Management of Biological Invasions (2017) Volume 8, Issue 1: 61–70 DOI: https://doi.org/10.3391/mbi.2017.8.1.06 Open Access © 2017 The Author(s). Journal compilation © 2017 REABIC Research Article Management implications of the influence of biological variability of invasive lionfish diet in Belize Me’ira Mizrahi1,*, Jennifer K. Chapman1, Charlotte L.A. Gough1, Frances Humber1 and Lucy G. Anderson2 1Blue Ventures Conservation, Omnibus Business Centre, 39-41 North Road, London, N7 9DP, UK 2Independent Researcher, Bath, UK *Corresponding author E-mail: [email protected] Received: 4 April 2016 / Accepted: 27 October 2016 / Published online: 9 December 2016 Handling editor: Amy Fowler Abstract With a voracious appetite for juvenile fish and invertebrates, invasive alien red lionfish (Pterois volitans) constitute one of the greatest threats to the Caribbean’s coral reefs. Although the eradication of lionfish is no longer considered possible, population suppression to site-specific densities can allow native fish populations to recover. Understanding the diet of lionfish in invaded areas is critical to understanding local impacts they pose to coral reef communities. This study explored the diet of lionfish in the northern end of the Belize Barrier Reef and tested whether biological variables (size, sex or reproductive stage) affect the diversity and/or abundance of prey species consumed. Between 2011 and 2014, 1023 lionfish were dissected and their gut contents analysed in the Bacalar Chico Marine Reserve. Gut contents analyses revealed that large sized lionfish consumed the highest abundance of prey (Mean (M)= 3.27 prey items) compared to small (M= 1.74 prey items) and medium (M= 3.15 prey items) lionfish, and that reproductive females consumed a higher abundance of prey (M= 3.66) compared to non-reproductive females of the same size (M= 2.85). As we found that medium and large lionfish are generalist predators and feed on a diverse assemblage of prey items, the effects of lionfish on the biomass of any one species may be reduced. This may enable individual prey species to have relatively stable abundances, although this hypothesis bears further testing. If management efforts are focused on improving a site-specific population of an individual prey species, such as an endemic or threatened fish, it is important to include removal efforts of small lionfish, particularly if they inhabit the same niche habitat. However, we recommend that existing lionfish focused cull dives continue using non-size discriminatory methods in order to account for site-specific, ecologically and commercially important prey items and to deter the likelihood of a successful invasion. Key words: Pterois volitans, Caribbean, coral reef; invasive species, prey diversity The invasion of lionfish is one of the first cases in Introduction which an introduced marine fish has become a key invasive threat. As such, it has been recognized as Native to the Indo-Pacific, the red lionfish (Pterois one of the Caribbean’s principal conservation concerns volitans Linnaeus, 1758) is now firmly established (Albins and Hixon 2013; Dahl and Patterson 2014; in the waters of the Western Atlantic and Caribbean, Sutherland et al. 2010). Invasive alien lionfish in and its range continues to expand throughout much New Providence, Bahamas have been reported at of the tropical and subtropical western Atlantic densities greater than 390 lionfish per hectare (Green Ocean and Caribbean Sea (Morris 2009; Schofield and Côté 2008), more than eight times greater than 2010). Following the first documented sighting in in their indigenous range within the Red Sea (47.9 Turneffe Atoll, Belize in 2008 (Searle et al. 2012), lionfish per hectare) (McTee and Grubich 2014). In alien lionfish have expanded their range throughout other invaded areas of the Caribbean, high growth the Belize Barrier Reef Reserve System UNESCO and reproduction rates have also being reported, with World Heritage Site (UNESCO 1996). lionfish reproducing year round and in excess of 61 M. Mizrahi et al. two-million eggs per female per year (Morris 2009; established in the BCMR and have increased in size Morris and Akins 2009). and abundance during four subsequent years of The successful invasion of the lionfish has been monitoring (Chapman et al. 2016). attributed, in part, to a generalist diet (Dahl and The additional threat to fish and invertebrate Patterson 2014; Layman and Allgeier 2012). In their populations posed by lionfish is particularly concer- native habitat, lionfish feed primarily on fish, crabs ning to the BCMR ecosystem. The overall reef health and shrimp (Fishelson 1997; Sano et al. 1987), though in the BCMR is considered to be “poor” (Chapman occasionally on other invertebrates such as isopods 2013). A combination of decreased mean hard coral and gastropods (Harmelin-Vivien and Bouchon 1976). cover (18% in 2004 (Garcia-Salgado et al. 2008) to Lionfish gut analyses in the Bahamas revealed a 9% in 2013 (Chapman 2013), dominance of fleshy typical diet consisting of small reef fishes, particularly macro algae (23% in 2013), critically low long- gobies (Gobiidae), wrass (Labridae) and basselets spined sea urchin (Diadema sp.) populations (key (Grammatidae) (Albins and Hixon 2013; Morris and reef grazers and bioeroders) (Chapman 2013) and Akins 2009). Other reported lionfish prey items in low reef fish diversity (Chapman 2013) has placed invaded ranges include parrotfish, an ecologically the BCMR on alert status since 2004 (Garcia- important herbivore known for preventing the domi- Salgado et al. 2008). nance of algae on coral reefs (Albins and Hixon 2008; Given the outstanding ecological and economic Albins and Hixon 2013; Layman and Allgeier 2012; value of the Belize Barrier Reef and its resources, Rotjan and Lewis 2006). Lionfish also demonstrate a there is an urgent need to develop systems for the range of morphometric characteristics and behaviours, effective management of invasive alien lionfish such as cryptic coloration, elongated fin rays and (Barbour et al. 2011; Gongora 2012). The total defensive venomous spines, that are unfamiliar to estimated value of fisheries, tourism and shoreline native fish prey in their invasive range, giving them protection services in Belize’s coral reef and mang- a competitive advantage over native piscivores roves is US$ 395–559 million per year (2008 value) (Albins 2013; Albins and Hixon 2013; Albins and (Nuenninghoff et al. 2015). Belize attracts up to Lyons 2012). The overfishing of competitor meso- 294,000 tourists annually (2013 data), (World Bank predators in the West Atlantic, such as small-bodied 2016), many of whom visit the Belize Barrier Reef, groupers, has further contributed to the availability making tourism the greatest foreign exchange earner of potential prey species (Farmer and Karnauskas in the country (CIA 2015; Diedrich 2007). 2013; Whitfield et al. 2007). Existing lionfish removal efforts in many invaded In addition, lionfish invasions can impact ecosystems centre around culls conducted by recrea- community structure. Bahamian reefs invaded by tional SCUBA divers who target lionfish with spears lionfish displayed significantly lower native coral reef or hooks (Nuttall 2014; Pitt and Tammy 2013). fish community recruitment rates compared to un- Although many dive operations take part in con- invaded reefs (Albins 2013). The presence of lionfish trolled culls, they often lack sufficient time, funds or caused a reduction in native reef fish abundance— labour to conduct removals at a level that is eco- 2.5 times that of a similarly sized native piscivores— logically effective (Pitt and Tammy 2013). In addition, as well as a reduction in reef fish species richness lionfish residing in deeper, mesophotic habitats (Albins 2013). In addition, in these same reef systems, remain below the limit of recreation SCUBA divers a single lionfish reduced native coral reef fish (Nuttall 2014). Although eradication of lionfish is no recruitment rates by up to 79% in five weeks (Albins longer considered possible due to the broad geogra- and Hixon 2008). Such a decline in reef fish popu- phic extent of the invasion, population suppression to lations could in turn lead to declines in commercially site-specific threshold densities can protect native important fish species such as groupers, snappers fish communities from lionfish-induced community and goatfishes (Albins and Hixon 2013), or a shift in biomass declines (Green et al. 2014). If lionfish the diet of lionfish to other prey items such as populations are to be suppressed in the long term, a invertebrates (Layman et al. 2014). more efficient management approach is required. The first confirmed report of a red lionfish in This study explores the diet of lionfish in the Belize was in December 2008 (Schofield 2009). BCMR in order to understand the local impacts posed Although accurate estimates of the lionfish popula- to coral reef communities. The aim of this study is to tion in Belize are deficient, lionfish sighting data identify the diversity and abundance of prey species collected from the Bacalar Chico Marine Reserve targeted by lionfish in Belize and to test whether (BCMR), in the northern end of the Belize Barrier prey consumption varies with lionfish size, sex, or Reef, since 2010 suggest that lionfish are firmly reproductive stage. 62 Lionfish diet in Belize Figure 1. Map of the Bacalar Chico Marine Reserve (BCMR) Showing Preservation Zone (PZ); Conservation Zone 1(CZ1); General Use Zone 1 (GUZ1); Conservation Zone 2 (CZ2); General Use Zone 2 (GUZ2). Methods tail) to the nearest 10 mm. All dives took place between the hours of 06:30 and 18:00 during every Ethics statement month of the calendar year between 2011 and 2014, Blue Ventures has a research permit under the Belize including both the wet (June to November) and dry Fisheries Department, and Blue Ventures’ staff hold (December to May) seasons. Dives took place within lionfish hunting licenses that permit research on and 24 dive sites throughout the BCMR to a maximum culling of lionfish on SCUBA dives within the depth of 30m.