Advertisement

Oecologia

, Volume 189, Issue 3, pp 803–813 | Cite as

Warming-induced shifts in amphibian phenology and behavior lead to altered predator–prey dynamics

  • Fabian G. JaraEmail author
  • Lindsey L. Thurman
  • Pierre-Olivier Montiglio
  • Andrew Sih
  • Tiffany S. Garcia
Community ecology – original research

Abstract

Climate change-induced phenological variation in amphibians can disrupt time-sensitive processes such as breeding, hatching, and metamorphosis, and can consequently alter size-dependent interactions such as predation. Temperature can further alter size-dependent, predator–prey relationships through changes in species’ behavior. We thus hypothesized that phenological shifts due to climate warming would alter the predator–prey dynamic in a larval amphibian community through changes in body size and behavior of both the predator and prey. We utilized an amphibian predator–prey system common to the montane wetlands of the U.S. Pacific Northwest: the long-toed salamander (Ambystoma macrodactylum) and its anuran prey, the Pacific chorus frog (Pseudacris regilla). We conducted predation trials to test if changes in predator phenology and environmental temperature influence predation success. We simulated predator phenological shifts using different size classes of the long-toed salamander representing an earlier onset of breeding while using spring temperatures corresponding to early and mid-season larval rearing conditions. Our results indicated that the predator–prey dynamic was highly dependent upon predator phenology and temperature, and both acted synergistically. Increased size asymmetry resulted in higher tadpole predation rates and tadpole tail damage. Both predators and prey altered activity and locomotor performance in warmer treatments. Consequently, behavioral modifications resulted in decreased survival rates of tadpoles in the presence of large salamander larvae. If predators shift to breed disproportionately earlier than prey due to climate warming, this has the potential to negatively impact tadpole populations in high-elevation amphibian assemblages through changes in predation rates mediated by behavior.

Keywords

Ambystoma Pseudacris Temperature Behavior Size mismatch 

Notes

Acknowledgements

This research was founded by a research fellowship from the National Scientific and Technical Research Council Argentina (CONICET). M. Perotti and M. Diéguez helped develop the fellowship project. We would also like to thank the Department of Environmental Science and Policy at the University of California at Davis for support for this project and the Department of Fisheries and Wildlife at Oregon State University for providing the temperature-controlled facilitates. Thanks to J. Urbina and E. Bredeweg for their assistance in the field and experimental work. We thank two anonymous reviewers for constructive comments on an earlier draft of this study. Animals were collected under Oregon Department of Fisheries and Wildlife Special Use Permit no. 025-15 and Oregon State University Animal Care and Use Protocol no. 4356.

Author contribution statement

FJ, AS, TG originally formulated the idea; FJ, LT, TG developed methodology; FJ, LT conducted fieldwork; FJ, PM, LT performed statistical analyses; FJ, LT, PM, TG and AS wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2019_4360_MOESM1_ESM.docx (182 kb)
Supplementary material 1 (DOCX 181 kb)

References

  1. Adrian R, O’Reilly CM, Zagarese H, Baines SB, Hessen DO, Keller W, Livingstone DM, Sommaruga R, Straile D, Van Donk E, Weyhenmeyer GA, Winder M (2009) Lakes as sentinels of climate change. Limnol Oceanogr 54:2283–2297.  https://doi.org/10.4319/lo.2009.54.6_part_2.2283 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alford RA (1989) Variation in predator phenology affects predator performance and prey community composition. Ecology 70:206–219CrossRefGoogle Scholar
  3. Allan BJM, Domenici P, McCormick MI, Watson S-A, Munday PL (2013) Elevated CO2 affects predator–prey interactions through altered performance. PLoS One 8:e58520CrossRefPubMedPubMedCentralGoogle Scholar
  4. Allan BJM, Domenici P, Munday PL, McCormick MI (2015) Feeling the heat: the effect of acute temperature changes on predator–prey interactions in coral reef fish. Conserv Physiol.  https://doi.org/10.1093/conphys/cov011 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Arnell NW, Reynard NS (1996) The effects of climate change due to global warming on river flows in Great Britain. J Hydrol 183:397–424CrossRefGoogle Scholar
  6. Arrighi JM, Lencer ES, Jukar A, Park D, Phillips PC, Kaplan RH (2013) Daily temperature fluctuations unpredictably influence developmental rate and morphology at a critical early larval stage in a frog. BMC Ecol.  https://doi.org/10.1186/1472-6785-13-18 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bancroft BA, Baker NJ, Searle CL, Garcia TS, Blaustein AR (2008) Larval amphibians seek warm temperatures and do not avoid harmful UVB radiation. Behav Ecol 19:879–886.  https://doi.org/10.1093/beheco/arn044 CrossRefGoogle Scholar
  8. Benard MF (2015) Warmer winters reduce frog fecundity and shift breeding phenology, which consequently alters larval development and metamorphic timing. Glob Change Biol 21:1058–1065.  https://doi.org/10.1111/gcb.12720 CrossRefGoogle Scholar
  9. Blair J, Wassersug RJ (2000) Variation in the Pattern of predator-induced damage to tadpole tails. Copeia 2:390–401.  https://doi.org/10.1643/00458511(2000)000%5b0390:vitpop%5d2.0.co;2 CrossRefGoogle Scholar
  10. Blaustein AR, Walls SC, Bancroft BA, Lawler JJ, Searle CL, Gervasi SS (2010) Direct and indirect effects of climate change on amphibian populations. Diversity 2:281–313.  https://doi.org/10.3390/d2020281 CrossRefGoogle Scholar
  11. Borcherding J, Beeck P, De Angelis DL, Scharf WR (2010) Match or mismatch: the influence of phenology on size-dependent life history and divergence in population structure. J Anim Ecol 79:1101–1112.  https://doi.org/10.1111/j.1365-2656.2010.01704.x CrossRefPubMedGoogle Scholar
  12. Chivers DP, Ramasamy RA, McCormick MI, Watson S-A, Siebeck UE, Ferrari MCO (2014) Temporal constraints on predation risk assessment in a changing world. Sci Total Environ 500–501:332–338.  https://doi.org/10.1016/j.scitotenv.2014.08.059 CrossRefPubMedGoogle Scholar
  13. Darrow J, Nulton A, Pompili D (2004) Effects of temperature on the development of the wood frog, Rana sylvatica. J Ecol Res 6:20–24Google Scholar
  14. Dayton GH, Fitzgerald L (2005) Priority effects and desert anuran communities. Can J Zool 83:1112–1116.  https://doi.org/10.1139/z05-105 CrossRefGoogle Scholar
  15. Dayton GH, Saenz D, Baum KA, Langerhans RB, DeWitt TJ (2005) Body shape, burst speed and escape behavior of larval anurans. Oikos 111:582–591.  https://doi.org/10.1111/j.1600-0706.2005.14340.x CrossRefGoogle Scholar
  16. Dell AI, Pawar S, Savage VM (2013) The thermal dependence of biological traits. Ecology 94:1205.  https://doi.org/10.1890/12-2060.1 CrossRefGoogle Scholar
  17. Duarte H, Tejedo M, Katzenberger M, Marangoni F, Baldo D, Beltrán JF, Martí DA, Richter-Boix A, Gonzalez-Voyer A (2012) Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Glob Change Biol 18:412–421CrossRefGoogle Scholar
  18. Durant JM, Hjermann DO, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283.  https://doi.org/10.3354/cr033271 CrossRefGoogle Scholar
  19. Eck B, Byrne A, Popescu VD, Harper EB, Patrick DA (2014) Effects of water temperature on larval amphibian predator–prey dynamics. Herpetol Conserv Biol 9:302–308Google Scholar
  20. Erwin KL (2009) Wetlands and global climate change: the role of wetland restoration in a changing world. Wetl Ecol Manag 17:71–84.  https://doi.org/10.1007/s11273-008-9119-1 CrossRefGoogle Scholar
  21. Fraker ME (2008) The influence of the circadian rhythm of green frog (Rana clamitans) tadpoles on their antipredator behavior and the strength of the nonlethal effects of predators. Am Nat 171:545–552.  https://doi.org/10.1086/528961 CrossRefPubMedGoogle Scholar
  22. Gatz AJ (1971) Intraspecific variations in critical thermal maxima of Ambystoma maculatum. Herpetologica 29:264–268Google Scholar
  23. Gazzola A, Sacchi R, Ghitti M, Balestrieri A (2018) The effect of thinning and cue: density ratio on risk perception by Rana dalmatina tadpoles. Hydrobiologia 813:75.  https://doi.org/10.1007/s10750-018-3510-6 CrossRefGoogle Scholar
  24. Gerick AA, Munshaw RG, Palen WJ, Combes SA, O’Regan SM (2014) Thermal physiology and species distribution models reveal climate vulnerability of temperate amphibians. J Biogeogr 41:713–723CrossRefGoogle Scholar
  25. Gvoždík L, Van Damme R (2008) The evolution of thermal performance curves in semi-aquatic newts: thermal specialists on land and thermal generalists in water? J Therm Biol 33:395–403CrossRefGoogle Scholar
  26. Hayden MT, Reeves MK, Holyoak M, Perdue M, King AL, Tobin SC (2015) Thrice as easy to catch! Copper and temperature modulate predator–prey interactions in larval dragonflies and anurans. Ecosphere 6:1–17.  https://doi.org/10.1890/es14-00461.1 CrossRefGoogle Scholar
  27. Hering D, Schmidt-Kloiber A, Murphy J, Lucke S, Zamora-Muñoz C, Lopez-Rodriguez M, Huber T, Graf W (2009) Potential impact of climate change on aquatic insects: a sensitivity analysis for European caddisflies (Trichoptera) based on distribution patterns and ecological preferences. Aquat Sci 71:3–14.  https://doi.org/10.1007/s00027-009-9159-5 CrossRefGoogle Scholar
  28. Holbrook CT, Petranka JW, Douglas ME (2004) Ecological Interactions between Rana sylvatica and Ambystoma maculatum: evidence of interspecific competition and facultative intraguild predation. Copeia 4:932–939.  https://doi.org/10.1643/ce-04-037r1 CrossRefGoogle Scholar
  29. Hopkins WA (2007) Amphibians as models for studying environmental change. ILAR J 48:270–277CrossRefGoogle Scholar
  30. Howard JH, Wallace RL (1983) Critical thermal maxima in populations of Ambystoma macrodactylum from different elevations. J Herpetol 7:400–4002CrossRefGoogle Scholar
  31. Jara FG (2008) Tadpole–odonate larvae interactions: influence of body size and diel rhythm. Aquat Ecol 42:503–509.  https://doi.org/10.1007/s10452-007-9110-6 CrossRefGoogle Scholar
  32. Jones LLC, Leonard WP, Olson DH (2005) Amphibians of the Pacific northwest. Seattle Audubon Society, SeattleGoogle Scholar
  33. Lawler SP, Morin PJ (1993) Temporal overlap, competition, and priority effects in larval anurans. Ecology 74:174–182.  https://doi.org/10.2307/1939512 CrossRefGoogle Scholar
  34. Lee S-Y, Ryan ME, Hamlet AF, Palen WJ, Lawler JJ, Halabisky M (2015) Projecting the hydrologic impacts of climate change on montane wetlands. PLoS One 10(9):e0136385.  https://doi.org/10.1371/journal.pone.0136385 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Leonard WP, Brown HA, Jones LLC, McAllister KR, Storm RM (1993) Amphibians of Washington and Oregon. Seattle Audubon Society, SeattleGoogle Scholar
  36. Martin P, Bateson P (1993) Measuring behaviour, an introductory guide. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  37. Morin PJ, Lawler SP, Johnson EA (1990) Ecology and breeding phenology of larval Hyla andersonii: the disadvantages of breeding late. Ecology 71:1590–1598CrossRefGoogle Scholar
  38. Mote PW, Hamlet AF, Clark MP, Lettenmaier DP (2005) Declining mountain snowpack in western North America. Bull Am Meteorol Soc 86:39–49.  https://doi.org/10.1175/bams-86-1-39 CrossRefGoogle Scholar
  39. Neven LG (2000) Physiological responses of insects to heat. Postharvest Biol Technol 21:103–111CrossRefGoogle Scholar
  40. Nosaka M, Katayama N, Kishida O (2015) Feedback between size balance and consumption strongly affects the consequences of hatching phenology in size-dependent predator–prey interactions. Oikos 124:225–234.  https://doi.org/10.1111/oik.01662 CrossRefGoogle Scholar
  41. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872.  https://doi.org/10.1111/j.1365-2486.2007.01404.x CrossRefGoogle Scholar
  42. Poff NL, Olden JD, Strayer DS (2012) Climate change and freshwater extinction risk. In: Hannah L (ed) Saving a million species: extinction risk from climate change. Island Press, Washington DCGoogle Scholar
  43. Rajchard J (2006) Antipredator pheromones in amphibians: a review. Vet Med 51:409–413CrossRefGoogle Scholar
  44. Rasmussen NL, Rudolf VHW (2016) Individual and combined effects of two types of phenological shifts on predator–prey interaction. Ecology 97:3414–3421.  https://doi.org/10.1002/ecy.1578 CrossRefPubMedGoogle Scholar
  45. Ryan ME, Palen WJ, Adams MJ, Rochefort RM (2014) Amphibians in the climate vice: loss and restoration of resilience of montane wetland ecosystems of the American West. Front Ecol Environ 12:232–240.  https://doi.org/10.1890/130145 CrossRefGoogle Scholar
  46. Stauffer HP, Semlitsch RD (1993) Effects of visual, chemical and tactile cues of fish on the behavioural response of tadpoles. Anim Behav 46:355–364.  https://doi.org/10.1006/anbe.1993.1197 CrossRefGoogle Scholar
  47. Storey KB, Storey JM (2012) Strategies of molecular adaptation to climate change: the challenges of amphibians and reptiles. In: Storey KB, Tanino KK (eds) Temperature adaptation in a changing climate. CABI Publisher, Wallingford, pp 98–115Google Scholar
  48. Swart CC, Taylor RC (2004) Behavioral interactions between the giant water bug (Belostoma lutarium) and tadpoles of Bufo woodhousii. Southeast Nat 3:13–24CrossRefGoogle Scholar
  49. Thurman LL, Garcia TS (2017) Differential plasticity in response to simulated climate warming in a high-elevation amphibian assemblage. J Herpetol 51:232–239.  https://doi.org/10.1670/16-502 CrossRefGoogle Scholar
  50. Thurman LL, Garcia TS, Hoffman PD (2014) Elevational differences in trait response to UV-B radiation by long-toed salamander populations. Oecologia 175:835–845.  https://doi.org/10.1007/s00442-014-2957-z CrossRefPubMedGoogle Scholar
  51. Todd BD, Scott DE, Pechmann JHK, Gibbons JW (2011) Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community. Proc R Soc B 278:2191–2197.  https://doi.org/10.1098/rspb.2010.1768 CrossRefPubMedGoogle Scholar
  52. Urban MC (2007a) Predator size and phenology shape prey survival in temporary ponds. Oecologia 154:571–580.  https://doi.org/10.1007/s00442-007-0856-2 CrossRefPubMedGoogle Scholar
  53. Urban MC (2007b) The growth-predation risk tradeoff under a growing gape-limited predation threat. Ecology 88:2587–2597.  https://doi.org/10.1890/06-1946.1 CrossRefPubMedGoogle Scholar
  54. Wells KD (2010) Ecology and behavior of amphibians. University of Chicago Press, ChicagoGoogle Scholar
  55. Wilbur HM (1997) Experimental ecology of food webs: complex systems in temporary ponds. The Robert H. Mac-Arthur Award lecture. Ecology 78:2279–2302.  https://doi.org/10.1890/0012-9658(1997)078%5b2279:eeofwc%5d2.0.co;2 CrossRefGoogle Scholar
  56. Wildy EL (2001) Cannibalism in larvae of the long-toed salamander, Ambystoma macrodactylum. Ph.D. dissertation, Department of Zoology, Oregon State University, USAGoogle Scholar
  57. Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Glob Change Biol 10:1844–1856.  https://doi.org/10.1111/j.1365-2486.2004.00849.x CrossRefGoogle Scholar
  58. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10.  https://doi.org/10.1111/j.1461-0248.2009.01402.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA, UNComahue-CONICET)San Carlos de BarilocheArgentina
  2. 2.U.S. Geological Survey, Northern Rocky Mountain Science CenterBozemanUSA
  3. 3.Department of Environmental Science and PolicyUniversity of California at DavisDavisUSA
  4. 4.Department of Biology and Redpath MuseumMcGill UniversityMontrealCanada
  5. 5.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA

Personalised recommendations