A novel marine bioinvasion vector: Ichthyochory, live passage through fish

Many species of Indo-Pacific holobenthic foraminifera have been introduced and successfully established sustainable populations in the Mediterranean Sea over the past few decades. However, known natural and anthropogenic vectors do not explain how these species were introduced long distances from their origin. We present evidence for a novel marine bioinvasion vector explaining this long-distance transport and introduction using both contemporary field and historical analyses. In 2015–2016, we found living specimens of 29 foraminiferal species in the fecal pellets of two Red Sea herbivorous rabbitfish—Siganus rivulatus and Siganus luridus in the Mediterranean. In our historical analysis, we found 34 foraminiferal species in preserved Red Sea rabbitfish specimens, dating between 1967 and 1975. In addition, we found congruent propagation patterns of the non-indigenous rabbitfish and foraminifera, lagging 4–11 yrs between discoveries, respectively. Predation of marine benthos by non-indigenous fish, followed by incomplete digestion and defecation of viable individuals, comprise the main introduction vector of these organisms into novel environments. *Correspondence: [email protected] Present address: GEOMAR, Helmholtz Centre of Ocean Research Kiel, Marine Ecology, Germany. Author Contribution Statement: The study was conceived by TGH and OHK. TGH led and designed the study. TGH and EY performed the experiments. OHK and AAL conducted the taxonomic analysis. TGH and OHK analyzed the data. TGH, OHK, EY, AAL and JTC developed the conceptual framework and drafted the manuscript. Data Availability Statement: Data supporting the results are archived at doi:10.1594/PANGAEA.872632. T.G.-H. and O.H.-K contributed equally to this work. Additional Supporting Information may be found in the online version of this article. This is an open access article under the terms of the Creative Commons Attribution NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Scientific Significance Statement Bioinvasions, the expansions of species into regions outside their native range, threaten biodiversity, and human livelihood worldwide. In the sea, international shipping has been considered the primary vector for the introduction of these nonindigenous species, although in many cases the specific vector is not known nor well understood. We present evidence for a novel bioinvasion vector that can explain the appearance and dispersal of dozens of benthic non-indigenous species in the Mediterranean Sea—that of live passage through fish digestive tracts (ichthyochory). This newly identified vector should be considered when evaluating both the history of prior invasions and the potential vectors of future invasions world-wide. 80 Limnology and Oceanography Letters 2, 2017, 80–89 VC 2017 The Author. Limnology and Oceanography Letters published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lol2.10039 Non-indigenous species (NIS) are increasingly being discovered in terrestrial, freshwater, and marine habitats, altering community structure and ecosystem functions (Simberloff 2001; Sanders et al. 2003; Lowry et al. 2013). Nevertheless, the vectors of NIS introduction often remain obscure. In the sea, human-mediated transport mechanisms, primarily vessel hull fouling and ballast water, fisheries, aquaculture, and canals (Ruiz and Carlton 2003), are known to play important roles in NIS dispersal. However, none of these vectors explain the invasion of at least 68 benthic foraminifera NIS from the Red Sea into the Mediterranean Sea over the past decades (Zenetos et al. 2012; Weinmann et al. 2013). Since the opening of the Suez Canal in 1869, hundreds of NIS from the Red Sea have been recorded in the Mediterranean Sea (Galil et al. 2015). The unidirectional advancement of Red Sea species via the canal is termed “Lessepsian migration” and the Red Sea NIS are termed “Lessepsian migrants,” after Ferdinand de Lesseps, the French diplomat who was in charge of the canal’s construction (Por 1978). The Lessepsian migrants moved with currents or under their own volition, as well as by vessel-mediated transport. Many benthic organisms are meroplanktonic, undergoing a larval planktonic phase, and thus are potentially capable of dispersing long distances, including travelling through waterways. Most benthic foraminifera, however, are holobenthic, being permanent bottom-dwellers in sediments, on rocks, or as epiphytes on seaweeds and seagrass, with no planktonic stage (Hyams-Kaphzan et al. 2008). Although capable of active movement across surfaces, benthic foraminifera speedrates range between 1.8 mm h and 8.4 mm h (Kitazato 1988). It would thus take a persistent foraminiferal species about 4000 yrs to “walk” the 164 km long Suez Canal. Several mechanisms have been proposed to explain the range expansions of benthic foraminifera (Alve 1999): ballast water taking up suspended foraminifera stirred up from sediments (McGann et al. 2000), passive dispersal by currents and sediment transport (Alve and Goldstein 2010), attachment to gastropod veliger shells (Nesbitt 2005), ship hull fouling (Gollasch 2002), rafting on marine plants or debris (Winston 2012), and movement with aquaculture products (Cohen 2012). To date, no data have been found to support any of these hypotheses to explain new invasions of rocky substrate or epiphytic foraminifera. First, while foraminifera are known from ballast water and ballast sediments, these are in large part species associated with soft-sediment habitats, as are the few other foraminifera invasions in other regions of the world (McGann et al. 2000). Second, an extensive 10-yr survey of ballast protist communities of cargo vessels arriving in Israeli Mediterranean ports did not reveal any of the known benthic foraminifera NIS (Galil and H€ ulsmann 1997). Third, dispersal by juvenile drifting or rafting are less probable vectors as the westward propagation of benthic foraminifera NIS in the Mediterranean is both clockwise and anti-clockwise, inconsistent with the Levantine anticlockwise longshore current (Robinson et al. 1992). Therefore, it is necessary to consider alternate mechanisms of introduction for foraminifera NIS invasion, particularly for the Mediterranean. One phenomenon that has been overlooked is the potential of other non-indigenous species to act as biotic vectors. In the Mediterranean Sea, the majority of foraminifera NIS inhabit the rocky subtidal, attached to carbonate-rich hard substrates and seaweeds (Hyams-Kaphzan et al. 2014). Over the past decades, these habitats have undergone a profound phase-shift from algal forests to turf barrens, due to over-grazing by invasive Indian Ocean herbivorous rabbitfish [Siganus rivulatus, first observed in 1924 (Steinitz 1927), and Siganus luridus, first observed in 1955 (Ben-Tuvia 1964)] found in the entire eastern basin (Fig. 1). Rising seawater temperature over the past several decades may have facilitated their expansion westward toward the Atlantic and northward into the Ionian, Tyrrhenian, Aegean, and Adriatic Seas (Verg es et al. 2014) (Fig. 2). These and other herbivorous fish may incidentally ingest living epiphytic foraminifera and then defecate them unharmed, although their calcareous tests may be destroyed in those fish with an acidic digestion phase (Debenay et al. 2011). In this study, our objective was to compile evidence for the ability of invasive herbivorous fish to transport the large number of benthic foraminifera species from the Red Sea to the Mediterranean Sea and to facilitate their long-distance westward dispersal. We addressed this objective by: (1) testing the viability of benthic foraminifera species in fecal pellets of invasive rabbitfish in the Mediterranean Sea, (2) examining the presence of foraminifera species in the digestive tracts of museum specimens of Red Sea rabbitfish Fig. 1. A marbled spinefoot rabbitfish Siganus rivulatus grazing on turf algae near Mikhmoret, Israel. The arrow points to a large epiphytic nonindigenous Indo-Pacific foraminifera, Sorites orbiculus, magnified at bottom right. Other benthic foraminifera species, smaller than can be seen by the naked eye, are plentiful in the shallow rocky reefs of the Eastern Mediterranean. Guy-Haim et al. A novel marine bioinvasion vector