Abstract
Habitat loss and fragmentation, and biological invasions are widely considered the most significant threats to global biodiversity. While marine invasions have already shown dramatic impacts around the world’s coasts, many of these habitats are becoming increasingly urbanized, resulting in fragmentation of natural landscape worldwide. This study developed in Madeira (NE Atlantic) aims to understand the synergistic interactions between fragmentation and biological invasions using submerged experimental settlement panels in the field for 3 months. We fragmented crustose coralline habitats, decreasing patch size without an overall habitat loss, and determined its effects on the patterns of abundance of marine fouling organisms across limiting assemblages with or without the presence of non-indigenous species (NIS, considered invaded and non-invaded systems in this study). The presence of crustose coralline algae suppressed the recruitment of some NIS (Parasmitina alba and Botrylloides niger). Our results also showed that the abundance of NIS (e.g. B. niger) could be prompted in highly fragmented habitats, colonizing bare substrates very efficiently. Overall, evidence indicates that fragmentation events modulate biotic interactions and consequently determine the structure of the fouling communities. Future research should address both processes when analyzing biotic resistance to invasion in urban marine habitats.
Similar content being viewed by others
Availability of data and material
Data available on request from the authors.
References
Ahyong S, Costello MJ, Galil BS, Gollash S, Hutchins P, et al. (2018) World Register of Introduced Marine Species (WRiMS). Accessed at http://www.marinespecies.org/introduced on 2020–06.
Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol Annu Rev 45:345–405
Airoldi L, Turon X, Perkol-Finkel S, Rius M, Biologiche S (2015) Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Divers Distrib 21:755–768
Airoldi L, Beck MW, Firth LB, Bugnot AB, Steinberg PD et al (2021) Emerging solutions to return nature to the urban ocean. Ann Rev Mar Sci 13:445–477
Alves FMA, Chícharo LM, Serrão E, Abreu AD (2001) Algal cover and sea urchin spatial distribution at Madeira Island (NE Atlantic). Scientia Marina 65(4):383–392. https://doi.org/10.3989/scimar.2001.65n4383
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef Stat Ref Online:1–15
AquaNIS-Editorial-Board (2015) Information system on Aquatic Non-Indigenous and Cryptogenic Species. World Wide Web electronic publication. www.corpi.ku.lt/databases/aquanis. Version 2.36+. Accessed 2020–06
Arenas F, Sánchez I, Hawkins SJ, Jenkins SR (2006) The invasibility of marine algal assemblages: role of functional diversity and identity. Ecology 87:2851–2861
Benedetti-Cecchi L, Trussell GC (2014) Intertidal rocky shores. In: Bertness M, Bruno J, Silliman B, Stachowicz J (eds) Marine community ecology and conservation. Sinauer Associates, INC, pp 203–225
Bertocci I, Arenas F, Cacabelos E, Martins GM, Seabra MI et al (2017) Nowhere safe? Exploring the influence of urbanization across mainland and insular seashores in continental Portugal and the Azorean Archipelago. Mar Pollut Bull 114:644–655
Bertolini C, Montgomery W, O’Connor NE (2020) Edge effects are not linked to key ecological processes in a fragmented biogenic reef. Estuaries Coasts 43:708–721
Bianchi CN, Morri C, Sartoni G, Wirtz P (1998) Sublittoral epibenthic communities around Funchal. Bol Mus Mun Funchal 5:59–80
Bishop M, Mayer-Pinto M, Airoldid L, Firth LB, Morris RL, Loke LHL, Hawkins SJ, Naylor LA, Coleman RA, Chee SY, Dafforn KA (2017) Effects of ocean sprawl on ecological connectivity: impacts and solutions. J Exp Mar Biol Ecol 492:7–30
Bonaviri C, Fernandez TV, Fanelli G, Badalamenti F, Gianguzza P (2011) Leading role of the sea urchin Arbacia lixula in maintaining the barren state in southwestern Mediterranean. Mar Biol 158:2505–2513
Boström C, Pittman SJ, Simenstad C, Kneib RT (2011) Seascape ecology of coastal biogenic habitats: advances, gaps, and challenges. Mar Ecol-Prog Ser 427:191–217
Brown BL, Barney JN (2021) Rethinking biological invasions as a metacommunity problem. Front Ecol Evol. https://doi.org/10.3389/fevo.2020.584701
Bulleri F (2005) Experimental evaluation of early patterns of colonisation of space on rocky shores and seawalls. Mar Environ Res 60:355–374
Bulleri F, Bertocci I, Micheli F (2002) Interplay of encrusting coralline algae and sea urchins in maintaining alternative habitats. Mar Ecol Prog Ser 243:101–109
Cacabelos E, Martins GM, Thompson R, Prestes ACL, Azevedo MN et al (2016a) Material type and roughness influence structure of intertidal communities on coastal defenses. Mar Ecol 37:801–812
Cacabelos E, Martins GM, Thompson R, Prestes ACL, Azevedo MN et al (2016b) Factors limiting the establishment of canopy-forming algae on artificial structures. Estuar Coast Shelf Sci 181:277–283
Cadenasso ML, Pickett STA, Weathers KC, Jones CG (2003) A framework for a theory of ecological boundaries. Bioscience 53:750–758
Canning-Clode J (2015) Biological invasions in changing ecosystems. vectors, ecological impacts, management and predictions. De Gruyter, Berlin, p 488
Canning-Clode J, Fofonoff P, McCann L, Carlton JT, Ruiz G (2013) Marine invasions on a subtropical island: fouling studies and new records in a recent marina on Madeira Island (Eastern Atlantic Ocean). Aquat Invasions 8:261–270
Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77(6):1653–1655
Caselle JE, Davis K, Marks L (2018) Marine management affects the invasion success of a non - native species in a temperate reef system in California, USA. Ecol Lett 21:43–53
Chainho P, Fernandes A, Amorim A, Ávila SP, Canning-Clode J et al (2015) Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands. Estuar Coast Shelf Sci 167:199–211
Chapman ARO (1981) Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St. Margarets Bay, eastern Canada. Mar Biol 62:307–311
Cole VJ, Johnson LG, McQuaid CD (2012) Effects of Patch-Size on Populations of Intertidal Limpets, Siphonaria spp., in a Linear Landscape. PLoS One 7:e52076
Collinge SK (1996) Ecological consequences of habitat fragmentation: Implications for landscape architecture and planning. Landsc Urban Plan 36:59–77
Collinge SK (2009) Ecology of fragmented landscapes, Johns Hopk. Baltimore
Colomer J (2021) Serra T (2021) The world of edges in submerged vegetated marine canopies: from patch to canopy scale. Water 13:2430
Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315
Diamond JM (1975) The island dilemma: lessons of modern biogeographic studies for the design of natural reserves. Biol Cons 7:129–146
Didham RK (2010) Ecological consequences of habitat fragmentation. Encyclopedia of life sciences. John Wiley & Sons, Chichester
Didham R, Tylianakis JM, Gemmell NJ, Rand TA, Ewers RM (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2007.07.001
Dugan JE, Airoldi L, Chapman MG, Walker SJ, Schlacher T (2011) Estuarine and coastal structures: environmental effects, A focus on shore and nearshore structures. Treatise Estuar Coast Sci 8:17–41
Elo M, Kareksela S, Haapalehto T, Vuori H, Aapala K et al (2016) The mechanistic basis of changes in community assembly in relation to anthropogenic disturbance and productivity. Ecosphere 7(4):e01310
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
EU (2014) Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515
Filbee-Dexter K, Scheibling RE (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar Ecol Prog Ser 495:1–25
Fofonoff PW, Ruiz GM, Steves B, Simkanin C, Carlton JT (2018) National Exotic Marine and Estuarine Species Information System. http://invasions.si.edu/nemesis/. Accessed June 2020
Friedlander AM, Ballesteros E, Clemente S, Goncalves EJ, Estep A et al (2017) Contrasts in the marine ecosystem of two Macaronesian islands: a comparison between the remote Selvagens Reserve and Madeira Island. PLoS One 12:e0187935
Gallien L, Carboni M (2016) The community ecology of invasive species: where are we and what’s next? Ecography 40:335–352
Gestoso I, Ramalhosa P, Oliveira P, Canning-Clode J (2017) Marine protected communities against biological invasions : a case study from an offshore island. Mar Pollut Bull 119:72–80
Gestoso I, Ramalhosa P, Canning-Clode J (2018) Biotic effects during the settlement process of non-indigenous species in marine benthic communities. Aquat Invasions 13:247–259
Giakoumi S, Pey A (2017) Assessing the effects of marine protected areas on biological invasions: a global review. Front Mar Sci. https://doi.org/10.3389/fmars.2017.00049
Gizzi F, Jiménez J, Schafer S, Castro N, Costa S, Lourenço S, José R, Canning-Clode J, Monteiro J (2020) Before and after a disease outbreak: tracking a keystone species recovery from a mass mortality event. Mar Environ Res 156:1–8
Goodsell PJ, Chapman MG, Underwood AJ (2007) Differences between biota in anthropogenically fragmented habitats and in naturally patchy habitats. Mar Ecol Prog Ser 351:15–23
Gray JS (1997) Marine biodiversity: patterns, threats and conservation needs. Biodivers Conserv 6:153–175
Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A et al (2015) Habitat fragmentation and its lasting impact on earth’s ecosystems. Sci Adv 1:1–9
Hagen M, Kissling WD, Rasmussen C, De Aguiar MAM, Brown LE et al (2012) Biodiversity, species interactions and ecological networks in a fragmented world. Adv Ecol Res 46:89–210
Halpern B, Walbridge S, Selkoe KA, Kappel CV, Micheli F et al (2008) A global map of human impact on marine ecosystems. Science 319:948–952
Hernández JC, Clemente S, Sangil C, Brito A (2008) The key role of the sea urchin Diadema antillarum in controlling macroalgae assemblages throughout the Canary Islands (eastern subtropical Atlantic): an spatio-temporal approach. Mar Environ Res 66(2):259–270
Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337
Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current. Ecol Monogr 75:3–35
Howeth JG (2017) Native species dispersal reduces community invasibility by increasing species richness and biotic resistance. J Anim Ecol 86:1380–1393
Hughes TP (1994) Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science 265:1547–1551
Hutchison MAS (2008) Interactions between habitat fragmentation and invasions: factors driving exotic plant invasions in native forest remnants, West Coast. University of Canterbury, New Zealand
Jenkins SR, Martins GM (2010) Succession on hard substrata. In: Dürr S, Thomason JC (eds) Biofouling. Blackwell Publishing Ltd
Katsanevakis S, Wallentinus I, Zenetos A, Leppäkoski E, Çinar ME (2014) Impacts of invasive alien marine species on ecosystem services and biodiversity: a pan-European review. Aquat Invasions 9:391–423
Kohler K, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269
Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 80:15–26
Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1526
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz F (2000) Biotic invasions: causes, epidemiology, global consequences and control. Ecol Appl 10:689–710
Marchini A, Galil BS, Occhipinti-Ambrogi A (2015) Recommendations on standardizing lists of marine alien species: lessons from the Mediterranean Sea. Mar Pollut Bull 101:267–273
Martins GM, Neto AI, Cacabelos E (2016) Ecology of a key ecosystem engineer on hard coastal infrastructure and natural rocky shores. Mar Environ Res 113:88–94
Matias MG, Arenas F, Rubal M, Pinto IS (2015) Macroalgal composition determines the structure of benthic assemblages colonizing fragmented habitats. PLoS One 10:e0142289
Megina C, González-Duarte MM, López-González PJ, Piraino S (2013) Harbours as marine habitats: hydroid assemblages on sea-walls compared with natural habitats. Mar Biol 160:371–381
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492
Moschella PS, Abbiati M, Aberg P, Airoldi L, Anderson JM et al (2005) Low-crested coastal defence structures as artificial habitats for marine life: using ecological criteria in design. Coast Eng 52:1053–1071
Muricy and Tailor 2011 (listed twice), Herdman, 1886 and Huxley, 1855 are not references but authors of species. Checked in WORMS database. https://www.marinespecies.org/aphia.php?p=taxdetails&id=573180
Myers N, Mittermeier R, Mittermeier C, da Fonseca G, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Pardini R, Nichols E, Püttker T (2017) Biodiversity response to habitat loss and fragmentation. In: Encyclopedia of the Anthropocene. Elsevier Inc., pp 1–11
Price N (2010) Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia. Oecologia 163:747–758
Ramalhosa P, Gestoso I, Duarte B, Caçador I (2019) Metal pollution affects both native and non-indigenous biofouling recruitment in a subtropical island system. Mar Pollut Bull 141:373–386
Ramalhosa P, Gestoso I, Rocha RM, Lambert G, Canning-Clode J (2021) Ascidian biodiversity in the shallow waters of the Madeira Archipelago: Fouling studies on artificial substrates and new records. Reg Stud Mar Sci 43:101672
Reid WV, Mooney HA, Cropper A, Capistrano D, Carpenter SR et al. (2005) Ecosystems and Human Well-Being. Millennium Ecosystem Assessment Synthesis Report
Ries L, Sisk T (2004) A predictive model of edge effects. Ecology 85:2917–2926
Sangil C, Martins GM, Carlos J, Alves F, Neto AI et al (2018) Shallow subtidal macroalgae in the North-eastern Atlantic archipelagos (Macaronesian region): a spatial approach to community structure. Eur J Phycol 53:83–98
Sheets EA, Cohen CS, Ruiz GM, Rocha RM (2016) Investigating the widespread introduction of a tropical marine fouling species. Ecol Evol 6:2453–2471
Simberloff D (2009) The role of propagule pressure in biological invasions. Ann Rev Ecol Evol Syst 40:81–102. https://doi.org/10.1146/annurev.ecolsys.110308.120304
Simberloff D, von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32
Smoothey AF (2013) Habitat-associations of turban snails on intertidal and subtidal rocky reefs. PLos ONE 8:e61257
Stachowicz JJ, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262
Thompson RC, Crowe TP, Hawkins SJ (2002) Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environ Conserv 29:168–191
Tsiamis K, Palialexis A, Stefanova K, Ničević Ž, Skejić S et al (2019) Non-indigenous species refined national baseline inventories : a synthesis in the context of the European Union ’ s Marine Strategy Framework Directive. Mar Pollut Bull 145:429–435
Tuya F, Boyra A, Sanchez-Jerez P, Barbera C, Haroun RJ (2004) Relationships between rocky-reef fish assemblages, the sea urchin Diadema antillarum and macroalgae throughout the Canarian Archipelago. Mar Ecol Prog Ser 278:157–169
Vermeij MJA, Dailer ML, Smith CM (2011) Crustose coralline algae can suppress macroalgal growth and recruitment on Hawaiian coral reefs. Mar Ecol Prog Ser 422:1–7
Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-induced global change. N Z J Ecol 21:1–16
Wilcove DS, McLellan CH, Dobson AP (1986) Habitat fragmentation in the temperate zone. In: Conservation biology: the science of scarcity and diversity. Sinauer Associates, INC, Sunderland, MA: Sinauer, p 237–256
Wilson MC, Richard XC, Didham RK, Ding P, Holt RD et al (2016) Habitat fragmentation and biodiversity conservation : key findings and future challenges. Landsc Ecol 31:219–227
With KA (2002) The landscape ecology of invasive spread. Conserv Biol 16:1192–1203
With KA (2004) Assessing the risk of invasive spread in fragmented landscapes. Risk Anal 24:803–815
Wirth R, Meyer ST, Leal IR, Tabarelli M (2008) Plant herbivore interactions at the forest edge. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany 69:423–448. Springer, Berlin Heidelberg.
WoRMS Editorial Board 2020. World Register of Marine Species. Available from https://www.marinespecies.org at VLIZ. Accessed 2020–06. doi:https://doi.org/10.14284/170
Acknowledgements
The authors are grateful to Janina Beltz and João Ladeira for their help during the preparation of the experimental units, and the two anonymous reviewers for their comments and suggestions, which greatly improved the quality of this work. This work was partially funded by projects MIMAR (MAC/4.6.d/066) and MIMAR+ (MAC2/4.6d/249), in the framework of INTERREG MAC 2014-2020 Programme. EC and IGG were financially supported by post-doctoral grants in the framework of the 2015 ARDITI Grant Programme Madeira 14-20 (Project M1420-09-5369-FSE-000002). I.G. is supported financially by a Maria Zambrano contract UCA under the grants call for the requalification of the Spanish university system 2021-2023, funded by the European Union—NextGenerationEU. PR was partially funded by the Project Observatório Oceânico da Madeira-OOM (M1420-01-0145-FEDER-000001), co-financed by the Madeira Regional Operational Programme (Madeira 14-20), under the Portugal 2020 strategy, through the European Regional Development Fund (ERDF) and currently funded by project MARE-Centro de Ciências do Mar e do Ambiente (UIDB/04292/2020). JCC is funded by national funds through FCT—Fundação para a Ciência e a Tecnologia, I.P., under the Scientific Employment Stimulus—Institutional Call—[CEECINST/00098/2018]. Finally, this study also had the support of Fundação para a Ciência e Tecnologia (FCT), through the strategic project [UIDB/04292/2020] granted to MARE. This is contribution 97 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network.
Funding
This work was partially funded by projects MIMAR (MAC/4.6.d/066) and MIMAR + (MAC2/4.6d/249), in the framework of INTERREG MAC 2014–2020 Programme. EC and IGG were financially supported by post-doctoral grants in the framework of the 2015 ARDITI Grant Programme Madeira 14–20 (Project M1420-09–5369-FSE-000002). IGG is supported financially by a Maria Zambrano contract UCA under the grants call for the requalification of the Spanish university system 2021–2023, funded by the European Union—NextGenerationEU. PR was partially funded by the Project Observatório Oceânico da Madeira-OOM (M1420-01–0145-FEDER-000001), co-financed by the Madeira Regional Operational Programme (Madeira 14–20), under the Portugal 2020 strategy, through the European Regional Development Fund (ERDF) and currently funded by project MARE-Centro de Ciências do Mar e do Ambiente (UIDB/04292/2020). JCC is funded by national funds through FCT—Fundação para a Ciência e a Tecnologia, I.P., under the Scientific Employment Stimulus—Institutional Call—[CEECINST/00098/2018]. Finally, this study also had the support of Fundação para a Ciência e Tecnologia (FCT), through the strategic project [UIDB/04292/2020] granted to MARE. This is contribution 97 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network.
Author information
Authors and Affiliations
Contributions
EC: Conceptualization, Investigation, Data curation, Formal analysis, Writing—original draft, Writing—review and editing. IG: Conceptualization, Methodology, Investigation, Data curation, Writing—review and editing. PR: Methodology, Investigation, Data curation, Writing—review and editing. JC-C: Funding acquisition, Writing—review and editing.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cacabelos, E., Gestoso, I., Ramalhosa, P. et al. Role of non-indigenous species in structuring benthic communities after fragmentation events: an experimental approach. Biol Invasions 24, 2181–2199 (2022). https://doi.org/10.1007/s10530-022-02768-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-022-02768-9