75 Nawrot Et Al. 2015.Pdf

Diversity and Distributions, (Diversity Distrib.) (2015) 21, 1075–1086 BIODIVERSITY What guides invasion success? Ecological RESEARCH correlates of arrival, establishment and spread of Red Sea bivalves in the Mediterranean Sea Rafał Nawrot1*, Devapriya Chattopadhyay2 and Martin Zuschin1 1Department of Palaeontology, University of ABSTRACT Vienna, Althanstrasse 14, Vienna 1090, Aim The opening of the Suez Canal in 1869 re-established the direct link Austria, 2Department of Earth Sciences, between long-separated biogeographic realms, allowing hundreds of marine Indian Institute of Science Education and Research (IISER) Kolkata, Mohanpur, species to spread from the Red Sea to the Mediterranean. We use marine bival- WB-741246, India ves to relate species-level attributes to successful transition through successive stages of the invasion process. Location Mediterranean and Red Sea. Methods We compiled data on taxonomic composition, body size, life habit A Journal of Conservation Biogeography and geographic distribution of the Red Sea bivalve fauna from published litera- ture, museum collections and our own field surveys. Using multimodel infer- ence, we examined selectivity of the Lessepsian invasion and identify traits that distinguish successful species at three major stages of invasion: arrival, establishment and spread. Results The upper limit of bathymetric range and occurrence outside the tropical zone in other regions are the strongest predictors of successful transition through the Suez Canal. Establishment in the Mediterranean is positively corre- lated with earlier arrival and association with hard-bottom habitats. Preference for hard substrates together with large body size is the primary factor distin- guishing invasive aliens representing a significant threat to recipient ecosystems from other established species. Main conclusions The relative strength of abiotic and biotic filters changes along the course of the invasion: environmental affinity and climate match con- strain the pool of potential invaders, while the establishment in the new region and invasive status depend on the habitat preferences and life history traits of aliens, affecting their interactions with resident species. Our results together with previous studies suggest that the eastern Mediterranean rocky shores are more susceptible to the establishment of Lessepsian species, many of which may induce strong pressure on recipient communities as ecosystems engineers and competitors of native species. *Correspondence: Rafał Nawrot, Department and Distributions Keywords of Palaeontology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria. Alien species, biological invasions, biotic interchange, invasive species, Lessep- E-mail: [email protected] sian migration, marine invasions, Mollusca. into a global hotspot of marine bioinvasions (Rilov & Galil, INTRODUCTION 2009; Por, 2010; Edelist et al., 2013). This so-called Lessep- The opening of the Suez Canal in 1869 re-established the sian or Erythrean invasion (Por, 1971; Rilov & Galil, 2009; direct link between biogeographic realms separated since the Safriel, 2013) has led to profound changes in marine com- Diversity Middle Miocene and allowed hundreds of tropical species to munities of the eastern Mediterranean, which are now often spread from the Red Sea to the Mediterranean, turning it dominated by Red Sea taxa (Galil, 2007; Edelist et al., 2013; DOI: 10.1111/ddi.12348 ª 2015 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/ddi 1075 R. Nawrot et al. Rilov, 2013). In contrast to other human-mediated invasions, We use information on taxonomic composition, bathy- the Lessepsian invasion encompasses whole complexes of metric and geographic distribution, body size and life habits species that are sympatric in their native range (Por, 2010) of the Red Sea bivalve fauna to quantitatively examine the and maintain high levels of gene flow between their newly biological selectivity of the consecutive stages of the Lessep- established and parent populations (Bernardi et al., 2010). sian invasion. We attempt to determine which characteristics Although the introduction of some Red Sea species is of the Red Sea species predispose them to enter the Mediter- undoubtedly facilitated by maritime transport (Shefer et al., ranean Sea and thrive there, and how particular traits of suc- 2004), for most of them, the natural dispersal through the cessful immigrants affect their post-establishment spread and Suez Canal and along the Mediterranean coasts remains the impact on native communities. primary means of range expansion (Gofas & Zenetos, 2003; Ben Rais Lasram et al., 2008; Tzomos et al., 2012). METHODS The Lessepsian invasion can be regarded as a unique biogeographic experiment (Por, 2010) that shares many simi- Data collection larities with large-scale biotic interchanges in the geological past (Vermeij, 2005). It can thus serve as a model system for We compiled a database on body size and ecological charac- comparing marine invasions in natural and anthropogenical- teristics of 394 bivalve species occurring at continental shelf ly altered ecosystems. Moreover, identification of factors depths (<200 m) in the Red Sea (see Appendix S1 in Sup- contributing to the invasion process may help to alleviate the porting Information). Data were collected from primary lit- threats it poses to native biodiversity and human economy erature, major monographs and museum collections (see (Streftaris & Zenetos, 2006; Galil, 2007; Katsanevakis et al., Appendix S2). Substantial information was derived from 2014). Oliver (1992), Dekker & Orlin (2000), Huber (2010) and Molluscs, with over 200 alien species, are currently the from our own field studies (Zuschin & Oliver, 2003, 2005; most species-rich animal phylum among non-native taxa in Zuschin & Ebner, 2015). Taxonomic nomenclature was pri- the Mediterranean Sea (Zenetos et al., 2012). In this study, marily based on the World Register of Marine Species we focus on marine bivalves, which are routinely used as a (WoRMS Editorial Board, 2014). Teredinid bivalves (12 spe- model clade in macroecological and macroevolutionary cies) were excluded from the analyses. This group is poorly studies (e.g. Roy et al., 2000; Vermeij et al., 2008; Berke studied in the Red Sea and may include cryptogenic species. et al., 2013), and encompass some of the most notorious Species of Red Sea origin that are non-indigenous to the invasive species (Streftaris & Zenetos, 2006; Katsanevakis Mediterranean fauna were identified based on the inventories et al., 2014). Taxonomic identity and distribution of Lessep- of Gofas & Zenetos (2003) and Zenetos et al. (2010, 2012), sian bivalves in the Mediterranean Sea is well documented updated with the most recent records (Appendix S2). We (Gofas & Zenetos, 2003; Zenetos et al., 2010; Tzomos et al., did not attempt to differentiate between species spreading 2012), and our knowledge about the ecology and biology of through the Suez Canal by natural means of dispersal, that is selected species is continuously expanding (e.g. Rilov et al., ‘true’ Lessepsian migrants sensu Por (1971), and those pas- 2004; Zurel et al., 2012). Nonetheless, the strong focus of sively introduced by ships. For many species, both vectors previous studies on just a few of the most conspicuous may operate simultaneously, especially during their second- immigrants (reviewed by Safriel, 2013) is hindering our ary spread within the Mediterranean Sea (e.g. Shefer et al., ability to understand the dynamics of the entire invasion 2004; Galil, 2008). We use the term Lessepsian species in a process. We therefore address the biological correlates of the broad sense to denote all Red Sea species that have pene- Lessepsian invasion in the whole pool of potential bivalve trated through the Suez Canal. The three cosmopolitan spe- immigrants. cies Perna perna (Linnaeus, 1758), Irus irus (Linnaeus, 1758) The invasion is a multistage process (Blackburn et al., and Martesia striata (Linnaeus, 1758) were considered native 2011) in which the effect of any particular trait on the spe- to both regions and excluded from the source pool of cies’ success may change depending on the stage at which it invaders. is evaluated (Cassey et al., 2004; Jeschke & Strayer, 2006). The information on the acclimatization status of Lessep- Accordingly, proper delineation of the species pool and an sian species was taken from Zenetos et al. (2010, 2012) rep- appropriate control group at each successive stage is a prere- resenting the most comprehensive overview of marine alien quisite for the identification of factors promoting or imped- species in the Mediterranean Sea currently available (see also ing success of alien species (Cassey et al., 2004; Miller & Appendix S2 for supplementary sources). Their classification Ruiz, 2009). Three stages of the Lessepsian invasion can be of alien species can be easily incorporated into the multistage distinguished following the modified framework of Black- framework for biological invasions of Blackburn et al. burn et al. (2011): (1) arrival of a Red Sea species to the (2011). We considered all Red Sea bivalves with confirmed Mediterranean Sea, (2) establishment of a viable alien popu- records in the Mediterranean Sea as alien (i.e., Lessepsian) lation, and (3) population growth and spread, imposing a species that successfully completed the arrival stage. Depend- considerable impact on native communities (see also discus- ing on the successful establishment of free-living and

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