Advertisement

Marine Biology

, 166:23 | Cite as

Trait-mediated indirect effects in a natural tidepool system

  • Sarah A. GravemEmail author
  • Steven G. Morgan
Original paper

Abstract

We demonstrate an apparent trait-mediated indirect interaction (TMII) of predators on primary producers in a natural community by altering prey behavior over short and long time scales. Small predatory sea stars (Leptasterias spp.) caused herbivorous snails (Tegula funebralis) added to rocky intertidal tidepools to quickly flee into refuge microhabitats outside tidepools within days, and this was associated with a 58% increase in microalgal growth after 2 weeks. Similarly, removing sea stars caused snails to increase use of tidepools for 1–10 months. After adding sea stars to tidepools, snails quickly fled and then consistently increased use of refuges outside tidepools for 10 months. This was associated with average increases of 59% for microalgal growth over 1 month and 254% for macroalgal growth over 8 months inside tidepools. In 63 unmanipulated tidepools, densities of sea stars and snails were negatively correlated. High densities of snails were associated with unpalatable algal species and bare rock, while high densities of sea stars were associated with palatable algal species, suggesting that this apparent TMII may have community-level impacts. Though multiple lines of evidence suggest TMIIs were likely operating in this system, it was not possible to experimentally partition the relative contributions of TMIIs and density-mediated indirect interactions (DMIIs), so further caging experiments are necessary to distinguish their relative strengths. Overall, we suggest that predators can benefit primary producers by changing prey behavior even when predators and prey are unrestrained by cages or mesocosms, embedded in complex communities, and observed over multiple time scales.

Notes

Acknowledgements

For assistance in the field and laboratory, thanks to Sarah Traiger, Olivia Turnross, Aiko Michot, Alex von Boer, Jonathan Demmer, Ryanne Ardisana, Amy Fonarow, Andrew Chen, Preston Malm, and Mimi Gravem. Thanks to Blake Brown, Sarah Hameed, and Erin Satterthwaite for support. Thanks to Drs. Seth Miller, Mark Novak, Susan Williams, Andy Sih, Eric Sanford, Brian Gaylord, Jarrett Byrnes, Ben Dalziel and our anonymous reviewers for providing constructive comments on experimental design and/or the manuscript. This is a contribution of Bodega Marine Laboratory and dedicated to the memory of Dr. Susan Williams, whose many direct and indirect effects are intense, profound, and will be long-lasting.

Author contributions

SG and SM conceived the project idea. SG collected and analyzed the data and was the primary author. SM provided constant guidance and edited the manuscript.

Funding

This study was funded by California SeaGrants R/FISH218, R/MPA14 and R/MPA24 awarded to Steven Morgan, National Science Foundation Grants OCE-1334448 and OCE-0927196 awarded to Steven Morgan, National Science Foundation GK-12 Grant 0841297 awarded to Susan Williams, the Conchologists of America, the Mildred E. Mathias Foundation, Henry A. Jastro fellowship, the UC Davis Graduate Group in Ecology, and the Bodega Marine Laboratory Fellowship.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Ethical approval

All procedures performed in studies involving. animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All collections and manipulations of animals in the study were in compliance with the California Department of Fish and Game collecting permit SC-4688 to Steven Morgan and approved by the University of California Natural Reserve System.

References

  1. Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134.  https://doi.org/10.1086/285789 CrossRefGoogle Scholar
  2. Abrams PA (2007) Defining and measuring the impact of dynamic traits on interspecific interactions. Ecology 88(10):2555–2562.  https://doi.org/10.1890/06-1381.1 CrossRefPubMedGoogle Scholar
  3. Abrams PA (2008) Measuring the population-level consequences of predator-induced prey movement. Evol Ecol Res 10:333–350Google Scholar
  4. Aquilino KM, Coulbourne ME, Stachowicz JJ (2012) Mixed species diets enhance the growth of two rocky intertidal herbivores. Mar Ecol Prog Ser 468:179–189.  https://doi.org/10.3354/meps09893 CrossRefGoogle Scholar
  5. Bartl S (1980) A comparison of the feeding behavior of the six-rayed seastar, Leptasterias hexactis, and from two intertidal habitats. Bodega Marine Laboratory Cadet Hand Library, unpublished student report, Problems in Marine Biology courseGoogle Scholar
  6. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  7. Bernot RJ, Turner AM (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146.  https://doi.org/10.1007/s004420100705 CrossRefPubMedGoogle Scholar
  8. Best B (1964) Feeding activities of Tegula funebralis. The Veliger 6:42–45Google Scholar
  9. Bolker B, Holyoak M, Krivan V, Rowe L, Schmitz O (2003) Connecting theoretical and empirical studies of trait-mediated interactions. Ecology 84:1101–1114CrossRefGoogle Scholar
  10. Bouchet P, Rosenberg G (2015) Tegula funebralis. In: MolluscaBase (2015). Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=534190. Accessed 15 Sep 2015
  11. Bullock TH (1953) Predator recognition and escape responses of some intertidal gastropods in presence of starfish. Behaviour 5:130–140.  https://doi.org/10.1163/156853953x00078 CrossRefGoogle Scholar
  12. Callaway RM, Pennings SC, Richards CL (2003) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128CrossRefGoogle Scholar
  13. Flowers JM, Foltz DW (2001) Reconciling molecular systematics and traditional taxonomy in a species-rich clade of sea stars (Leptasterias subgenus hexasterias). Mar Biol 139:475–483.  https://doi.org/10.1007/s002270100595 CrossRefGoogle Scholar
  14. Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249CrossRefGoogle Scholar
  15. Grabowski JH, Kimbro DL (2005) Predator-avoidance behavior extends trophic cascades to refuge habitats. Ecology 86:1312–1319CrossRefGoogle Scholar
  16. Gravem SA, Morgan SG (2016) Prey state alters trait-mediated indirect interactions in rocky tidepools. Funct Ecol 30:1574–1582.  https://doi.org/10.1111/1365-2435.12628 CrossRefGoogle Scholar
  17. Gravem SA, Morgan SG (2017) Shifts in intertidal zonation and refuge use by prey after mass mortalities of two predators. Ecology 98:1006–1015CrossRefGoogle Scholar
  18. Green P, MacLeod CJ (2016) SIMR: an R package for power analysis of generalized linear mixed models by simulation. Methods Ecol Evol 7:493–498CrossRefGoogle Scholar
  19. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control and competition. Am Nat 94:421–425CrossRefGoogle Scholar
  20. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394CrossRefGoogle Scholar
  21. Long JD, Hay ME (2012) The impact of trait-mediated indirect interactions in marine communities. In: Ohgushi T, Schmitz OJ, Holt RD (eds) Trait-mediated indirect interactions: ecological and evolutionary perspectives. Cambridge University Press, New York, pp 47–68CrossRefGoogle Scholar
  22. Luttbeg B, Rowe L, Mangel M (2003) Prey state and experimental design affect relative size of trait- and density-mediated indirect effects. Ecology 84:1140–1150.  https://doi.org/10.1890/0012-9658(2003)084%5b1140:PSAEDA%5d2.0.CO;2 CrossRefGoogle Scholar
  23. Matassa CM, Trussell GC (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92:2258–2266.  https://doi.org/10.1890/11-0424.1 CrossRefPubMedGoogle Scholar
  24. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692.  https://doi.org/10.1016/j.tree.2005.08.002 CrossRefPubMedGoogle Scholar
  25. Morelissen B, Harley CDG (2007) The effects of temperature on producers, consumers, and plant-herbivore interactions in an intertidal community. J Exp Mar Biol Ecol 348:162–173.  https://doi.org/10.1016/j.jembe.2007.04.006 CrossRefGoogle Scholar
  26. Morgan SG, Gravem SA, Lipus AC, Grabiel M, Miner BG (2016) Trait-mediated indirect interactions among residents of rocky shore tidepools. Mar Ecol Prog Ser 552:31–46CrossRefGoogle Scholar
  27. Nielsen KJ (2001) Bottom-up and top-down forces in tide pools: test of a food chain model in an intertidal community. Ecol Monogr 71:187–217.  https://doi.org/10.1890/0012-9615(2001)071%5b0187:BUATDF%5d2.0.CO;2 CrossRefGoogle Scholar
  28. Ohgushi T, Schmitz OJ, Holt RD (2012) Trait-mediated indirect interactions: ecological and evolutionary perspectives. Cambridge University Press, New YorkCrossRefGoogle Scholar
  29. Okuyama T, Bolker BM (2007) On quantitative measures of indirect interactions. Ecol Lett 10:264–271.  https://doi.org/10.1111/j.1461-0248.2007.01019 CrossRefPubMedGoogle Scholar
  30. Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure- the 3rd Tansley lecture. J Anim Ecol 49:667–685.  https://doi.org/10.2307/4220 CrossRefGoogle Scholar
  31. Peacor SD (2003) Phenotypic modifications to conspecific density arising from predation risk assessment. Oikos 100:409–415CrossRefGoogle Scholar
  32. Peacor SD, Werner EE (1997) Trait-mediated indirect interactions in a simple aquatic food web. Ecology 78:1146–1156.  https://doi.org/10.2307/2265865 CrossRefGoogle Scholar
  33. Peacor SD, Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci USA 98:3904–3908.  https://doi.org/10.1073/pnas.071061998 CrossRefPubMedGoogle Scholar
  34. Persson L, De Roos AM (2003) Adaptive habitat use in size-structured populations: linking individual behavior to population processes. Ecology 84:1129–1139.  https://doi.org/10.1890/0012-9658(2003)084%5b1129:AHUISP%5d2.0.CO;2 CrossRefGoogle Scholar
  35. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? the effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509.  https://doi.org/10.1890/04-0719 CrossRefGoogle Scholar
  36. Raimondi PT, Forde SE, Delph LF, Lively CM (2000) Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms. Oikos 91:353–361CrossRefGoogle Scholar
  37. Ripple WJ, Beschta RL (2006) Linking wolves to willows via risk-sensitive foraging by ungulates in the northern Yellowstone ecosystem. For Ecol Manag 230:96–106.  https://doi.org/10.1016/j.foreco.2006.04.023 CrossRefGoogle Scholar
  38. Ruesink JL (2000) Intertidal mesograzers in field microcosms: linking laboratory feeding rates to community dynamics. J Exp Mar Biol Ecol 248:163–176.  https://doi.org/10.1016/s0022-0981(00)00170-2 CrossRefPubMedGoogle Scholar
  39. Schmitz OJ (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. Am Nat 151:327–342PubMedGoogle Scholar
  40. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163.  https://doi.org/10.1111/j.1461-0248.2003.00560.x CrossRefGoogle Scholar
  41. Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754.  https://doi.org/10.2307/1940154 CrossRefGoogle Scholar
  42. R Core Team (2013) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/. Accessed 7 Sept 2017 (ISBN: 3-900051-07-0)
  43. Toscano BJ, Newsome B, Griffen BD (2014) Parasite modification of predator functional response. Oecologia 175:345–352CrossRefGoogle Scholar
  44. Trussell GC, Ewanchuk PJ, Bertness MD (2002) Field evidence of trait-mediated indirect interactions in a rocky intertidal food web. Ecol Lett 5:241–245CrossRefGoogle Scholar
  45. Trussell GC, Ewanchuk PJ, Bertness MD, Silliman BR (2004) Trophic cascades in rocky shore tide pools: distinguishing lethal and nonlethal effects. Oecologia 139:427–432.  https://doi.org/10.1007/s00442-004-1512-8 CrossRefPubMedGoogle Scholar
  46. Trussell GC, Ewanchuk PJ, Matassa CM (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252.  https://doi.org/10.1111/j.1461-0248.2006.00981.x CrossRefPubMedGoogle Scholar
  47. Turner AM, Mittelbach GG (1990) Predator avoidance and community structure-interactions among piscivores, planktivores, and plankton. Ecology 71:2241–2254.  https://doi.org/10.2307/1938636 CrossRefGoogle Scholar
  48. Wada Y, Iwasaki K, Yusa Y (2013) Changes in algal community structure via density- and trait-mediated indirect interactions in a marine ecosystem. Ecology 94:2567–2574.  https://doi.org/10.1890/12-0725.1 CrossRefPubMedGoogle Scholar
  49. Weissburg M, Smee DL, Ferner MC (2014) The sensory ecology of nonconsumptive predator effects. Am Nat 184:141–157.  https://doi.org/10.1086/676644 CrossRefPubMedGoogle Scholar
  50. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992CrossRefGoogle Scholar
  51. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100.  https://doi.org/10.1890/0012-9658(2003)084%5b1083:AROTII%5d2.0.CO;2 CrossRefGoogle Scholar
  52. Wood SN (2006) Generalized additive models: an introduction. R Chapman and Hall/CRC, New YorkCrossRefGoogle Scholar
  53. Yarnall JL (1964) The responses of Tegula funebralis to starfishes and predatory snails (Mollusca: Gastropoda). Veliger 6:56–58Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Integrative BiologyOregon State UniversityCorvallisUSA
  2. 2.Bodega Marine LaboratoryUniversity of California DavisBodega BayUSA

Personalised recommendations