Advertisement

Oecologia

, Volume 187, Issue 2, pp 483–494 | Cite as

Temperature effects on a marine herbivore depend strongly on diet across multiple generations

  • Janine Ledet
  • Maria Byrne
  • Alistair G. B. Poore
SPECIAL TOPIC: FROM PLANTS TO HERBIVORES

Abstract

Increasing sea surface temperatures are predicted to alter marine plant–herbivore interactions and, thus, the structure and function of algal and seagrass communities. Given the fundamental role of host plant quality in determining herbivore fitness, predicting the effects of increased temperatures requires an understanding of how temperature may interact with diet quality. We used an herbivorous marine amphipod, Sunamphitoe parmerong, to test how temperature and diet interact to alter herbivore growth, feeding rates, survival, and fecundity in short- and long-term assays. In short-term thermal stress assays, S. parmerong was tolerant to the range of temperatures that it currently experiences in nature (20–26 °C), with mortality at temperatures > 27 °C. In longer term experiments, two generations of S. parmerong were reared in nine combinations of temperature (ambient, + 2, + 4 °C) and diet (two high- and one low-quality algal species) treatments. Temperature and diet interacted to determine total numbers of amphipods in the F1 generation and the potential F2 population size (sum of brooded eggs and newly hatched juveniles). The size and development rate of F1 individuals were affected by diet, but not temperature. Consumption rates per capita were highest at intermediate temperatures but could not explain the observed differences in survival. Our results show that predicting the effects of increasing temperature on marine herbivores will be complicated by variation in host plant quality, and that climate-driven changes to plant availability will affect herbivore performance, and thus the strength of plant–herbivore interactions.

Keywords

Herbivory Macroalgae Amphipods Survival Climate change 

Notes

Acknowledgements

This research was supported by a Grant from the Australian Research Council (DP150102771). We thank S. Dworjanyn (Southern Cross University) for the assistance with carbon and nitrogen measurements, E. Sotka (College of Charleston) for comments that improved this manuscript, N. Coombes and A. Niccum (Sydney Institute of Marine Science) for the help with aquarium facilities, T. Stelling-Wood, B. Lanham, and L. Martin (University of New South Wales) for the experiment and field support, and J. Harianto (University of Sydney) for harbour temperature data. We thank C. Müller and three anonymous reviewers for comments that improved this manuscript.

Author contribution statement

JL, MB, and AGBP conceived and designed the experiments. JL performed the experiments and analyzed the data. JL and AGBP wrote the manuscript and MB provided editorial contributions.

Supplementary material

442_2018_4084_MOESM1_ESM.docx (205 kb)
Supplementary material 1 (DOCX 205 kb)

References

  1. Alsterberg C, Eklöf JS, Gamfeldt L, Havenhand JN, Sundbäck K (2013) Consumers mediate the effects of experimental ocean acidification and warming on primary producers. Proc Natl Acad Sci USA 110(21):8603–8608.  https://doi.org/10.1073/pnas.1303797110 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Atkins RL, Griffin JN, Angelini C, O’Connor MI, Silliman BR (2015) Consumer-plant interaction strength: importance of body size, density and metabolic biomass. Oikos 124:1274–1281.  https://doi.org/10.1111/oik.01966 CrossRefGoogle Scholar
  3. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  4. Boersma M, Mathew KA, Niehoff B, Schoo KL, Franco-Santos RM, Meunier CL (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it’s hot? Ecol Lett 19:45–53.  https://doi.org/10.1111/ele.12541 CrossRefPubMedGoogle Scholar
  5. Burnaford JL (2004) habitat modification and refuge from sublethal stress drive a marine plant–herbivore association. Ecology 85:2837–2849CrossRefGoogle Scholar
  6. Burnell OW, Russell BD, Irving AD, Connell SD (2013) Eutrophication offsets increased sea urchin grazing on seagrass caused by ocean warming and acidification. Mar Ecol Prog Ser 485:37–46.  https://doi.org/10.3354/meps10323 CrossRefGoogle Scholar
  7. Burrows MT, Schoeman DS, Buckley LB, Moore P, Poloczanska ES, Brander KM, Brown C, Bruno JF, Duarte CM, Halpern BS, Holding J, Kappel CV, Kiessling W, O’Connor MI, Pandolfi JM, Parmesan C, Schwing FB, Sydeman WJ, Richardson AJ (2011) The pace of shifting climate in marine and terrestrial ecosystems. Science 334:652–655.  https://doi.org/10.1126/science.1210288 CrossRefPubMedGoogle Scholar
  8. Cardoso PG, Grilo TF, Dionísio G, Aurélio M, Lopes AR, Pereira R, Pacheco M, Rosa R (2017) Short-term effects of increased temperature and lowered pH on a temperate grazer-seaweed interaction. Estuar Coast Shelf Sci 197:35–44.  https://doi.org/10.1016/j.ecss.2017.08.007 CrossRefGoogle Scholar
  9. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365.  https://doi.org/10.1016/j.tree.2007.04.003 CrossRefPubMedGoogle Scholar
  10. Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc B Biol Sci.  https://doi.org/10.1098/rspb.2009.2069 CrossRefGoogle Scholar
  11. Cross WF, Hood JM, Benstead JP, Huryn AD, Nelson D (2015) Interactions between temperature and nutrients across levels of ecological organization. Glob Change Biol 21:1025–1040.  https://doi.org/10.1111/gcb.12809 CrossRefGoogle Scholar
  12. Cruz-Rivera E, Hay ME (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar Ecol Prog Ser 218:249–266CrossRefGoogle Scholar
  13. Davis AJ, Lawton JH, Shorrocks B, Jenkinson LS (1998) Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. J Anim Ecol 67:600–612CrossRefGoogle Scholar
  14. Diamond SE, Kingsolver JG (2010) Fitness consequences of host plant choice: a field experiment. Oikos 119:542–550.  https://doi.org/10.1111/j.1600-0706.2009.17242.x CrossRefGoogle Scholar
  15. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11–37.  https://doi.org/10.1146/annurev-marine-041911-111611 CrossRefPubMedGoogle Scholar
  16. Eisenlord ME, Groner ML, Yoshioka RM, Elliott J, Maynard J, Fradkin S, Turner M, Pyne K, Rivlin N, Van Hooidonk R, Harvell CD (2016) Ochre star mortality during the 2014 wasting disease epizootic: role of population size structure and temperature. Phil Trans R Soc B 371:20150212.  https://doi.org/10.1098/rstb.2015.0212 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Faulkner KT, Clusella-Trullas S, Peck LS, Chown SL (2014) Lack of coherence in the warming responses of marine crustaceans. Funct Ecol 28:895–903.  https://doi.org/10.1111/1365-2435.12219 CrossRefGoogle Scholar
  18. Fox LA, Morrow PA (1981) Specialization: species property or local phenomenon. Science 211:887–893CrossRefPubMedGoogle Scholar
  19. Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connell SD, Fabricius KE, Hall-Spencer JM, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Scheriber SJ, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15.  https://doi.org/10.1890/14-0802.1v CrossRefPubMedGoogle Scholar
  20. Goldenberg SU, Nagelkerken I, Ferreira CM, Ullah H, Connell SD (2017) Boosted food web productivity through ocean acidification collapses under warming. Glob Change Biol 23:4177–4184.  https://doi.org/10.1890/14-0802.1 CrossRefGoogle Scholar
  21. Gutow L, Petersen I, Bartl K, Huenerlage K (2016) Marine meso-herbivore consumption scales faster with temperature than seaweed primary production. J Exp Mar Biol Ecol 477:80–85.  https://doi.org/10.1016/j.jembe.2016.01.009 CrossRefGoogle Scholar
  22. Hale R, Calosi P, McNeill L, Mieszkowska N, Widdicombe S (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120:661–674.  https://doi.org/10.1111/j.1600-0706.2010.19469.x CrossRefGoogle Scholar
  23. Hardy NA, Lamare M, Uthicke S, Wolfe K, Doo S, Dworjanyn S, Byrne M (2014) Thermal tolerance of early development in tropical and temperate sea urchins: inferences for the tropicalization of eastern Australia. Mar Biol 161:395–409.  https://doi.org/10.1007/s00227-013-2344-z CrossRefGoogle Scholar
  24. Heldt KA, Connell SD, Anderson K, Russell BD, Munguia P (2016) Future climate stimulates population out-breaks by relaxing constraints on reproduction. Sci Rep 6:33383.  https://doi.org/10.1038/srep33383 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201.  https://doi.org/10.1146/annurev.physiol.67.040403.105027 CrossRefPubMedGoogle Scholar
  26. Hobday AJ, Lough JM (2011) Projected climate change in Australian marine and freshwater environments. Mar Freshw Res 62:1000–1014.  https://doi.org/10.1071/MF10302 CrossRefGoogle Scholar
  27. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363.  https://doi.org/10.1002/bimj.200810425 CrossRefPubMedGoogle Scholar
  28. King AD, Karoly DJ, Henley BJ (2017) Australian climate extremes at 1.5 °C and 2 °C of global warming. Nat Clim Change 7:412–416.  https://doi.org/10.1038/nclimate3296 CrossRefGoogle Scholar
  29. Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268Google Scholar
  30. Kordas RL, Harley CDG, Connor MIO (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Bio Ecol 400:218–226.  https://doi.org/10.1016/j.jembe.2011.02.029 CrossRefGoogle Scholar
  31. Lee KP, Roh C (2010) Temperature-by-nutrient interactions affecting growth rate in an insect ectotherm. Entomol Exp Appl 136:151–163.  https://doi.org/10.1111/j.1570-7458.2010.01018.x CrossRefGoogle Scholar
  32. Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93:2483–2489.  https://doi.org/10.1890/12-0375.1 CrossRefPubMedGoogle Scholar
  33. Lemoine NP, Shantz AA (2016) Increased temperature causes protein limitation by reducing the efficiency of nitrogen digestion in the ectothermic herbivore Spodoptera exigua. Physiol Entomol 41:143–151.  https://doi.org/10.1111/phen.12138 CrossRefGoogle Scholar
  34. Lemoine NP, Drews WA, Burkepile DE, Parker JD (2013) Increased temperature alters feeding behavior of a generalist herbivore. Oikos 122:1669–1678.  https://doi.org/10.1111/j.1600-0706.2013.00457.x CrossRefGoogle Scholar
  35. Malzahn AM, Doerfler D, Boersma M (2016) Junk food gets healthier when it’s warm. Limnol Oceanogr 61:1677–1685.  https://doi.org/10.1002/lno.10330 CrossRefGoogle Scholar
  36. Manyak-Davis A, Bell TM, Sotka EE (2013) The relative importance of predation risk and water temperature in maintaining Bergmann’s rule in a marine ectotherm. Am Nat 182:347–358.  https://doi.org/10.1086/671170 CrossRefPubMedGoogle Scholar
  37. Mrowicki R, O’Connor N (2015) Wave action modifies the effects of consumer diversity and warming on algal assemblages. Ecology 96:1020–1029.  https://doi.org/10.1890/14-0577.1 CrossRefPubMedGoogle Scholar
  38. O’Connor MI (2009) Warming strengthens an herbivore–plant interaction. Ecology 90:388–398CrossRefPubMedGoogle Scholar
  39. Ockendon N, Baker DJ, Carr JA, White EC, Almond REA, Amano T, Bertram E, Bradbury RB, Bradley C, Butchart SHM, Doswald N, Foden W, Gill DJC, Green RE, Sutherland WJ, Tanner EVJ, Pearce-Higgins JW (2014) Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects. Glob Change Biol 20:2221–2229.  https://doi.org/10.1111/gcb.12559 CrossRefGoogle Scholar
  40. Peart RA, Ahyong ST (2016) Phylogenetic analysis of the family Ampithoidae Stebbing, 1899 (Crustacea: Amphipoda), with a synopsis of the genera. J Crust Biol 36:456–474.  https://doi.org/10.1163/1937240X-00002449 CrossRefGoogle Scholar
  41. Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen I-C, Clark TD, Colwell RK, Danielsen F, Evengård B, Falconi L, Ferrier S, Frusher S, Garcia RA, Griffis RB, Hobday AJ, Janion-Scheepers C, Jarzyna MA, Jennings S, Lenoir J, Linnetved HI, Martin VY, McCormack PC, McDonald J, Mitchell NJ, Mustonen T, Pandolfi JM, Pettorelli N, Popova E, Robinson SA, Scheffers BR, Shaw JD, Sorte CJB, Strugnell JM, Sunday JM, Tuanmu M-N, Vergés A, Villanueva C, Wernberg T, Wapstra E, Williams SE (2017) Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science 355:eaai9214.  https://doi.org/10.1126/science.aai9214 CrossRefPubMedGoogle Scholar
  42. Pennings SC, Carefoot TH (1995) Post-ingestive consequences of consuming secondary metabolites in sea hares (Gastropoda: Opisthobranchia). Comp Biochem Physiol Part C Comp 111:249–256CrossRefGoogle Scholar
  43. Phelps CM, Boyce MC, Huggett MJ (2017) Future climate change scenarios differentially affect three abundant algal species in southwestern Australia. Mar Environ Res 126:69–80.  https://doi.org/10.1016/j.marenvres.2017.02.008 CrossRefPubMedGoogle Scholar
  44. Poore AGB, Steinberg PD (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol Monogr 69:443–464Google Scholar
  45. Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA, Emmett Duffy J (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922.  https://doi.org/10.1111/j.1461-0248.2012.01804.x CrossRefPubMedGoogle Scholar
  46. Poore AGB, Graba-Landry A, Favret M, Sheppard Brennand H, Byrne M, Dworjanyn SA (2013) Direct and indirect effects of ocean acidification and warming on a marine plant-herbivore interaction. Oecologia 173:1113–1124.  https://doi.org/10.1007/s00442-013-2683-y CrossRefPubMedGoogle Scholar
  47. Poore AGB, Graham SE, Byrne M, Dworjanyn SA (2016) Effects of ocean warming and lowered pH on algal growth and palatability to a grazing gastropod. Mar Biol 163:99.  https://doi.org/10.1007/s00227-016-2878-y CrossRefGoogle Scholar
  48. Schram JB, McClintock JB, Amsler CD, Baker BJ (2015) Impacts of acute elevated seawater temperature on the feeding preferences of an Antarctic amphipod toward chemically deterrent macroalgae. Mar Biol 162:425–433.  https://doi.org/10.1007/s00227-014-2590-8 CrossRefGoogle Scholar
  49. Schram JB, Schoenrock KM, McClintock JB, Amsler CD, Angus RA (2016) Seawater acidification more than warming presents a challenge for two Antarctic macroalgal-associated amphipods. Mar Ecol Prog Ser 554:81–97.  https://doi.org/10.3354/meps11814 CrossRefGoogle Scholar
  50. Sotka EE, Giddens H (2009) Seawater temperature alters feeding discrimination by cold-temperate but not subtropical individuals of an ectothermic herbivore. Biol Bull 216:75–84.  https://doi.org/10.2307/25470725 CrossRefPubMedGoogle Scholar
  51. Sotka EE, Reynolds PL (2011) Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts. Evol Ecol 25:1335–1355.  https://doi.org/10.1007/s10682-011-9473-y CrossRefGoogle Scholar
  52. Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99.  https://doi.org/10.1111/j.1529-8817.2008.00635.x CrossRefPubMedGoogle Scholar
  53. Stamp NE (1990) Growth versus molting time of caterpillars as a function of temperature, nutrient concentration and the phenolic rutin. Oecologia 82:107–113CrossRefPubMedGoogle Scholar
  54. Stamp N, Bowers MD (1990) Variation in food quality and temperature constrain foraging of gregarious caterpillars. Ecology 71:1031–1039CrossRefGoogle Scholar
  55. Stamp NE, Yang Y (1996) Response of insect herbivores to multiple allelochemicals under different thermal regimes. Ecology 77:1088–1102CrossRefGoogle Scholar
  56. Steinberg PD, van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222CrossRefGoogle Scholar
  57. Svensson F, Karlsson E, Gårdmark A, Olsson J, Adill A, Zie J, Snoeijs P, Eklöf JS, Svensson F (2017) In situ warming strengthens trophic cascades in a coastal food web. Oikos.  https://doi.org/10.1111/oik.03773 CrossRefGoogle Scholar
  58. Therneau T (2015) A package for survival analysis in S. version 2.38, https://CRAN.R-project.org/package=survival
  59. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363.  https://doi.org/10.1111/j.1461-0248.2008.01250.x CrossRefPubMedGoogle Scholar
  60. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL Jr, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, Van Sebille E, Sen Gupta A, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846.  https://doi.org/10.1098/rspb.2014.0846 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Watts SA, Hofer SC, Desmond RA, Lawrence AL, Lawrence JM (2011) The effect of temperature on feeding and growth characteristics of the sea urchin Lytechinus variegatus fed a formulated feed. J Exp Mar Biol Ecol 397:188–195.  https://doi.org/10.1016/j.jembe.2010.10.007 CrossRefGoogle Scholar
  62. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, De Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78.  https://doi.org/10.1038/nclimate1627 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Evolution and Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.School of Medical Sciences and School of Life and School of Environmental SciencesUniversity of SydneySydneyAustralia

Personalised recommendations