Abstract
Shifts in life history traits and in the behaviour of species can potentially alter ecosystem functioning. The reproduction of the central European fire salamander (Salamandra salamandra), which usually deposits its larvae in first-order streams, in small pool and pond-like habitats, is an example of a recent local adaptation in this species. Here we aimed to quantify the direct and indirect effects of the predatory larvae on the aquatic food webs in the ponds and on the flux of matter between the ponds and adjacent terrestrial habitats. Our estimates are based on biomass data of the present pond fauna as well as on the analysis of stomach content data, growth rates and population dynamics of the salamander larvae in pond habitats. By their deposition of larvae in early spring, female fire salamanders import between 0.07 and 2.86 g dry mass m−2 larval biomass into the ponds. Due to high mortality rates in the larval phase and the relatively small size at metamorphosis of the pond-adapted salamanders compared to stream-adapted ones, the biomass export of the metamorphosed salamanders clearly falls below the initial biomass import. Catastrophic events such as high water temperatures and low oxygen levels may even occasionally result in mass mortalities of salamander larvae and thus in a net 100 % import of the salamander biomass into the pond food webs. Indirect effects further accelerate this net import of matter into the aquatic habitat, e.g. the feeding of salamanders on aquatic insect larvae with the emergence of terrestrial adults—thus preventing export—and on terrestrial organisms that fall on the water surface (supporting import). This study demonstrates that the adaptation of salamanders to pond reproduction can alter food web linkages across ecosystem boundaries by enhancing the flux of materials and energy from terrestrial (i.e. forest) to the aquatic (i.e. pond) habitat.
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Allan JD, Wipfli MS, Caouette JP, Prussian A, Rodgers J (2003) Influence of streamside vegetation on inputs of terrestrial invertebrates to salmonid food webs. Can J Fish Aquatic Sci 60:309–320
Altig R, Whiles MR, Taylor CL (2007) What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshwater Biol 52:386–395
Bassar RD, Marshall MC, López-Sepulcre A, Zandora E, Auer SK, Travis J, Pringle CM, Flecker AS, Thomas SA, Fraser DF, Reznick DN (2010) Local adaption in Trinidadian guppies alters ecosystem processes. PNAS 23:3616–3621
Bassar RD, Ferriere R, Lopéz-Sepulcre A, Marshall MC, Travis J, Pringle CM, Reznick DN (2012) Direct and indirect ecosystem effects of evolutionary adaption in the Trinidadian guppy (Poecilia reticulata). Am Nat 180:167–185
Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshwater Biol 50:201–220
Benke AC, Huryn AD, Schmock LA, Wallace JB (1999) Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeast United States. J N Am Benthol Soc 18:308–343
Blaustein L, Friedman J, Fahima T (1996) Larval Salamandra drive temporary pool community dynamics: evidence from an artificial pool experiment. Oikos 76:392–402
Burton TM, Likens GE (1975) Energy flow and nutrient cycling in salamander populations in the Hubbard Brook experimental forest, New Hampshire. Ecology 56:1068–1080
Cooper SD, Walde SJ, Peckarsky BL (1990) Prey exchange rates and the impact of predators on prey populations in streams. Ecology 71:1503–1514
Crump ML (1979) Intra-population variability in energy parameters of the salamander Plethodon cinereus. Oecologia 38:235–247
Denoël M (2004) Feeding performance in heterochronic alpine newts is consistent with trophic niche and maintenance of polymorphism. Ethology 110:127–136
Denoël M, Joly P (2001) Adaptive significance of facultative paedomorphosis in Triturus alpestris (Amphibia, Caudata): resource partitioning in an alpine lake. Freshwater Biol 48:1387–1396
Dumont HJ, Vandevelde I, Dumont S (1975) Dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from plankton, periphyton and benthos of continental waters. Oecologia 19:75–97
Gasche P (1938) Beitrag zur Kenntnis der Entwicklung von Salamandra salamandra L. mit besonderer Berücksichtigung der Winterphase, der Metamorphose und des Verhaltens der Schilddrüse (Glandula thyreoidea). Rev Suisse Zool 46:403–548
Greven H (1998) Survey of the oviduct of salamandrids with special reference to the viviparous species. J Exp Zool 282:507–525
Hansen K, Vesterdal L, Kappel Schmidt I, Grundersen P, Sevel L, Bastrup-Birk A, Pedersen LB, Bille-Hansen J (2009) Litterfall and nutrient return in five tree species in a common garden experiment. For Ecol Manage 257:2133–2144
Harmon LJ, Matthews B, Des Roches S, Chase JM, Shurin JB, Schluter D (2009) Evolutionary diversification in sticklebacks affects ecosystem functioning. Nature 458:1167–1170
Holomuzki JR, Collins JP, Brunkow PE (2004) Trophic control of fishless ponds by tiger salamander larvae. Oikos 71:55–64
Johnson BR, Wallace JB (2005) Bottom-up limitation of a stream salamander in a detritus-based food web. Can J Fish Aquatic Sci 62:301–311
Kawaguchi Y, Taniguchi Y, Nakano S (2003) Terrestrial invertebrate inputs determine the local abundance of stream fishes in a forested stream. Ecology 84:701–708
Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883
Kraus J, Pletcher LT, Vonesh JR (2011) Variation in active and passive resource inputs to experimental pools: mechanisms and possible consequences for food webs. Freshwater Biol 56:491–502
Lebret M, Nys C, Forgeard F (2001) Litter production in an atlantic beech (Fagus sylvatica L.) time sequence. Ann For Sci 58:755–768
Leroux SJ, Loreau M (2008) Subsidy hypothesis and strength of trophic cascades across ecosystems. Ecol Lett 11:1147–1156
Manenti R, Ficetola GF, Marieni A, De Bernardi F (2011) Caves as breeding sites for Salamandra salamandra: habitat selection, larval development and conservation issues. Northwest J Zool 7:304–309
Mehner T, Ihlau J, Dorner H, Holker F (2005) Can feeding of fish on terrestrial insects subsidize the nutrient pool of lakes? Limnol Oceanogr 50:2022–2031
Murakami M, Nakano S (2001) Species-specific foraging behaviour of birds in a riparian forest. Ecol Res 15(5):913–922
Paetzold A, Schubert CJ, Tockner K (2005) Aquatic terrestrial linkages along a Braided-river: riparian arthropods feeding on aquatic insects. Ecosystems 8:748–759
Paetzold A, Smith M, Warren P, Maltby L (2011) Environmental impact propagated by cross-system subsidy: chronic stream pollution controls riparian spider populations. Ecology 92:1711–1716
Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316
Post DM, Palkovacs EP (2009) Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Phil Trans R Soc B 364:1629–1640
Post DM, Doyle MW, Sabo JL, Finlay J (2007) The problem of boundaries in defining ecosystems: a potential landmine for uniting geomorphology and ecology. Geomorphology 89:111–126
Ranvestel AW, Lips KR, Pringle CM, Whiles MR, Bixby RJ (2004) Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshwater Biol 49:274–285
Regester KJ, Lips KR, Whiles MR (2006) Energy flow and subsidies associated with the complex life cycle of ambystomatid salamanders in ponds and adjacent forest in southern Illinois. Oecologia 147:303–314
Regester KJ, Whiles MR, Lips KR (2008) Variation in the trophic basis of production and energy flow associated with emergence of larval salamander assemblages from forest ponds. Freshwater Biol 53:1754–1767
Rogers LE, Hinds WT, Buschbom RL (1976) General weight vs. length relationship for Insects. Ann Entomol Soc Am 69:387–389
Rogers LE, Buschbom RL, Watson CR (1977) Length-weight relationship of shrub-steppe invertebrates. Ann Entomol Soc Am 70:51–53
Sabo JL, Power ME (2002) Numerical response of lizards to aquatic insects and short-term consequences for terrestrial prey. Ecology 83:3023–3036
Schlüpmann M, Henf M, Geiger A (1995) Kescher für den Amphibienfang. Z Feldherpetol 2:227–229
Schreiber S, Rudolf VHW (2008) Crossing habitat boundaries: coupling dynamics of ecosystems through complex life cycles. Ecol Lett 11:576–587
Seale DB (1980) Influence of amphibian larvae on primary production, nutrient flux and competition in a pond ecosystem. Ecology 61:1531–1550
Steinfartz S, Vicario S, Arntzen JW, Caccone A (2007a) A Bayesian approach on molecuales and behavior: reconsidering phylogenetic and evolutionary patterns of the Salamandridae with emphasis on Triturus newts. J Exp Zool (Mol Dev Evol) 308B:139–162
Steinfartz S, Weitere M, Tautz D (2007b) Tracing the first step to speciation: ecological and genetic differentiation of a salamander population in a small forest. Mol Ecol 16:4550–4561
Straile D (1997) Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence on food concentration, predator-prey weight ratio, and taxonomic group. Limnol Oceanogr 42:1375–1385
Thiesmeier B (1992) Ökologie des Feuersalamanders, 1st edn. Westarp, Essen
Thiesmeier B (2004) Der Feuersalamander, 1st edn. Laurenti, Bielefeld
Verburg P, Kilham SS, Pringle CM, Lips KR, Drake DL (2007) A stable isotope study of a Neotropical stream food web prior to the extirpation of its large amphibian community. J Trop Ecol 23:643–651
Walls SC, Williams MG (2001) The effect of community composition on persistence of prey with their predators in an assemblage of pond-breeding amphibians. Oecologia 128:134–141
Weitere M, Tautz D, Neumann D, Steinfartz S (2004) Adaptive divergence vs. environmental plasticity: tracing local genetic adaptation of metamorphosis traits in salamanders. Mol Ecol 13:1665–1677
Youngs WD, Robson DS (1978) Estimation of population number and mortality. In: Beagenal T (ed) Methods of assessment of fish production in fresh waters, 1st edn. Blackwell, Oxford
Acknowledgments
The study was supported by a scholarship of the Deutsche Bundesstiftung Umwelt (DBU) to TR. This research was possible with the kind permission of the governmental forestry office in Bonn and the Nature Reserve Authority Erftkreis and Overath who granted the necessary permission for access and sampling of salamander larvae and invertebrates. We thank Frederic Bartlett, Andrew Kaus and Amy MacLeod for linguistic improvement of the manuscript and Dietrich Neumann for supporting the initial study.
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Communicated by Robert Hall.
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Reinhardt, T., Steinfartz, S., Paetzold, A. et al. Linking the evolution of habitat choice to ecosystem functioning: direct and indirect effects of pond-reproducing fire salamanders on aquatic-terrestrial subsidies. Oecologia 173, 281–291 (2013). https://doi.org/10.1007/s00442-013-2592-0
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DOI: https://doi.org/10.1007/s00442-013-2592-0