Skip to main content

Advertisement

Log in

Decline of a non-native ecosystem engineer and its replacement with a native on rocky shores: effects on the diversity and structure of benthic communities

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

Ecosystem engineer species create enhanced habitat resources, and therefore host exceptionally diverse communities. We studied the case of two ecosystem engineers: a non-native ascidian, Pyura praeputialis, and the native mussel, Perumytilus purpuratus, in the rocky shores of Antofagasta Bay, northern Chile. P. praeputialis was once dominant in mid- and low-intertidal zones, but human harvesting has severely reduced the extent of the P. praeputialis band, allowing for competition from P. purpuratus, which subsequently expanded and replaced P. praeputialis. We compared the macrobenthic community structure between these two ecosystem engineers at five sites throughout the bay. Our results suggest not only an important share of species composition between the ecosystem engineers (68.1%) but also dissimilarity due to differential changes in taxa abundance. Taxonomic richness and diversity were always high in both ecosystem engineers when analyzing communities in areas without these engineers. Diversity recorded in P. praeputialis was slightly higher than those in P. purpuratus; however, the re-establishment of the native mussel could prevent a substantial drop in diversity as the invasive bioengineer disappears. From a biogeographical standpoint, all recorded taxa associated with both ecosystem engineers were native, thus allowing us to conclude that P. praeputialis did not further facilitate the presence of invasive species; rather, this bioengineer could be considered a reservoir of native fauna. Our study highlights the importance of the coexistence of multiple ecosystems engineers and their interactions in the maintenance of biodiversity in rocky shores, especially in cases where human disturbance reduces the more dominant but invasive ecosystem engineer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Altieri AH, van de Koppel J (2014) Foundation species in marine ecosystems. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) Marine community ecology and conservation. Sinauer Associates, Sunderland, MA, pp 37–56

    Google Scholar 

  • Altieri AH, Witman JD (2014) Modular mobile foundation species as reservoirs of biodiversity. Ecosphere 5(10):124

    Google Scholar 

  • Altieri AH, van Wesenbeeck BK, Bertness MD, Silliman BR (2010) Facilitation cascade drives positive relationship between native biodiversity and invasion success. Ecology 91:1269–1275

    PubMed  Google Scholar 

  • Alvarado JL, Castilla JC (1996) Tridimensional matrices of mussels Perumytilus purpuratus on intertidal platforms with varying wave forces in Central Chile. Mar Ecol Prog Ser 133:135–141

    Google Scholar 

  • Alvarado JL, Pinto R, Marquet P, Pacheco C, Guiñez R, Castilla JC (2001) Patch recolonization by the tunicate Pyura praeputialis in the rocky intertidal of the bay of Antofagasta, Chile: evidence for self-facilitation mechanisms. Mar Ecol Prog Ser 224:93–101

    Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32–46

    Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. BioScience 61:782–789

    Google Scholar 

  • Arribas LP, Donnarumma L, Gabriela Palomo M, Scrosati RA (2014) Intertidal mussels as ecosystem engineers: their associated invertebrate biodiversity under contrasting wave exposures. Mar Biodivers 44(2):203–211

    Google Scholar 

  • Ashton T, Riascos JM, Pacheco A (2008) First record of Cymatium keenae Beu, 1970 (Mollusca: Ranellidae) from Antofagasta bay, northern Chile, in connection with El Niño events. Helgol Mar Res 62(Suppl 1):S107–S110

    Google Scholar 

  • Borsje BW, van Wesenbeeck BK, Dekker F, Paalvast P, Bouma TJ, van Katwijk MM, de Vries MB (2011) How ecological engineering can serve in coastal protection. Ecol Eng 73:113–122

    Google Scholar 

  • Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, MA, pp 201–220

    Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18(3):119–125

    Google Scholar 

  • Bulleri F, Bruno JF, Silliman BR, Stachowicz JJ (2016) Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning. Funct Ecol 30:70–78

    Google Scholar 

  • Buschbaum C, Dittmann S, Hong JS, Hwang IS, Strasser M, Thiel M, Valdivia N, Yoon SP, Reise K (2009) Mytilid mussels: global habitat engineers in coastal sediments. Helgol Mar Res 63:47–58

    Google Scholar 

  • Byers JE (2002) Impact of non-indigenous species enhanced by anthropogenic alteration of selection regimes. Oikos 97:449–458

    Google Scholar 

  • Caro AU, Guiñez R, Ortiz V, Castilla JC (2011) Competition between a native mussel and a non-indigenous invader for primary space on intertidal rocky shores in Chile. Mar Ecol Prog Ser 428:177–185

    Google Scholar 

  • Castilla JC, Neill PE (2009) Marine bioinvasions in the southeastern Pacific: status, ecology, economic impacts, conservation and management. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems, ecological studies 204. Springer-Verlag, Berlin, Heidelberg, pp 439–457

    Google Scholar 

  • Castilla JC, Collins AG, Meyer CP, Guiñez R, Lindbergs DR (2002) Recent introduction of the dominant tunicate, Pyura praeputialis (Urochordata, Pyuridae) to Antofagasta, Chile. Mol Ecol 11:1579–1584

    CAS  PubMed  Google Scholar 

  • Castilla JC, Lagos NA, Cerda M (2004a) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130

    Google Scholar 

  • Castilla JC, Guiñez R, Caro AU, Ortiz V (2004b) Invasion of a rocky intertidal shore by the tunicate Pyura praeputialis in the Bay of Antofagasta, Chile. Proc Natl Acad Sci U S A 101(23):8517–8524

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castilla JC, Uribe M, Bahamonde N, Clarke M, Desqueyroux-Faúndez R, Kong I, Moyano H, Rozbaczylo N, Santelices B, Valdovinos C, Zavala P (2005) Down under the southeastern Pacific: marine non-indigenous species in Chile. Biol Invasions 7(2):213–232

    Google Scholar 

  • Castilla JC, Manríquez PH, Delgado AP, Gargallo L, Leiva A, Radic D (2007) Bio-foam enhances larval retention in a free-spawning marine tunicate. Proc Natl Acad Sci U S A 104(46):18120–18122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castilla JC, Manríquez PH, Delgado A, Ortiz V, Jara ME, Varas M (2014) Rocky intertidal zonation pattern in Antofagasta, Chile: invasive species and shellfish gathering. PLoS One 9(10):e110301

    PubMed  PubMed Central  Google Scholar 

  • Cerda M, Castilla JC (2001) Diversity and biomass of macro-invertebrates in intertidal matrices of the tunicate Pyura praeputialis (Heller, 1878) in the Bay of Antofagasta, Chile. Rev Chil Hist Nat 74:841–853

    Google Scholar 

  • Clarke KR, Gorley RN (2015) PRIMER v7: User manual tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Clarke KR, Warwick RM (1998) Quantifying structural redundancy in ecological communities. Oecologia 113:278–289

    CAS  PubMed  Google Scholar 

  • Clarke M, Ortiz V, Castilla JC (1999) Does early development of the Chilean tunicate Pyura praeputialis (Heller, 1878) explain the restricted distribution of the species? Bull Mar Sci 65(3):745–754

    Google Scholar 

  • Coleman FC, Williams SL (2002) Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends Ecol Evol 17(1):40–44

    Google Scholar 

  • Crain CM, Bertness MD (2006) Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56(3):211–218

    Google Scholar 

  • Davis AR, Walls K, Jeffs A (2018) Biotic consequences of a shift in invertebrate ecosystem engineers: invasion of New Zealand rocky shores by a zone-forming ascidian. Mar Ecol. 39(3): e12502

    Google Scholar 

  • Dayton PK (1972) Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound. In: Parker BC (ed) Proceedings of the colloquium on conservation problems in Antarctica. Allen Press, pp 81–95

  • Donadi S, van der Heide T, Piersma T, van der Zee EM, Weerman EJ, van de Koppel J, Olff H, Devine C, Hernawan UE, Boers M, Planthof L, Eriksson BK (2015) Multi-scale habitat modification by coexisting ecosystem engineers drives spatial separation of macrobenthic functional groups. Oikos 124:1502–1510

    Google Scholar 

  • Eklöf JS, Donadi S, van der Heide T, van der Zee EM, Eriksson BK (2015) Effects of antagonistic ecosystem engineers on macrofauna communities in a patchy, intertidal mudflat landscape. J Sea Res 97:56–65

    Google Scholar 

  • Escribano R, Rosales SA, Blanco JL (2003) Understanding upwelling circulation off Antofagasta (northern Chile): a three-dimensional numerical-modeling approach. Cont Shelf Res 24:37–53

    Google Scholar 

  • Field JG, Clarke KR, Warwick RM (1982) A practical strategy for analyzing multispecies distribution patterns. Mar Ecol Prog Ser 8:37–52

    Google Scholar 

  • Gillis LG, Bouma TJ, Jones CG, van Katwijk MM, Nagelkerken I, Jeuken CJL, Herman PMJ, Ziegler AD (2014) Potential for landscape-scale positive interactions among tropical marine ecosystems. Mar Ecol Prog Ser 503:289–303

    Google Scholar 

  • Guiñez R, Castilla JC (1999) A tridimensional self-thinning model for multilayered intertidal mussels. Am Nat 154:341–357

    PubMed  Google Scholar 

  • Gutiérrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90

    Google Scholar 

  • Guzman N, Saá S, Ortlieb L (1998) Descriptive catalogue of nearshore molluscs (Gastropoda and Pelecypoda) from Antofagasta area, 23°S (Chile). Estud Oceanol 17:17–86

    Google Scholar 

  • Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241

    PubMed  Google Scholar 

  • Häussermann V, Försterra G (eds) (2009) Marine benthic fauna of Chilean Patagonia. Nature in Focus, Puerto Montt, 1000 pp

    Google Scholar 

  • Jones CG, Lawton JH, Shachk M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Google Scholar 

  • Keen AM (1971) Seashells of tropical West America. Stanford University Press, Stanford (California), 1064 pp

    Google Scholar 

  • Liu QX, Herman PMJ, Mooij WM, Huisman J, Scheffer M, Olff H, van de Koppel J (2014) Pattern formation at multiple spatial scales drives the resilience of mussel bed ecosystems. Nat Commun 5:5234

  • Marincovich L (1973) Intertidal mollusks of Iquique, Chile, vol 16. Natural History Museum of Los Angeles County, Los Angeles, CA, pp 1–49

    Google Scholar 

  • Menge BA, Branch GM (2001) Rocky intertidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sunderland, MA, Sinauer Associates, Inc, pp 221–251

    Google Scholar 

  • Monteiro SM, Chapman MG, Underwood AJ (2002) Patches of the ascidian Pyura stolonifera (Heller, 1878): structure of habitat and associated intertidal assemblages. J Exp Mar Biol Ecol 270:171–189

    Google Scholar 

  • Moreno RA, Neill PE, Rozbaczylo N (2006) Native and non-indigenous boring polychaetes in Chile: a threat to native and commercial mollusk species. Rev Chil Hist Nat 79:263–278

    Google Scholar 

  • Orensanz JM, Schwindt E, Pastorino G, Bortolus A, Casas G, Darrigran G, Elías R, López Gappa JJ, Obenat S, Pascual M, Penchaszadeh P, Piriz ML, Scarabino F, Spivak ED, Vallarino EA (2002) No longer the pristine confines of the world ocean: a survey of exotic marine species in the southwestern Atlantic. Biol Invasions 4:115–143

    Google Scholar 

  • Paine RT, Suchanek TH (1983) Convergence of ecological processes between independently evolved competitive dominants: a tunicate-mussel comparison. Evolution 37(4):821–831

    CAS  PubMed  Google Scholar 

  • Piñones A, Castilla JC, Guiñez R, Largier JL (2007) Nearshore surface temperatures in Antofagasta Bay (Chile) and adjacent upwelling centers. Cienc Mar 33:37–48

    Google Scholar 

  • Prado L, Castilla JC (2006) The bioengineer Perumytilus purpuratus (Mollusca: Bivalvia) in Central Chile: biodiversity, habitat structural complexity and environmental heterogeneity. J Mar Biol Assoc UK 86:417–421

    Google Scholar 

  • Rius M, Teske PR, Manríquez PH, Suárez-Jimenez R, Mcquaid CD, Castilla JC (2017) Ecological dominance along rocky shores, with a focus on intertidal ascidians. Oceanogr Mar Biol 55:2–33

    Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939

    Google Scholar 

  • Rozbaczylo N (1980) Clave para el reconocimiento de familias de anélidos poliquetos del mar chileno. Stud Neotropical Fauna Environ 15:167–196

    Google Scholar 

  • Sueiro MC, Bortolus A, Schwindt E (2011) Habitat complexity and community composition: relationships between different ecosystem engineers and the associated macroinvertebrate assemblages. Helgol Mar Res 65(4):467–477

    Google Scholar 

  • Tapia L (2002) Algas, Guía de biodiversidad No. 4, vol. 1 Macrofauna y algas marinas. Universidad de Antofagasta, Centro regional de estudios y educación ambiental, Chile. 64 pp

  • Thiel M, Ullrich N (2002) Hard rock versus soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile, and considerations on the functional role of mussel beds. Helgol Mar Res 56:21–30

    Google Scholar 

  • Watt CA, Scrosati RA (2013) Bioengineer effects on understory species richness, diversity, and composition change along an environmental stress gradient: experimental and mensurative evidence. Estuar Coast Shelf Sci 123:10–18

    Google Scholar 

  • Zuñiga O (2002) Crustáceos, Guía de biodiversidad No. 2, vol 1 Macrofauna y algas marinas. Universidad de Antofagasta, Centro regional de estudios y educación ambiental, Chile. 71 pp

Download references

Acknowledgments

Partial results of this study were presented as part of the Marine Ecology degree of D. A. Andrade. We deeply thank M. Malebran and M. Fajardo for helping during sampling and for providing much taxonomic advice. Two anonymous reviewers helped us to improve an early version of this manuscript. K. Plummer kindly revised the English of this manuscript.

Funding

Partial support for sampling was provided by FONDECYT grants No. 11110030 and 1150042 granted to A. S. Pacheco.

Author information

Authors and Affiliations

Authors

Contributions

ASP designed the study; DGA conducted the sampling and laboratory analysis; ASP and DGA performed statistical analysis; ASP wrote the manuscript; ASP and DGA prepared the figures and Tables. Both authors reviewed the manuscript and approved the final article.

Corresponding author

Correspondence to Aldo S. Pacheco.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for animal testing, animal care, and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities.

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Additional information

Communicated by P. Lana

Publisher’s note

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

Electronic supplementary material

ESM1

(XLSX 30 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pacheco, A.S., Andrade, D.G. Decline of a non-native ecosystem engineer and its replacement with a native on rocky shores: effects on the diversity and structure of benthic communities. Mar. Biodivers. 50, 2 (2020). https://doi.org/10.1007/s12526-019-01033-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12526-019-01033-y

Keywords

Navigation