Predator tactics and prey densities modulate the strength of trophic interactions in a temperate rocky reef

Abstract

Evaluating the species-specific effects of multiple predators on shared prey helps to identify the mechanisms regulating predator impacts. Here, we investigate the trophic impact of two predators of the Chilean rocky subtidal, the fish Graus nigra [F] and the octopus Robsonella fontaniana [O] on their shared prey, the porcelain crab, Petrolisthes violaceus. Manipulative laboratory experiments were performed to evaluate mortality and behavior of porcelain crab in different treatments, including prey alone; prey with single predator ([O] or [F]); and prey with combined predators ([F + F], [O + O], and [O + F]). Different prey densities (N = 3, 9, and 12 individuals) were used to explore density-dependent predation mortality for single and combined predators using an orthogonal (crossed) design that allows to tease apart the effects of predator taxonomic identity from prey density. Behavioral responses of interacting species were registered every 4 h for 2 consecutive days, and were used to identify predator foraging strategies and prey refuge use. Mortality values (proportional prey mortality and predator per capita consumption) were compared among treatments. Results indicated differences in mortality among treatments. The cause of increase of prey proportional mortality was due to an increase in prey availability outside the refuge in fish treatments at high initial prey densities, while it was density independent in octopus’ treatments. Changes in predator per capita consumption were registered depending on the predator combination and the initial prey density. These patterns may reflect contrasting predator foraging strategies and changes in refuge use by porcelain crabs, suggesting effects on prey mortality and predator impacts.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Data/code availability

The data and r-code that support the findings of this study are available from the corresponding author [APM], upon reasonable request.

References

  1. Abrams PA, Ginzburg LR (2000) The nature of predation: prey dependent, ratio dependent or neither? Trends Ecol Evol 15(8):337–341

    CAS  PubMed  Article  Google Scholar 

  2. Ahrens RN, Walters CJ, Christensen V (2012) Foraging arena theory. Fish Fish 13(1):41–59

    Article  Google Scholar 

  3. Angel A, Ojeda FP (2001) Structure and trophic organization of subtidal fish assemblages on the northern Chilean coast: the effect of habitat complexity. Mar Ecol Prog Ser 217:81–91

    Article  Google Scholar 

  4. Berrios VC, Vargas MF (2004) Estructura trófica de la asociación de peces intermareales de la costa rocosa del norte de Chile. Rev Biol Trop 52(1):201–212

    PubMed  Article  Google Scholar 

  5. Berrios PA, Farias AA, Ojeda FP (2011) Spatio-temporal variability in ontogenetic guild structure of an intertidal fish assemblage in central Chile. Rev Chil Hist Nat 84(4):553–570

    Article  Google Scholar 

  6. Boyle P, Rodhouse P (2005) Cephalopods: ecology and fisheries. Blackwell Publishing, Oxford, pp 222–233

    Google Scholar 

  7. Castilla JC, Paine RT (1987) Predation and community organization on eastern Pacific, temperate zone, rocky intertidal shores. Rev Chil Hist Nat 60:131–151

    Google Scholar 

  8. Casula P, Wilby A, Thomas MB (2006) Understanding biodiversity effects on prey in multi-enemy systems. Ecol Lett 9(9):995–1004

    PubMed  Article  Google Scholar 

  9. Clarke T (1970) Territorial behavior and population dynamics of a pomacentrid fish, the garibaldi, Hypsypopsrubicunda. Ecol Monogr 40(2):189–212

    Article  Google Scholar 

  10. Connell SD (2000) Is there safety-in-numbers for prey. Oikos 88(3):527–532

    Article  Google Scholar 

  11. Crawley MJ (2007) The R Book. John Wiley & Sons, Chichester

    Google Scholar 

  12. Dunn RP (2016) Tool use by a temperate wrasse, California sheephead Semicossyphus pulcher. J Fish Biol 88(2):805–810

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. Emparanza EJ (2007) Patterns of distribution of dominant porcelain crabs (Decapoda: Porcellanidae) under boulders in the intertidal of northern Chile. J Mar Biol Assoc UK 87(2):523–531

    Article  Google Scholar 

  14. Evans EW (1991) Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids. Oecologia 87(3):401–408

    PubMed  Article  PubMed Central  Google Scholar 

  15. Fuentes HR (1982) Feeding habits of Graus nigra (Labridae) in coastal waters of Iquique in northern Chile. Jpn J Ichthyol 29(1):95–98

    Google Scholar 

  16. Gerking SD (1994) Mouth and sense organs. In: Gerking SD (ed) Feeding ecology of fish. Academic Press, New York, pp 15–40

  17. Hassell MP (1978) The dynamics of arthropod predator–prey systems. Princeton University Press, Princeton

    Google Scholar 

  18. Haggerty MB, Anderson TW, Long JD (2018) Fish predators reduce kelp frond loss via a trait-mediated trophic cascade. Ecology 99(7):1574–1583

    PubMed  Article  Google Scholar 

  19. Hastie T, Pregibon D (1991) Generalized linear models. In: Chambers JM, Hastie T (eds) Statistical models editors. Wadsworth and Brooks, Cole

  20. Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83(10):2855–2868

    Article  Google Scholar 

  21. Holling CS (1965) The functional response of predators to prey density and its role in mimicry and population regulation. Mem Entomol Soc Can 97(S45):5–60

    Article  Google Scholar 

  22. Ibáñez CM, Sepúlveda RD, Guerrero J, Chong J (2008) Redescription of Robsonella fontaniana (Cephalopoda: Octopodidae). J Mar Biol Association United Kingdom 88(3):617–624

  23. Ibañez CM, Sepúlveda RD, Sanhueza E, Ruiz J, Chong J (2009) Estrategias de forrajeo de Robsonella fontaniana (d’Orbigny, 1834) (Cephalopoda: Octopodidae). Rev Biol Mar Oceanogr 44(2):277–283

    Article  Google Scholar 

  24. Kéfi S, Berlow EL, Wieters EA, Joppa LN, Wood SA, Brose U, Navarrete SA (2015) Network structure beyond food webs: mapping non-trophic and trophic interactions on Chilean rocky shores. Ecology 96(1):291–303

    Article  Google Scholar 

  25. Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. Bioscience 48(1):25–34

    Article  Google Scholar 

  26. McCoy MW, Stier AC, Osenberg CW (2012) Emergent effects of multiple predators on prey survival: the importance of depletion and the functional response. Ecol Lett 15(12):1449–1456

    PubMed  Article  Google Scholar 

  27. Muñoz AA, Ojeda FP (1998) Guild structure of carnivorous intertidal fishes of the Chilean coast: implications of ontogenetic dietary shifts. Oecologia 114(4):563–573

    PubMed  Article  Google Scholar 

  28. Musrri CA, Poore AG, Hinojosa IA et al (2019) Variation in consumer pressure along 2500 km in a major upwelling system: crab predators are more important at higher latitudes. Mar Biol 166(11):142

    Article  Google Scholar 

  29. Navarrete SA, Castilla JC (2003) Experimental determination of predation intensity in an intertidal predator guild: dominant versus subordinate prey. Oikos 100(2):251–262

    Article  Google Scholar 

  30. Navarrete SA, Manzur T (2008) Individual-and population-level responses of a keystone predator to geographic variation in prey. Ecology 89(7):2005–2018

    PubMed  Article  Google Scholar 

  31. Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88(3):539–546

    Article  Google Scholar 

  32. Ory NC, Dudgeon D, Dumont CP, Miranda L, Thiel M (2012) Effects of predation and habitat structure on the abundance and population structure of the rock shrimp Rhynchocinetes typus (Caridea) on temperate rocky reefs. Mar Biol 159(9):2075–2089

    PubMed  PubMed Central  Article  Google Scholar 

  33. Paine RT (1966) Food web complexity and species diversity. Am Nat 100(910):65–75

    Article  Google Scholar 

  34. Pérez-Matus A, Shima JS (2010) Disentangling the effects of macroalgae on the abundance of temperate reef fishes. J Exp Mar Biol Ecol 388(1–2):1–10

    Article  Google Scholar 

  35. Pérez-Matus A, Pledger S, Díaz F, Ferry-Graham LA, Vásquez JA (2012) Plasticity in feeding selectivity and trophic structure of kelp forest associated fishes from northern Chile. Rev Chil Hist Nat 85:29–48

    Article  Google Scholar 

  36. Pérez-Matus A, Ospina-Alvarez A, Camus PA, Carrasco SA et al (2017) Temperate rocky subtidal reef community reveals human impacts across the entire food web. Mar Ecol Prog Ser 567(1):16

    Google Scholar 

  37. Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter nonconsumptive effects in predator–prey interactions. Ecology 88(11):2744–2751

    PubMed  Article  PubMed Central  Google Scholar 

  38. Riquelme-Pérez N, Musrri CA, Stotz WB, Cerda O, Pino-Olivares O, Thiel M (2019) Coastal fish assemblages and predation pressure in northern-central Chilean Lessonia trabeculata kelp forests and barren grounds. PeerJ 7:e6964

    PubMed  PubMed Central  Article  Google Scholar 

  39. Ritz DA (1994) Social aggregation in pelagic invertebrates. In: Blaxter JHS, Southward AJ (eds) Advances in marine biology. Academic Press, London, pp 155–211

    Google Scholar 

  40. Rivadeneira MM, Hernáez P, Antonio Baeza J, Boltana S et al (2010) Testing the abundant-centre hypothesis using intertidal porcelain crabs along the Chilean coast: linking abundance and life-history variation. J Biogeogr 37(3):486–498

    Article  Google Scholar 

  41. Schmitz OJ, Suttle KB (2001) Effects of top predator species on direct and indirect interactions in a food web. Ecology 82(7):2072–2081

    Article  Google Scholar 

  42. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13(9):350–355

    CAS  PubMed  Article  Google Scholar 

  43. Sokol-Hessner L, Schmitz OJ (2002) Aggregate effects of multiple predator species on a shared prey. Ecology 83(9):2367–2372

    Article  Google Scholar 

  44. Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18(1):1–35

  45. Soluk DA (1993) Multiple predator effects: predicting combined functional response of stream fish and invertebrate predators. Ecology 74(1):219–225

    Article  Google Scholar 

  46. Soluk DA, Collins NC (1988) Synergistic interactios between fish and invertebrate predators: facilitation and interference among stream predators. Oikos 52(94):100

    Google Scholar 

  47. Thompson PL, Guzman LM, De Meester L, Horváth Z, Ptacnik R, Vanschoenwinkel B et al (2020) A process-based metacommunity framework linking local and regional scale community ecology. Ecol Lett 23:1314–1329

    PubMed  PubMed Central  Article  Google Scholar 

  48. Van Son TC, Thiel M (2006) Multiple predator effects in an intertidal food web. J Anim Ecol 75(1):25–32

    PubMed  Article  Google Scholar 

  49. Varas E, Ojeda FP (1990) Intertidal fish assemblages of the central Chilean coast: diversity, abundance and trophic patterns. Rev Biol Mar 25(2):59–70

    Google Scholar 

  50. Viviani CA (1969) Los Porcellanidae (Crustacea Anomura) chilenos: Distribución geográfica, y algunas observaciones biocenóticas sobre los porcelánidos en la bahía de Mehuín. Stud Neotrop Fauna Environ 6(1):40–56

    Google Scholar 

Download references

Acknowledgements

Authors would like to thank V. Garmendia, C. Ruz (SUBELAB), and N. Osiadacz for their assistance in the field and laboratory, and V. Cifuentes (PUC) for providing octopus drawings. We would also like to thank Dr. Robert Lamb and three anonymous reviewers who provided comments that significantly improved our manuscript.

Funding

This research was funded by CONICYT-FONDECYT through the regular Grant #1151094 to APM and the post-doctoral Grant #3140416 and Initiation Grant #11170617 to SC.

Author information

Affiliations

Authors

Contributions

APM and SC conceived the study; RMC conducted all experiments and provided earlier drafts. APM and RMC conducted statistical analysis. RMC, AMP, SC, and FPO wrote the paper.

Corresponding author

Correspondence to Alejandro Pérez-Matus.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethic approval

All procedures involving animals were in compliance with ethics committee of Faculty of Biological Sciences, Pontificia Universidad Catolica de Chile under CBB-192/2014 for reef fishes and crustaceans and CBB-14/2013 for cephalopods.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: S. Connell.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 339 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Muñoz-Cordovez, R.H., Carrasco, S.A., Ojeda, F.P. et al. Predator tactics and prey densities modulate the strength of trophic interactions in a temperate rocky reef. Mar Biol 168, 38 (2021). https://doi.org/10.1007/s00227-021-03842-x

Download citation