Landscape Genetics (M1, M3); Le Lay, Angelone, Holderegger, Flory, Kienast, Bolliger 13
The role of management intervention in enhancing breeding- habitat networks in the European tree frog
Gwenaëlle Le Lay1, Sonia Angelone1,3 Rolf Holderegger1, Christoph Flory2, Felix Kienast1, Janine Bolliger1
1 Swiss Federal Research Institute WSL, Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland
2 CreaNatira, Stroppelstr. 9, 5417 Untersiggenthal
3 Grün Stadt Zürich, Beatenplatz 2, 8001 Zürich
Summary
Functional connectivity in fragmented landscapes is a critical factor to facilitate movement between habi- tats and populations. Management actions which aim at fostering habitat networks are often promoted but rarely functionally evaluated. Here, we explored the number and origin of colonising individuals at newly created stepping-stone ponds for the threatened European tree frog (Hyla arborea) in the Reuss valley, Switzerland. Collecting buccal material of 85 frogs sampled at newly built stepping-stone ponds, we identified source populations of migrating frogs by means of 11 microsatellite markers. Results show that new ponds were colonized within one year, and that the number of colonising frogs increased with the new ponds’ age. Some migrating individuals originated from small or distant populations (up to 5 km), and even crossed expected barriers such as a river. The landscape in the study area appeared thus quite permeable to tree frogs. Our measures revealed that building new stepping-stone breeding ponds is an efficient and successful conservation action.
State of the art and motivation: how effective is the provisioning of stepping- stone breeding habitats for tree-frogs?
Amphibians are highly affected by human-impacted ecosystems (Stuart et al. 2004) and one third of amphibian species are threatened by extinction (Baillie et al. 2004). Main factors are the loss of habitat area and its fragmentation (Cushman 2006b; Funk et al. 2005). A few recent studies looked at de- fragmentation such as the provisioning of stepping-stone ponds (Lesbarrères et al. 2010, Le Lay et al.
submitted), however, the effectiveness of mitigation actions are difficult to measure as it remains unclear whether the individuals colonising new stepping stones stem from nearby populations or whether they form a much broader sample of individuals originating from more distant populations. Thus, detailed evaluation of the functional permeability of a landscape is crucial, in particular, as the decision on the extent and location of measures in conservation management rarely rely on organism-based functional connectivity (Lesbarrères et al. 2010). One promising tool to perform such analyses includes landscape genetics. Landscape genetics seeks to assess how ecological processes such as migration, dispersal and gene flow are affected by landscape structure and composition. The field amalgamates population genetics and landscape ecology by combining theory, concepts and methods of population genetics with the spatially dynamic framework of landscape ecology, spatial statistics and modelling (Manel et al.
2003). Landscape ecology and population genetics are both based on well-established disciplinary meth- ods. Landscape ecology assesses the relationship between spatially dynamic patterns and processes in landscapes by using statistical models including the characterization of landscape structure (e.g., suitable versus unsuitable habitats, barriers and corridors), while population genetics uses a variety of genetic techniques (e.g., AFLPs, microsatellites or SNPs) to describe the genetic structure of populations or indi- viduals. Landscape genetics thus provides a powerful tool for explaining genetic structure and gene flow based on spatially dynamic patterns and processes (Fahrig 2003; Sander et al. 2006; Cushman 2006a) and allows to identify the effects of explicit landscape properties on ecological processes.
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Genetic methods for conservation management
We applied genetic assignment tests (Manel et al. 2005) to address the role of management intervention in enhancing landscape permeability by building new stepping stone breeding ponds for the threatened European tree frog Hyla arborea L., Figs. 1–3). Genetic methods permit reliable assessments of contem- porary or recent movement directions, which allow drawing conclusions on the functional landscape con- nectivity. We benefit from a rare well documented dataset, i.e. genetic data encompassing all populations before and after the construction of new ponds. First, we identified the number of colonising frogs present in the newly built ponds which were implemented to improve the breeding-habitat network for the tree frog. Second, we identified the origins of colonising tree frogs to assess the spatial range of movement.
The Reuss valley offered a unique situation to study the geographic origin of tree frogs colonising new stepping-stone ponds in real time (Fig. 2). The study of Angelone and Holderegger (2009) provided a data set of all established tree-frog populations in the Reuss valley in 2006, i.e. before new ponds were built.
Our sampling campaign in 2009 used the 2006 data as reference to evaluate the effectiveness of newly built stepping-stone breeding ponds. In spring 2009 we sampled buccal swabs from 85 tree frogs at four new ponds for genetic analysis. We applied the same allelic scoring scheme as presented by Angelone and Holderegger (2009). In brief, DNA extraction was conducted with the DNeasy Tissue Kit (QUIAGEN), and microsatellites were amplified in four multiplexed polymerase chain reactions and analysed on a 3130 automated sequencer (Applied Biosystems). Peaks were scored using GENEMAPPER 3.7 (Applied Biosystems).
Key insight: stepping-stone ponds are a successful conservation-management strategy to foster tree-frog habitat networks
Within one to three years after construction, all newly built ponds were occupied by tree frogs. This confirms the species’ assumed strong colonization ability (Fog 1993, Lesbarrères et al. 2010) but also demonstrates that the tree-frog habitat network in the study area was already well functioning (Angelone et al. 2011). We not only found fast and abundant colonisation of new ponds, results also showed that the age of the new ponds mattered as the oldest newly created pond exhibited the largest amount of new colonizers. Colonizing individuals originated from populations at distances of up to 5 km, with 50 % of the first generation migrants originating from source populations at distances of less than 2 km. Thus, the landscape of the Reuss valley appears to be generally well permeable for tree frogs. As the number of colonising frogs increased during the first years of the pond creation, and as these frogs come from a large variety of population sources, we conclude that the provisioning of new stepping-stone breeding ponds is a successful conservation strategy to increase the number of breeding sites and to enhance the gene flow between tree-frog populations. The so supplemented habitat network de-centralizes individual habitat importance which leads to an increased resilience of the entire habitat network (Bolliger et al., in prep).
Fig. 1. The European tree-frog (Hyla arborea); © Gwenaëlle Le Lay.
Landscape Genetics (M1, M3); Le Lay, Angelone, Holderegger, Flory, Kienast, Bolliger 15
Fig. 2. Tree-frog sampling sites in the Reuss valley, Switzerland; © Gwenaëlle Le Lay.
Fig. 3. Newly created stepping-stone breeding habitats for the tree frog in the Reuss valley, Switzerland;
© Christoph Flory.
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References
Angelone, S. & Holderegger, R. (2009) Population genetics suggests effectiveness of habitat connectivity measures for the European tree frog in Switzerland. Journal of Applied Ecology, 46: 879–887.
Angelone, S., Kienast, F. & Holderegger, R. (2011) Where movement happens: scale-dependent landscape effects on genetic differentiation in the European tree frog. Ecography, 34: 714–722.
Baillie, J. E. M., Hilton-Taylor, C. & Stuart, S. N. (2004) Red List of threatened species. A global species assessment. IUCN, Gland, Switzerland and Cambridge, UK.
Bolliger, J., Angelone, S., Le Lay, G., Flory, C. & Holderegger, R. (in prep) Importance of habitat and connectivity in tree-frog breeding networks. Molecular Ecology.
Cushman, S. A. (2006a) Effects of habitat loss and fragmentation on amphibians: a review and prospects. Biological Con- servation, 128: 231–240.
Cushman, S. A. (2006b) Effects of habitat loss and fragmentation on amphibians: A review and prospectus. Biological Conservation, 128: 231–240.
Fahrig, L. (2003) Effects of habitat fragmentation on biodiversity. Annual Review of Ecology and Evolution, 34: 487–515.
Fog, K. (1993) Migration in the tree frog Hyla arborea. Ecology and Conservation of the European Tree Frog (eds A. H. P.
Stumpel & U. Tester), pp. 55–64. Institute for Forestry and Nature Research, Wageningen.
Funk, W. C., Blouin, M. S., Corn, P. S., Maxell, B. A., Pilliod, D. S., Amish, S. & Allendorf, F. W. (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Molecular Ecology Resources, 14:
483–496.
Le Lay, G., Angelone, S., Holderegger, R., Flory, C. & Bolliger, J. (submitted) The role of management intervention in en- hancing breeding-habitat networks in the European tree frog. Conservation Biology.
Lesbarrères, D., Fowler, M. S., Pagano, A. & Lode, T. (2010) Recovery of anuran community diversity following habitat replacement. Journal of Applied Ecology, 47: 148–156.
Manel, S., Gaggiotti, O. E. & Waples, R. S. (2005) Assignment methods: matching biological questions techniques with appropriate. Trends In Ecology & Evolution, 20: 136–142.
Manel, S., Schwartz, M., Luikart, G. & Taberlet, P. (2003) Landscape genetics: combining landscape ecology and population genetics. Trends in Ecology and Evolution, 18: 189–197.
Sander, A.-C., Purtauf, T., Holzhauer, I. J. & Wolters, V. (2006) Landscape effects on the genetic structure of the ground beetle Poecilus versicolor STURM 1824. Landscape Ecology, 15: 245–259.
Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L. & Waller, R. W. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306: 1783–1786.
