Barnum Et Al. 2013 (Tropical Ecology)

Journal of Tropical Ecology (2013) 29:291–299. © Cambridge University Press 2013 doi:10.1017/S026646741300028X Use of stable isotope ratios to characterize potential shifts in the isotopic niches of grazing insects following an amphibian decline in a Neotropical stream ,1 Thomas R. Barnum∗ ,PietVerburg ,SusanS.Kilham ,MattR.Whiles ,KarenR.Lips∗∗, † ‡ § Checo Colon-Gaud´ and Catherine M. Pringle∗ †† ∗ Odum School of Ecology, University of Georgia, Athens, GA, USA National Institute of Water and Atmospheric Research, Hamilton, New Zealand † Department of Biodiversity, Earth and Environmental Science, Drexel University, Philadelphia, PA, USA ‡ Department of Zoology and Center for Ecology, Southern Illinois University, Carbondale, IL, USA § ∗∗ Department of Biology, University of Maryland, College Park, MD, USA Department of Biology, Georgia Southern University, Statesboro, GA, USA †† (Received 26 September 2012; revised 25 April 2013; accepted 25 April 2013; first published online 23 May 2013) Abstract: Neotropical streams are losing dominant consumer groups as a result of disease-driven amphibian declines. The herbivorous tadpoles of Lithobates warszewitschii were once abundant in the Rio Maria in the Eastern Cordillera Central of Panama, where they consumed algae and organic matter. The decline of this once abundant grazer has the potential to affect the resources consumed by insect grazers in this system. Stable isotopes were used to characterize changes in the resource use before and after amphibian declines of four abundant insect grazer taxa: Stenonema spp., Thraulodes spp., Psephenus spp. and Petrophila spp. We collected 11 isotope samples of L. warszewitschii and 27 isotope samples of these insect taxa in 2006, and then 24 more isotope samples of the same insect taxa in 2008, 20 mo. after a disease-driven amphibian extirpation. We also tested for potential functional redundancy of insects with tadpoles by comparing the post-decline isotopic niche of each insect taxon to the isotopic niche of L. warszewitschii. The isotopic niche of Psephenus spp., Petrophila spp. and Stenonema spp. shifted from 2006 to 2008, but none of the insect taxa in 2008 occupied the same isotopic niche as tadpoles. Our study builds on previous evidence that the ecological roles of tadpoles were not replaced through functional redundancy after amphibian declines. Key Words: amphibian declines, chytrid, emerging infectious disease, functional redundancy, isotopic niches, species loss, stable isotopes, tropical streams INTRODUCTION variation in δ15N and δ13Cofindividualsinapopulation can be used to characterize the δ space (or isotopic niche) Ecosystems worldwide are facing unprecedented biod- of the whole population (Bearhop et al. 2004, Bolnick et al. iversity declines (Pereira et al. 2010). Efforts to 2003). Layman et al. (2007) proposed using the convex understand biodiversity losses generally focus on hull and the mean distance to centroid to describe the ecosystem descriptors such as changes in species size and location of the isotopic niche of a population. The abundancesandcommunitycomposition.Characterizing convexhullencompassesthedatapointsofthepopulation changes in energy flow or resource use is more difficult and gives an indication of the isotopic niche width of and consequently is usually neglected. The ratio of the that population while the mean distance to centroid stable isotopes of nitrogen (15N) and carbon (13C) can be gives information on how similar two populations are useful tools for integrating temporal data to characterize in isotopic space. Recently, methods to statistically test the trophic level (δ15N) and energy source (δ13C) of an for differences in the location in isotopic space of a single individual or a population (Newsome et al. 2007). The population over time, or between two populations, were developed (Jackson et al. 2011, Turner et al.2010). Stable isotopes have been used to examine community 1 Corresponding author. Email: [email protected] responses to species invasion (Nilsson et al. 2012, Vander 292 THOMAS R. BARNUM ET AL. Zanden & Casselman 1999), but not the opposite, 2% of their pre-decline biomass by February 2008 (Whiles species extirpations. Catastrophic amphibian declines et al. 2012). The remaining consumer community occurringinCentralAmericacanpotentiallyaffectstream includes an insectivorous fish (Brachyraphis roswithae ecosystems (Whiles et al. 2006). Tadpoles consume algae Meyer & Etzel), the freshwater crab Pseudothelphusa and detritus and may thus compete with grazing insects tristani Rathburn and 40 aquatic insect taxa that (Kupferburg 1997), but they can also facilitate access were common in the headwater∼ streams pre- and post- to these resources for some grazing insects through amphibian decline. bioturbation (Ranvestel et al. 2004). Therefore, the extirpation of grazing tadpoles could potentially affect access to the resources consumed by grazing insects, Sampling of insect biomass and resources with the consequences manifested through changes in the carbon and nitrogen isotopic ratios in the grazing Insects were sampled pre-decline (February and March insects. 2006)andpost-decline(FebruaryandMarch2008)along As part of the Tropical Amphibian Declines in the same 100-m reach. Samples were collected during Streams (TADS) project, we used invertebrate samples the dry season because insect biomass and abundance in collected from a Panamanian stream before and after Neotropical streams are highest during the dry season tadpole declines to provide a snapshot of the potential (Colon-Gaud´ et al.2010a).Threestove-pipebenthic consequences of tadpole declines on the isotopic niches cores (314 cm2 sampling area) were collected from and energy sources of four grazing insect taxa. We depositional habitats (pools) and four Surber samples also examined the potential for these grazing insects (930 cm2 sampling area, 250-µm mesh) were collected to replace the ecological role of the dominant grazing from erosional habitats (riffles and runs). All samples were tadpole Lithobates warszewitschii. We measured biomass elutriated through a 250-µm sieve and placed in a bag and examined the diet (using stable isotopes ratios and with 8% formalin. In the laboratory, all insects from gut content analysis) of the four grazing insect taxa and coarse∼ fractions (insects with a body length > 1mm) L. warszewitschii and measured the C and N stable isotope were removed and identified to genus. Fine fractions ratios of the epilithon. Post-decline isotopic niches of (insects with a body length between < 1mm> 250 µm) the grazing insects were compared with the pre-decline were also examined under a dissecting microscope and isotopic niche of tadpoles to determine if grazing insects were occasionally subsampled (from 1/2 to 1/32) with a occupied a similar isotopic niche to tadpoles after the Folsom plankton splitter. decline. We predicted that grazing insects would change Taxa were classified into functional feeding groups diets to include more diatoms in the absence of tadpoles, (FFG) based on Merritt et al. (2008) and previous natural and that at least one grazing insect taxon in 2008 would abundance stable isotope data (Verburg et al. 2007). occupy the same isotopic niche as tadpoles from 2006. Individual insects were measured (total body length) and biomass was estimated using published ash-free dry mass (AFDM) length-mass regressions (Benke et al. MATERIALS AND METHODS 1999) or regressions developed from our own specimens using methods of Benke et al.(1999).TheAFDMwas Study site then summed on each sampling date to obtain taxon- specific biomass estimates, which were then habitat R´ıo Maria is a headwater stream near El Valle de Anton weighted according to the proportion of each habitat in the eastern Cordillera Central of Panama. R´ıo Maria is during base flow conditions (64% riffle/run, 36% pool). ahigh-gradientstreamat 900 m asl with an average Biomass estimates from 2006 (pre-decline) and 2008 wetted width of 3.5 m during∼ the dry season (January to (post-decline) of grazing insect taxa were analysed using mid-May). Stream flow did not significantly differ between anon-parametricbootstrap.Teststatisticswerethe the 2006 and 2008 dry seasons (mean 1SD 22.4 differences between 2006 and 2008 means. The means 1 ±1 = ± 2.9 L s− in 2006 and 22.9 2.4 L s− in 2008). The were compared to permuted means of the pooled 2006 site remained undisturbed between± sampling events, but and 2008 data which were resampled 10 000 times. P within 6 mo of our 2008 sampling event a small dam was values were the percentage of permuted differences that built and a construction project in the middle of the study lay outside the test statistic with P < 0.05 considered reach prevented a second post-decline sampling event. significant. Four grazing insect taxa, Stenonema The tadpoles of more than 20 species were present in spp. (Ephemeroptera: Heptageniidae), Thraulodes spp. the pre-decline amphibian assemblage, including grazing (Ephemeroptera: Leptophlebiidae), Psephenus spp. (Cole- Hyloscirtus spp. and Lithobates warszewitschii. Amphibian optera: Psephenidae) and Petrophila spp. (Lepidoptera: declines occurred at R´ıo Maria during the 2006 wet- Crambidae), were selected for stable isotope and gut season (June–December) and amphibians had declined to content analysis because they constituted > 80% of the Effect of amphibian declines on grazing insects 293 grazer biomass. Immature stages of stream insects are musica Ehrenberg, would not separate from the non-algal

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