Marine subsidies change short-term foraging activity and habitat utilization of terrestrial lizards

Abstract

Resource pulses are brief periods of unusually high resource abundance. While population and community responses to resource pulses have been relatively well studied, how individual consumers respond to resource pulses has received less attention. Local consumers are often the first to respond to a resource pulse, and the form and timing of individual responses may influence how the effects of the pulse are transmitted throughout the community. Previous studies in Bahamian food webs have shown that detritivores associated with pulses of seaweed wrack provide an alternative prey source for lizards. When seaweed is abundant, lizards (Anolis sagrei) shift to consuming more marine-derived prey and increase in density, which has important consequences for other components of the food web. We hypothesized that the diet shift requires individuals to alter their habitat use and foraging activity and that such responses may happen very rapidly. In this study, we used recorded video observations to investigate the immediate responses of lizards to an experimental seaweed pulse. We added seaweed to five treatment plots for comparison with five control plots. Immediately after seaweed addition, lizards decreased average perch height and increased movement rate, but these effects persisted for only 2 days. To explore the short-term nature of the response, we used our field data to parametrize heuristic Markov chain models of perch height as a function of foraging state. These models suggest a “Synchronized-satiation Hypothesis,” whereby lizards respond synchronously and feed quickly to satiation in the presence of a subsidy (causing an initial decrease in average perch height) and then return to the relative safety of higher perches. We suggest that the immediate responses of individual consumers to resource pulse events can provide insight into the mechanisms by which these consumers ultimately influence community-level processes.

REFERENCES Abrams, P. A., & Matsuda, H. (1996). Positive indirect effects between prey species that share predators. Ecology, 77, 610–616. https://doi.org/10.2307/2265634 Bates, D., Maechler, M., & Bolker, B. (2014). lme4: Linear mixed-effects models using Eigen and S4. R Package Version, 1, 1–23. Beckerman, A. P., Uriarte, M., & Schmitz, O. J. (1997). Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. Proceedings of the National Academy of Sciences, 94, 10735–10738. https://doi.org/10.1073/pnas.94.20.10735 Bergeron, P., Réale, D., Humphries, M. M., & Garant, D. (2011). Anticipation and tracking of pulsed resources drive population dynamics in eastern chipmunks. Ecology, 92, 2027–2034. https://doi.org/10.1890/11-0766.1 Colombini, I., Chelazzi, L., Gibson, R. N., & Atkinson, R. J. A. (2003). Influence of marine allochthonous input on sandy beach communities. Oceanography and Marine Biology: An Annual Review, 41, 115–159. Cooper Jr, W. E. (2005). Duration of movement as a lizard foraging movement variable. Herpetologica, 61, 363–372. https://doi.org/10.1655/04-36.1 Crawley, M. J. (2007). The R book, 2nd ed. West Sussex, UK: John Wiley and Sons. https://doi.org/10.1002/9780470515075 Curran, L., & Leighton, M. (2000). Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs, 70, 101–128. https://doi.org/10.1890/0012-9615(2000)070[0101:VRTSVI]2.0.CO;2 Dugan, J. E., Hubbard, D. M., McCrary, M. D., & Pierson, M. O. 2003. The response of macrofauna communities and shorebirds to macrophyte wrack subsidie on exposed sandy beaches of southern California. Estuarine, Coastal, and Shelf Science, 58S:25–40. https://doi.org/10.1016/S0272-7714(03)00045-3 Epanchin, P. N., Knapp, R. A., & Lawler, S. P. (2010). Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. Ecology, 91, 2406–2415. https://doi.org/10.1890/09-1974.1 Greeff, J. M., & Whiting, M. J. (2000). Foraging-mode plasticity in the lizard Platysaurus broadleyi. Herpetologica, 56, 402–407. Kirkman, H., & Kendrick, G. A. (1997). Ecological significance and commercial harvesting of drifting and beach-cast macro-algae and seagrasses in Australia: A review. Journal of Applied Phycology, 9, 311–326. https://doi.org/10.1023/A:1007965506873 Lapiedra, O., Chejanovski, Z., & Kolbe, J. J. (2017). Urbanization and biological invasion shape animal personalities. Global Change Biology, 23, 592–603. https://doi.org/10.1111/gcb.13395 Lister, B. C., & Garcia Aguayo, A. (1992). Seasonality, predation, and the behaviour of a tropical mainland anole. Journal of Animal Ecology, 61, 717–733. https://doi.org/10.2307/5626 Lopez-Darias, M., Schoener, T. W., Spiller, D. A., & Losos, J. B. (2012). Predators determine how weather affects the spatial niche of lizard prey: Exploring niche dynamics at a fine scale. Ecology, 93, 2512–2518. https://doi.org/10.1890/12-0483.1 Losos, J. B., Schoener, T. W., Langerhans, R. B., & Spiller, D. A. (2006). Rapid temporal reversal in predator-driven natural selection. Science, 314, 1111. Losos, J. B. (2009). Lizards in an evolutionary tree: Ecology and adaptive radiation of anoles. Berkeley, CA: University of California Press. McLoughlin, P. D., Lysak, K., Debeffe, L., & Perry, T. (2016). Density-dependent resource selection by a terrestrial herbivore in response to sea-to-land nutrient transfer by seals. Ecology, 97, 1929–1937. https://doi.org/10.1002/ecy.1451 Norris, A. R., & Martin, K. (2014). Direct and indirect effects of an insect outbreak increase the reproductive output for an avian insectivore and nest-cavity excavator, the red-breasted nuthatch Sitta canadensis. Journal of Avian Biology, 45, 280–290. https://doi.org/10.1111/jav.2014.45.issue-3 Ostfeld, R. S., & Keesing, F. (2000). Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends in Ecology and Evolution, 15, 232–237. https://doi.org/10.1016/S0169-5347(00)01862-0 Paterson, A. V. (1999). Effects of prey availability on perch height of female bark anoles, Anolis distichus. Herpetologica, 55, 242–247. Piovia-Scott, J., Spiller, D. A., & Schoener, T. W. (2011). Effects of experimental seaweed deposition on lizard and ant predation in an island food web. Science, 331, 461–463. https://doi.org/10.1126/science.1200282 Piovia-Scott, J., Spiller, D. A., Takimoto, G., Yang, L. H., Wright, A. N., & Schoener, T. W. (2013). The effect of chronic seaweed subsidies on herbivory: Plant-mediated fertilization pathway overshadows lizard-mediated predator pathways. Oecologia, 172, 1129–1135. https://doi.org/10.1007/s00442-012-2560-0 Polis, G. A., Anderson, W. B., & Holt, R. D. (1997). Toward an integration of landscape and food web ecology: The dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics, 28, 289–316. https://doi.org/10.1146/annurev.ecolsys.28.1.289 R Core Team (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Rose, M. D., & Polis, G. A. (1998). The distribution and abundance of coyotes: The effects of allochthonous food subsidies from the sea. Ecology, 79, 998–1007. https://doi.org/10.1890/0012-9658(1998)079[0998:TDAAOC]2.0.CO;2 Schmidt, K. A., & Ostfeld, R. S. (2008). Numerical and behavioral effects within a pulse-driven system: Consequences for shared prey. Ecology, 89, 635–646. https://doi.org/10.1890/07-0199.1 Schmitz, O. J. (2005). Behavior of predators and prey and links with population level processes. In P. Barbosa & I. Castellanos (Eds.), Ecology of predator-prey interactions (pp. 256–278). New York, NY: Oxford University Press. Schmitz, O. J., Beckerman, A. P., & O'Brien, K. M. (1997). Behaviorally mediated trophic cascades: Effects of predation risk on food web interactions. Ecology, 78, 388–1399. Schmitz, O. J., Krivan, V., & Ovadia, O. (2004). Trophic cascades: The primacy of trait-mediated indirect interactions. Ecology Letters, 7, 153–163. https://doi.org/10.1111/ele.2004.7.issue-2 Schoener, T. W. (1967). The ecological significance of sexual dimorphism in size in the lizard Anolis conspersus. Science, 155, 474–477. https://doi.org/10.1126/science.155.3761.474 Schoener, T. W. (1968). The Anolis lizards of Bimini: Resource partitioning in a complex fauna. Ecology, 49, 704–726. https://doi.org/10.2307/1935534 Schoener, T. W. (1979). Feeding, spacing, and growth in the four species of Bimini Anolis lizards. National Geographic Society research reports, 1970 projects (pp 479–485). Washington D.C: NGS. Schoener, T. W., & Spiller, D. A. (2012). Kinds of trait-mediated indirect effects in ecological communities: In a synthesis. In T. Ohgushi, O. Schmitz & R. D. Holt (Eds.), Ecology and evolution of trait-mediated indirect interactions: Linking evolution, community, and ecosystems (pp. 9–27). Cambridge, UK: Cambridge University Press. https://doi.org/10.1017/CBO9780511736551 Schoener, T. W., Spiller, D. A., & Losos, J. B. (2002). Predation on a common Anolis lizard: Can the foodweb effects of a devastating predator be reversed? Ecological Monographs, 72, 383–407. https://doi.org/10.1890/0012-9615(2002)072[0383:POACAL]2.0.CO;2 Scott, N. J., Wilson, D. E., Jones, C., & Andrews, R. M. (1976). The choice of perch dimensions by lizards of the genus Anolis (Reptilia, Lacertilia, Iguanidae). Journal of Herpetology, 10, 75–84. https://doi.org/10.2307/1562787 Spedicato, G. (2015). Markovchain: Discrete time Markov chains made easy. R package version 0.3.0.1. Spiller, D. A., Piovia-Scott, J., Wright, A. N., Yang, L. H., Takimoto, G., Schoener, T. W., & Iwata, T. (2010). Marine subsidies have multiple effects on coastal food webs. Ecology, 91, 1424–1434. https://doi.org/10.1890/09-0715.1 Stamps, J. A. (1977). The function of the survey posture in Anolis lizards. Copeia, 1977, 756–758. https://doi.org/10.2307/1443181 Stamps, J. A., & Tanaka, S. (1981). The relationship between food and social behavior in juvenile lizards (Anolis aeneus). Copeia, 1981, 422–434. https://doi.org/10.2307/1444233 Stewart, D. T., Herman, T. B., & Teferi, T. (1989). Littoral feeding in a high-density insular population of Sorex cinereus. Canadian Journal of Zoology, 67, 2074–2077. https://doi.org/10.1139/z89-295 Takimoto, G., Iwata, T., & Murakami, M. (2009). Timescale hierarchy determines the indirect effects of fluctuating subsidy inputs on in situ resources. The American Naturalist, 173, 200–211. https://doi.org/10.1086/595759 Werner, E. E., & Peacor, S. D. (2003). A review of trait-mediated indirect interactions in ecological communities. Ecology, 84, 1083–1100. https://doi.org/10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2 Wright, A. N., Piovia-Scott, J., Spiller, D. A., Takimoto, G., Yang, L. H., & Schoener, T. W. (2013). Pulses of marine subsidies amplify reproductive potential of lizards by increasing individual growth rate. Oikos, 122, 1496–1504. Yang, L. H., Bastow, J. L., Spence, K. O., & Wright, A. N. (2008). What can we learn from resource pulses? Ecology, 89, 621–634. https://doi.org/10.1890/07-0175.1 Yang, L. H., Edwards, K., Byrnes, J. E., Bastow, J. L., Wright, A. N., & Spence, K. O. (2010). A meta-analysis of resource pulse-consumer interactions. Ecological Monographs, 80, 125–151. https://doi.org/10.1890/08-1996.1