Marine Pollution Bulletin 105 (2016) 480–488 Contents lists available at ScienceDirect Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul Living on the edge: Vulnerability of coral-dependent fishes in the Gulf Jack R. Buchanan a, Friedhelm Krupp b,c, John A. Burt d, David A. Feary e,GinaM.Ralpha, Kent E. Carpenter a,⁎ a IUCN Species Programme, Marine Biodiversity Unit, Biological Sciences, Old Dominion University, Norfolk, VA 23529, United States of America b Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt a.M., Germany c Qatar Museums, P.O. Box 2777, Doha, Qatar d Department of Biology, New York University — Abu Dhabi, PO Box 129188, Abu Dhabi, United Arab Emirates e School of Life Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, United Kingdom article info abstract Article history: In the Gulf, multiple human impacts and recurrent bleaching events have resulted in serious declines of coral as- Received 30 June 2015 semblages, particularly in near-shore areas. However, the degree to which the extinction risk of coral-dependent Received in revised form 24 October 2015 fishes is impacted by these coral declines has been uncertain. Using primary literature and expert knowledge, Accepted 11 November 2015 coral-dependent fishes of the Gulf were identified and species-specific data on the regional distribution, popula- Available online 19 November 2015 tion status, life history characteristics, and major threats were compiled to determine their likelihood of extinc- tion under the IUCN Red List of Threatened Species' Categories and Criteria. Due to the limited area and degraded Keywords: fi fi Persian Gulf and fragmented nature of coral assemblages in the Gulf, all coral-dependent shes (where data was suf cient to Arabian Gulf assess) were listed at elevated risk of extinction. Cross-boundary collaboration among Gulf States is necessary for Coral assemblages effective management and protection of coral assemblages and their associated communities within this globally Marine conservation important region. Extinction risk © 2015 Elsevier Ltd. All rights reserved. IUCN Red List 1. Introduction the degree to which a species is associated with live coral (Sale, 2015). As an estimated 10% of coral-reef fishes can be classified as “coral Productive and highly diverse marine ecosystems such as coral reefs dependent” (Pratchett et al., 2008), the existence of intact, live coral are an essential component in shaping the structure of tropical coastal may be essential for continued survival of a large range of coral-reef regions. An estimated 25% of all marine species utilize coral habitat, in- fishes (Munday et al., 2008). While the impact of widespread coral cluding at least 4000 fish species (Burke et al., 2011; McAllister, 1995; loss extends well beyond the coral-dependent fishes (Jones et al., Spalding et al., 2001). In addition, coral reefs and their associated 2004; Pratchett et al., 2011), the extinction risk of habitat specialists fauna provide substantial societal benefits, through food and liveli- (e.g., coral-dependent fishes) is directly affected by the amount and hoods, tourism, shoreline protection and both realized and potential quality of suitable habitat available (Mace et al., 2008). Coral- treatments for disease (Burke et al., 2011). However, coral reefs are dependent fishes are generally categorized by their functional relation- highly threatened (Bryant et al., 1998; Burke et al., 2011; Spalding ship to live coral: ‘obligate coral dwellers’ live exclusively in live coral et al., 2001). Localized impacts, such as those from destructive fishing throughout their ontogeny (Gardiner and Jones, 2005; Munday et al., practices, pollution, and land development, are interacting with global 1997), ‘corallivores’ (facultative and obligate) are species that feed pre- climate change and ocean acidification to threaten even the most dominantly or exclusively on live coral (Pratchett et al., 2013), while remote of reefs (Burke et al., 2011). Globally, more than 60% of coral ‘coral recruiters’ always settle to live coral (Booth and Wellington, reefs are impacted by localized threats, increasing to 75% when global 1998; Holbrook et al., 2000; Öhman et al., 1998). For these coral- climate stressors are included (Burke et al., 2011). dependent species, live coral loss may negatively impact their abun- The degree to which current and future declines in coral reefs will dance and diversity within coral reef systems (Bellwood et al., 2006; impact the fish species inhabiting them is likely to depend heavily on Halford et al., 2004; Kokita and Nakazono, 2001; Munday, 2004; Munday et al., 2008; Pratchett et al., 2006, 2008; Spalding and Jarvis, 2002), and lead to substantial changes in the composition and structure ⁎ Corresponding author at: Global Marine Species Assessment, Marine Biodiversity of coral reef fish assemblages (Bellwood et al., 2006; Munday et al., Unit, IUCN Species Programme, Biological Sciences, Old Dominion University, Norfolk, 2008; Pratchett et al., 2008; Sale, 2015). VA 23529-0266, USA. The Persian/Arabian Gulf (hereafter referred to as ‘the Gulf’)isa E-mail addresses: [email protected] (J.R. Buchanan), [email protected] (F. Krupp), [email protected] (J.A. Burt), [email protected] (D.A. Feary), shallow, sub-tropical sea adjacent to the northwestern Indian Ocean [email protected] (G.M. Ralph), [email protected] (K.E. Carpenter). (Reynolds, 1993). Its coral reef ecosystem is characterized by some of http://dx.doi.org/10.1016/j.marpolbul.2015.11.033 0025-326X/© 2015 Elsevier Ltd. All rights reserved. J.R. Buchanan et al. / Marine Pollution Bulletin 105 (2016) 480–488 481 the world's most extreme environmental conditions, including salinity Deficient, and Not Evaluated. A species qualifies for Extinct when values often N45 ppt, as well as the highest variability in annual temper- there is no reasonable doubt that the last individual has died. A species ature encountered by coral reefs globally (Riegl, 2001; Sheppard and is listed as Extinct in the Wild when it is extinct in its natural habitat Loughland, 2002; Sheppard et al., 1992). In the Gulf, true-reef building (Subcommittee, 2014). A species qualifies for one of three ‘threatened’ framework is reduced due to the Gulf's extreme environment and rela- categories (e.g. Critically Endangered, Endangered, or Vulnerable) if it tively young age (Purkis and Riegl, 2012; Sheppard et al., 2010). Thus, meets the thresholds and conditions for that category in one of five coral “reefs” in the Gulf are better described as ‘coral assemblages’ different available criteria (IUCN, 2012a). These five independent (Burt et al., 2014; Purkis and Riegl, 2012; Sheppard et al., 1992). criteria are based on different issues related to extinction risk, including Various forms of coral assemblages occur in the Gulf. In the northern rapid population declines, small geographic ranges or very small popu- Gulf (i.e., Iraq, Kuwait, northern Saudi Arabia), near-shore coral assem- lation sizes (IUCN, 2012a; Mace et al., 2008). A species is listed as Near blages form patch and fringing reef assemblages (Coles and Tarr, 1990; Threatened if the current data for the species is close to but does not Krupp and Müller, 1994; McCain et al., 1984; Sheppard et al., 1992). quite meet the thresholds and conditions for a threatened category in However, at the seven offshore islands of Saudi Arabia and Iran in the one of the five criteria. A species is assigned to Least Concern if there northern Gulf, coral assemblages form into incipient fringing reefs are no known threats to the species or it does not qualify for a threat- (i.e., coral cays, Sheppard et al., 1992). These are by far the most com- ened category or Near Threatened. A species is assigned to the Data plex and extensive coral habitats in the Gulf, and represent much of Deficient category if there is inadequate information to apply any of the only true reefs in the Gulf. In contrast, the near-shore areas within the five criteria. This category is mainly used when there is taxonomic the southern Gulf (i.e., United Arab Emirates, Bahrain, and Qatar) are uncertainty, little biological information or insufficient data to quantify dominated by coral carpets or biostromes (Burt et al., 2014; Purkis the impact of known threats. The Not Evaluated category is used for and Riegl, 2012), though patch and fringing reef assemblages are also species that have not yet been evaluated against the five criteria. present (Sheppard et al., 1992, 2010). Although the IUCN Red List was originally developed for use at the In the Gulf, coral assemblages have been heavily degraded as a result global level, increasing interest in sub-global assessments led to the of recurrent bleaching events and coastal development activities (Burt creation of regional guidelines (IUCN, 2012b). Two additional categories et al., 2014; Riegl, 2001). In 1996 and 1998, increased sea-surface tem- to assess the conservation status of species are used in regional assess- peratures (SSTs) resulted in mass mortality of coral, particularly in ments: Regionally Extinct, which refers to species that are considered Acropora dominated areas (Burt et al., 2008, 2013a, 2014; Riegl, 2002; extinct within the focal region but still exist in the wild elsewhere, Riegl and Purkis, 2012). While recovery was observed in some areas, and Not Applicable, which refers to species that have not been assessed recurrent bleaching events in 2002, 2007, 2010, and 2011 impeded because they are unsuitable for inclusion in the regional Red List and often reversed this recovery (Burt et al., 2008, 2013a, 2014; Riegl (e.g., introduced species). Regional assessments use the same quantita- and Purkis, 2012). Widespread coastal development over the past tive thresholds and conditions that are used for global assessments to 50 years has further exacerbated the degradation of coral assemblages allow for comparisons across regions (IUCN, 2012b). However, the in the Gulf (Burt, 2014; Burt et al., 2014; Sheppard et al., 1992).