may be linked to a loss of important nesting-environments provided by open manure heaps in small-scale farming. Our study suggests that information obtained from museum databases potentially may be used to explore population trends for snakes and other reptiles.

  • 3.
    Hagman, Mattias
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kärvemo, Simon
    Elmberg, Johan
    Löwenborg, Kristin
    Stockholm University, Faculty of Science, Department of Zoology.
    Life at the edge: the nesting ecology of the world’s most northerly oviparous snake and its implications for conservation2013In: Reptiles in Research: Investigations of Ecology, Physiology and Behavior from Desert to Sea / [ed] William I. Lutterschmidt, New York: Nova Science Publishers, Inc., 2013, p. 247-264Chapter in book (Refereed)
  • 4.
    Hagman, Mattias
    et al.
    University of New South Wales, Australia.
    Löwenborg, Kristin
    Stockholm University, Faculty of Science, Department of Zoology.
    Shine, Richard
    University of Sydney, Australia.
    Determinants of anti-predator tactics in hatchling grass snakes (Natrix natrix)2015In: Behavioural Processes, ISSN 0376-6357, E-ISSN 1872-8308, Vol. 113, p. 60-65Article in journal (Refereed)
    Abstract [en]

    Many organisms exhibit diverse anti-predator tactics, influenced by genetics and prior experience. In ectothermic taxa, offspring phenotypes are often sensitive to developmental temperatures. If the effectiveness of alternative anti-predator responses depends on thermally sensitive traits, then the temperatures experienced during embryonic life should also affect how offspring respond to an approaching predator. We incubated 16 clutches of Swedish grass snakes (Natrix natrix) at a range of developmental temperatures, and scored body size, colour pattern, locomotor performance and anti-predator responses of 213 hatchlings from those clutches. A hatchling snake’s size and locomotor abilities were affected by its clutch of origin, its developmental temperature, and by an interaction between these two factors. Anti-predator tactics were strongly linked to locomotor ability, such that slower snakes tended to rely upon aggressive displays rather than flight. Incubation temperatures that generated slow (and thus aggressive) snakes also modified the colour of the snake’s nuchal spot. Temperatures in the low to medium range generated mostly cream, white and orange spots, whereas medium to high temperatures generated more yellow spots. Incubation effects, and gene X environment interactions, thus may generate complex correlations between morphology, locomotor ability, and anti-predator tactics.

  • 5.
    Löwenborg Di Marino, Kristin
    Stockholm University, Faculty of Science, Department of Zoology.
    Nesting ecology of the grass snake (Natrix natrix) and its implications for conservation2016Doctoral 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.  

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  • 6.
    Löwenborg, Kristin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Hagman, Mattias
    Stockholm University, Faculty of Science, Department of Zoology.
    How a thermal dichotomy in nesting environments influences offspring of the world's most northerly oviparous snake, Natrix natrix (Colubridae)2012In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 107, no 4, p. 833-844Article in journal (Refereed)
    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.

  • 7.
    Löwenborg, Kristin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Hagman, Mattias
    Stockholm University, Faculty of Science, Department of Zoology.
    Scale asymmetries and lateral rib duplication in snakes: correlates and effects on locomotor performance2017In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 120, no 1, p. 189-194Article in journal (Refereed)
    Abstract [en]

    Thermally-induced scale asymmetries in reptiles are often considered to be indicative of underlying osteological deformities that incur fitness costs. However, this typically rests on subjective plausibility arguments and anecdotal reports about links between deformities and fitness, as well as between superficial asymmetries and deeper deformities rather than on empirical data. To shed light on these issues, we used a combination of Xrays of museum specimens and locomotor performance trials of hatchlings grass snakes (Natrix natrix) incubated in the laboratory at either 25 degrees C or 31 degrees C. We found that 30% of the museum specimens with asymmetrical ventral scales also had a rib duplication on one side of the underlying vertebrae associated with a scale asymmetry. In some cases, there was also a second extra rib on the opposite side of the vertebrae. However, although there was a statistically significant association between asymmetric ventral scales and rib duplication, a relatively weak correlation coefficient (r(s) = 0.35) indicated that scale asymmetries are not a very strong predictor of rib duplication. In the performance trials, scale asymmetries had a significant effect on terrestrial but not aquatic locomotor ability of the hatchlings, and the magnitude of this effect depended on the temperature regimes that they experienced as embryos during incubation. Although both asymmetrical and normal snakes incubated at the higher temperature had more stamina than their respective counterparts incubated at the lower temperature, asymmetrical hatchlings overall became exhausted much sooner than normal snakes across the two treatments.

  • 8.
    Löwenborg, Kristin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kärvemo, Simon
    Hagman, Mattias
    Stockholm University, Faculty of Science, Department of Zoology.
    Snokens vanor kartläggs2009In: Fauna och Flora, ISSN 0014-8903, Vol. 104, no 2, p. 42-45Article in journal (Other (popular science, discussion, etc.))
  • 9.
    Löwenborg, Kristin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kärvemo, Simon
    Tiwe, Alma
    Stockholm University, Faculty of Science, Department of Zoology.
    Hagman, Mattias
    Stockholm University, Faculty of Science, Department of Zoology.
    Agricultural by-products provide critical habitat components for cold-climate populations of an oviparous snake (Natrix natrix)2012In: Biodiversity and Conservation, ISSN 0960-3115, E-ISSN 1572-9710, Vol. 21, no 10, p. 2477-2488Article in journal (Refereed)
    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.

  • 10.
    Löwenborg, Kristin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Shine, R.
    Hagman, Mattias
    Stockholm University, Faculty of Science, Department of Zoology.
    Fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by female grass snakes, Natrix natrix (Colubridae)2011In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 24, no 1, p. 177-183Article in journal (Refereed)
    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.

  • 11.
    Löwenborg, Kristin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Shine, Richard
    Kärvemo, Simon
    Hagman, Mattias
    Stockholm University, Faculty of Science, Department of Zoology.
    Grass snakes exploit anthropogenic heat sources to overcome distributional limits imposed by oviparity2010In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 24, no 5, p. 1095-1102Article in journal (Refereed)
    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.

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