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The role of recruitment and behaviour in the formation of mussel-dominated assemblages: an ontogenetic and taxonomic perspective

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Abstract

Behaviour influences individual fitness with effects that can propagate from the individual to the group. Here, we tested for higher-level effects of individual behaviour in the structuring of intertidal populations of two competing ecosystem engineering species. We used the partial habitat segregation exhibited by co-occurring indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels in South Africa to test for possible attraction of different size classes of recruits to conspecific adults, using a combination of field and laboratory studies. Each of the two species dominates a particular height on the shore with overlap in the mid-mussel zone, but measurements of settlement and recruitment in the field partially refuted previous findings, generally showing no within-shore pattern of zonation of settlers and recruits. At smaller scales, recruits of both species were found more frequently on adults of Mytilus in natural beds where adults coexist in mixed-species populations. Finally, the results of laboratory choice experiments showed that recruits of all sizes responded to adult cues by movement, but that the smallest recruits showed only minimal movement and never reached adults; only large recruits of Perna responded positively to conspecific Perna adults. This study emphasises how observations made at different scales, from shore (among sites) to mussel bed (within shores), to the individual (field and laboratory), can produce different, or even contrasting, information, highlighting how behavioural traits, like attraction to conspecifics, can differ within the same group of organisms (congeneric species) and change ontogenetically within a species. Incorporating fine-scale responses makes predictions of population dynamics more complex, but identifying the relative strengths of mechanisms that lead to patterns of distribution is necessary for understanding higher-level interactions within a system.

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References

  • 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

    Article  Google Scholar 

  • Bertness MD, Crain CM, Silliman BR et al (2006) T he community structure of western Atlantic Patagonian rocky shores. Ecol Monogr 76:439–460. doi:10.1890/0012-9615(2006)076[0439:TCSOWA]2.0.CO;2

    Article  Google Scholar 

  • Bownes SJ, McQuaid CD (2006) Will the invasive mussel Mytilus galloprovincialis Lamarck replace the indigenous Perna perna L. on the south coast of South Africa? J Exp Mar Bio Ecol 338:140–151. doi:10.1016/j.jembe.2006.07.006

    Article  Google Scholar 

  • Bownes SJ, McQuaid CD (2009) Mechanisms of habitat segregation between an invasive and an indigenous mussel: settlement, post-settlement mortality and recruitment. Mar Biol 156:991–1006. doi:10.1007/s00227-009-1143-z

    Article  Google Scholar 

  • Burrows MT, Hawkins SJ (1998) Modelling patch dynamics on rocky shores using deterministic cellular automata. Mar Ecol Prog Ser 167:1–13. doi:10.3354/meps167001

    Article  Google Scholar 

  • Chapman MG (2000) Poor design of behavioural experiments gets poor results: examples from intertidal habitats. J Exp Mar Bio Ecol 250:77–95. doi:10.1016/S0022-0981(00)00180-5

    Article  Google Scholar 

  • Cole VJ, McQuaid CD (2010) Bioengineers and their associated fauna respond differently to the effects of biogeography and upwelling. Ecology 91:3549–3562. doi:10.1890/09-2152.1

    Article  Google Scholar 

  • Commito JA, Dow WE, Grupe BM (2006) Hierarchical spatial structure in soft-bottom mussel beds. J Exp Mar Biol Ecol 330:27–37

    Article  Google Scholar 

  • Commito JA, Commito AE, Platt R V., et al (2014) Recruitment facilitation and spatial pattern formation in soft-bottom mussel beds. Ecosphere 5. art160. doi:10.1890/ES14-00200.1

  • Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Syst 3:169–192

    Article  Google Scholar 

  • Crowe TP, Underwood AJ (1998) Testing behavioural “preference” for suitable microhabitat. J Exp Mar Biol Ecol 225:1–11. doi:10.1016/S0022-0981(97)00187-1

    Article  Google Scholar 

  • Díaz E, McQuaid C (2014) Short-term spatial stability in trophic interactions. J Ecol 102:1138–1149. doi:10.1111/1365-2745.12272

    Article  Google Scholar 

  • Dill LM, Heithaus MR, Walters CJ (2003) Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84:1151–1157. doi:10.1890/0012-9658(2003)084[1151:BMIIIM]2.0.CO;2

    Article  Google Scholar 

  • Erlandsson J, McQuaid CD (2004) Spatial structure of recruitment in the mussel Perna perna at local scales: effects of adults, algae and recruit size. Mar Ecol Prog Ser 267:173–185. doi:10.3354/meps267173

    Article  Google Scholar 

  • Erlandsson J, McQuaid CD, Kostylev VE (2005) Contrasting spatial heterogeneity of sessile organisms within mussel (Perna perna L.) beds in relation to topographic variability. J Exp Mar Biol Ecol 314:79–97

    Article  Google Scholar 

  • Erlandsson J, Pal P, McQuaid CD (2006) Re-colonisation rate differs between co-existing indigenous and invasive intertidal mussels following major disturbance. Mar Ecol Prog Ser 320:169–176. doi:10.3354/meps320169

    Article  Google Scholar 

  • Erlandsson J, McQuaid CD, Sköld M (2011) Patchiness and co-existence of indigenous and invasive mussels at small spatial scales: the interaction of facilitation and competition. PLoS ONE 6(11):e26958. doi:10.1371/journal.pone.0026958

    Article  CAS  Google Scholar 

  • Fordyce J (2006) The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J Exp Biol 209:2377–2383. doi:10.1242/jeb.02271

    Article  Google Scholar 

  • Garcia Charton JA, Perez Ruzafa A (1999) Ecological heterogeneity and the evaluation of the effects of marine reserves. Fish Res 42:1–20

    Article  Google Scholar 

  • García-Charton JA, Pérez-Ruzafa A, Sánchez-Jerez P et al (2004) Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on Western Mediterranean rocky reef fish assemblages. Mar Biol 144:161–182. doi:10.1007/s00227-003-1170-0

    Article  Google Scholar 

  • Griffiths CL, Hockey PAR (1987) A model describing the interactive roles of predation, competition and tidal elevation in structuring mussel populations. S Afr J Mar Sci 5:547–556. doi:10.2989/025776187784522496

    Article  Google Scholar 

  • Guichard F, Gouhier TC (2014) Non-equilibrium spatial dynamics of ecosystems. Math Biosci 255:1–10

    Article  Google Scholar 

  • Guichard F, Halpin PM, Allison GW et al (2003) Mussel disturbance dynamics: signatures of oceanographic forcing from local interactions. Am Nat 161:889–904. doi:10.1086/375300

    Article  Google Scholar 

  • Gutiérrez L (1998) Habitat selection by recruits establishes local patterns of adult distribution in two species of damselfishes: Stegastes dorsopunicans and S. planifrons. Oecologia 115:268–277. doi:10.1007/s004420050516

    Article  Google Scholar 

  • Hassell MP, Comins HN, May RM (1994) Species coexistence and self-organizing spatial dynamics. Nature 370:290–292. doi:10.1038/370290a0

    Article  Google Scholar 

  • Hazlett BA (1988) Behavioural plasticity as an adaptation to a variable environment. In Behavioral adaptation to intertidal life. NATO ASI Series. Series A, life sciences, vol 151. Springer, pp 317–332

  • Hazlett B, Acquistapace P, Gherardi F (2002) Differences in memory capabilities in invasive and native crayfish. J Crustac Biol 22:439–448. doi:10.1163/20021975-99990251

    Article  Google Scholar 

  • Hewitt JE, Thrush SF, Dayton PK, Bonsdorff E (2007) The effect of spatial and temporal heterogeneity on the design and analysis of empirical studies of scale-dependent systems. Am Nat 169:398–408. doi:10.1086/510925

    Article  Google Scholar 

  • Hollander J (2008) Testing the grain-size model for the evolution of phenotypic plasticity. Evolution (N Y) 62:1381–1389. doi:10.1111/j.1558-5646.2008.00365.x

    Google Scholar 

  • Kaehler S (1999) Incidence and distribution of phototrophic shell-degrading endoliths of the brown mussel Perna perna. Mar Biol 135:505–514

    Article  Google Scholar 

  • Kaehler S, McQuaid CD (1999) Lethal and sub-lethal effects of phototrophic endoliths attacking the shell of the intertidal mussel Perna perna. Mar Biol 133:497–503

    Article  Google Scholar 

  • Kostylev V, Erlandsson J (2001) A fractal approach for detecting spatial hierarchy and structure on mussel beds. Mar Biol 139:497–506

    Google Scholar 

  • Kostylev VE, Erlandsson J, Mak YM, Williams GA (2005) The relative importance of habitat complexity and surface area in assessing biodiversity: fractal application on rocky shores. Ecol Complex 2:272–286. doi:10.1016/j.ecocom.2005.04.002

    Article  Google Scholar 

  • Largaespada C, Guichard F, Archambault P (2012) Meta-ecosystem engineering: nutrient fluxes reveal intraspecific and interspecific feedbacks in fragmented mussel beds. Ecology 93:324–333. doi:10.1890/10-2359.1

    Article  Google Scholar 

  • Levin SA (1976) Population dynamic models in heterogeneous environments. Annu Rev Ecol Syst 7:287–310. doi:10.1146/annurev.es.07.110176.001443

    Article  Google Scholar 

  • Lima FP, Nicholas P. Burnett NP, Brian Helmuth B, Nicole Kish N, Kyle Aveni-Deforge K, Wethey DS (2011) Monitoring the intertidal environment with biomimetic devices, biomimetic based applications. In: Cavrak M (ed). ISBN: 978-953-307-195-4

  • Liu Q-X, Weerman EJ, Herman PMJ et al (2012) Alternative mechanisms alter the emergent properties of self-organization in mussel beds. Proc R Soc B Biol Sci 279:2744–2753. doi:10.1098/rspb.2012.0157

    Article  Google Scholar 

  • Liu Q-X, Doelman A, Rottschafer V et al (2013) Phase separation explains a new class of self-organized spatial patterns in ecological systems. Proc Natl Acad Sci USA 110:11905–11910. doi:10.1073/pnas.1222339110

    Article  CAS  Google Scholar 

  • Liu Q-X, Herman PMJ, Mooij WM et al (2014) Pattern formation at multiple spatial scales drives the resilience of mussel bed ecosystems. Nat Commun 5:5234. doi:10.1038/ncomms6234

    Article  CAS  Google Scholar 

  • McQuaid CD, Porri F, Nicastro KR, Zardi GI (2015) Simple, scale-dependent patterns emerge from very complex effects: an example from the intertidal mussels Mytilus galloprovincialis and Perna perna. Oceanogr Mar Biol 53:127–156

    Article  Google Scholar 

  • Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21. doi:10.2307/2937158

    Article  Google Scholar 

  • Mundy CN, Babcock RC (1998) Role of light intensity and spectral quality in coral settlement: implications for depth-dependent settlement? J Exp Mar Biol Ecol 223:235–255. doi:10.1016/S0022-0981(97)00167-6

    Article  Google Scholar 

  • Olff H, Alonso D, Berg MP et al (2009) Parallel ecological networks in ecosystems. Philos Trans R Soc Lond B Biol Sci 364:1755–1779. doi:10.1098/rstb.2008.0222

    Article  Google Scholar 

  • Patterson TA, Thomas L, Wilcox C et al (2008) State-space models of individual animal movement. Trends Ecol Evol 23:87–94

    Article  Google Scholar 

  • Petraitis PS (1995) The role of growth in maintaining spatial dominance by mussels (Mytilus edulis). Ecology 76:1337–1346. doi:10.2307/1940940

    Article  Google Scholar 

  • Petrović F, Guichard F (2008) Scales of Mytilus spp population dynamics: importance of adult displacement and aggregation. Mar Ecol Prog Ser 356:203–214

    Article  Google Scholar 

  • Plass-Johnson JG, McQuaid CD, Porri F (2010) Top–down effects on intertidal mussel populations: assessing two predator guilds in a South African marine protected area. Mar Ecol Prog Ser 411:149–159. doi:10.3354/meps08681

    Article  Google Scholar 

  • Porri F, McQuaid CD, Radloff S (2006) Spatio-temporal variability of larval abundance and settlement of Perna perna: differential delivery of mussels. Mar Ecol Prog Ser 315:141–150. doi:10.3354/meps315141

    Article  Google Scholar 

  • Porri F, Zardi GI, McQuaid CD, Radloff S (2007) Tidal height, rather than habitat selection for conspecifics, controls settlement in mussels. Mar Biol 152:631–637. doi:10.1007/s00227-007-0716-y

    Article  Google Scholar 

  • Porri F, Jordaan T, McQuaid CD (2008) Does cannibalism of larvae by adults affect settlement and connectivity of mussel populations? Estuar Coast Shelf Sci 79:687–693. doi:10.1016/j.ecss.2008.06.010

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Reaugh-Flower K, Branch GM, Harris JM, McQuaid CD, Currie B, Dye A, Robertson B (2011) Scale-dependent patterns and processes of intertidal mussel recruitment around southern Africa. Mar Ecol Prog Ser 434:101–119. doi:10.3354/meps09169

    Article  Google Scholar 

  • Richards CL, Bossdorf O, Muth NZ et al (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. doi:10.1111/j.1461-0248.2006.00950.x

    Article  Google Scholar 

  • Rochette R, Dill LM (2000) Mortality, behavior and the effects of predators on the intertidal distribution of littorinid gastropods. J Exp Mar Bio Ecol 253:165–191. doi:10.1016/S0022-0981(00)00253-7

    Article  Google Scholar 

  • Sardiña P, Cataldo DH, Boltovskoy D (2009) Effects of conspecifics on settling juveniles of the invasive golden mussel, Limnoperna fortunei. Aquat Sci 71:479–486. doi:10.1007/s00027-009-0103-5

    Article  Google Scholar 

  • Sexton JP, McKay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climates in North America. Ecol Appl 12:1652–1660. doi:10.1890/1051-0761(2002)012[1652:PAGDMA]2.0.CO;2

    Article  Google Scholar 

  • Siddon CE, Witman JD (2004) Behavioral indirect interactions: multiple predator effects and prey switching in the rocky subtidal. Ecology 85:2938–2945. doi:10.1890/03-0519

    Article  Google Scholar 

  • Siegel D, Mitarai S, Costello CJ et al (2008) The stochastic nature of larval connectivity among nearshore marine populations. Proc Natl Acad Sci USA 105:8974–8979. doi:10.1073/pnas.0802544105

    Article  CAS  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Bertness MD (2003) Trait-mediated effects in rocky intertidal food chains: predator risk cues alter prey feeding rates. Ecology 84:629–640. doi:10.1890/0012-9658(2003)084[0629:TMEIRI]2.0.CO;2

    Article  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, pp 1–522

    Google Scholar 

  • Underwood A, Chapman M (1996) Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107:212–224. doi:10.1007/BF00327905

    Article  Google Scholar 

  • Underwood AJ, Chapman MG, Connell SD (2000) Observations in ecology: you can’t make progress on processes without understanding the patterns. J. Exp. Mar. Bio. Ecol. 250:97–115

    Article  Google Scholar 

  • van de Koppel J, Rietkerk M, Dankers N, Herman PMJ (2005) Scale-dependent feedback and regular spatial patterns in young mussel beds. Am Nat 165:E66–E77. doi:10.1086/428362

    Article  Google Scholar 

  • van de Koppel J, Gascoigne JC, Theraulaz G et al (2008) Experimental evidence for spatial self-organization and its emergent effects in mussel bed ecosystems. Science (80) 322:739–742. doi:10.1126/science.1163952

  • Von Der Meden CEO, Porri F, McQuaid CD et al (2010) Fine-scale ontogenetic shifts in settlement behaviour of mussels: changing responses to biofilm and conspecific settler presence in Mytilus galloprovincialis and Perna perna. Mar Ecol Prog Ser 411:161–171. doi:10.3354/meps08642

    Article  Google Scholar 

  • Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100. doi:10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2

    Article  Google Scholar 

  • Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397. doi:10.2307/2389612

    Article  Google Scholar 

  • Williams GA (1994) The relationship between shade and molluscan grazing in structuring communities on a moderately-exposed tropical rocky shore. J Exp Mar Bio Ecol 178:79–95. doi:10.1016/0022-0981(94)90226-7

    Article  Google Scholar 

  • Williams GA, Morritt D (1995) Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Mar Ecol Prog Ser 124:89–103

    Article  Google Scholar 

  • Wootton JT (1992) Indirect effects, prey susceptibility, and habitat selection: impacts of birds on limpets and algae. Ecology 73:981–991

    Article  Google Scholar 

  • Wootton JT (2001) Local interactions predict large-scale pattern in empirically derived cellular automata. Nature 413:841–844. doi:10.1038/35101595

    Article  CAS  Google Scholar 

  • Zardi GI, Nicastro KR, McQuaid CD et al (2006) Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy. Mar Biol 150:79–88. doi:10.1007/s00227-006-0328-y

    Article  Google Scholar 

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Acknowledgments

We thank C.E.O von der Meden and T. Jordaan for assistance during the field collections and F.K. McQuaid and I. McQuaid and E. Yeruham for help in processing samples in the laboratory. Many thanks also go to V.J. Cole for advice on the statistical analyses. This study was funded by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) and SIDA/Sarec, Sweden. This contribution is based upon research supported by the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation.

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  1. Johan Erlandsson

    Present address: Department of Aquatic Resources, Institute of Coastal Research, Swedish University of Agricultural Sciences, Skolgatan 6, 74242, Öregrund, Sweden

Authors and Affiliations

  1. South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown, 6140, South Africa

    Francesca Porri

  2. Coastal Research Group, Department of Zoology and Entomology, Rhodes University, PO Box 94, Grahamstown, South Africa

    Francesca Porri & Christopher D. McQuaid

  3. Department of Systems Ecology, Stockholm University, 106 91, Stockholm, Sweden

    Johan Erlandsson

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  1. Francesca Porri
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  2. Christopher D. McQuaid
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Correspondence to Francesca Porri.

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Porri, F., McQuaid, C.D. & Erlandsson, J. The role of recruitment and behaviour in the formation of mussel-dominated assemblages: an ontogenetic and taxonomic perspective. Mar Biol 163, 157 (2016). https://doi.org/10.1007/s00227-016-2932-9

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