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Habitat Plasticity in Native Pacific Red Lionfish Pterois Volitans Facilitates Successful Invasion of the Atlantic

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Habitat Plasticity in Native Pacific Red Lionfish Pterois Volitans Facilitates Successful Invasion of the Atlantic Vol. 506: 243–253, 2014 MARINE ECOLOGY PROGRESS SERIES Published June 23 doi: 10.3354/meps10789 Mar Ecol Prog Ser Habitat plasticity in native Pacific red lionfish Pterois volitans facilitates successful invasion of the Atlantic Katherine Cure1,4,*, Jennifer L. McIlwain1,2, Mark A. Hixon3 1The Marine Laboratory, University of Guam, Mangilao, Guam 96923, USA 2Department of Environment and Agriculture, Curtin University, Perth, WA 6845, Australia 3Department of Biology, University of Hawai‘i at Ma-noa, Honolulu, HI 96822, USA 4Present address: School of Plant Biology, The University of Western Australia, Crawley, WA 6009, Australia ABSTRACT: Red lionfish were transported outside their native Pacific range to supply aquaria, subsequently escaped or were released, and have established breeding populations in Atlantic reefs. This invasion has negatively affected coral reef fishes, reducing recruitment success through predation. To provide insight into the factors explaining invasion success, we examined the distribution and abundance of native lionfish in 2 regions of the Western Pacific (Marianas and Philippines). Densities of lionfish and other predatory coral reef fishes were evaluated via strati- fied surveys targeting habitat preferred by lionfish. There were considerable regional differences in species composition of lionfishes in general and density of Pterois volitans in particular. Red lionfish were uncommon on Guam (3.5 fish ha−1) but 6 times more abundant in the Philippines (21.9 fish ha−1). Densities in both regions were an order of magnitude less than reported in the invaded Atlantic. There was no relationship between density of lionfish and that of other reef predators, including groupers. Both native populations of P. volitans were more common on reef- associated habitats (sandy slopes, reef channels, and artificial reefs) than on coral reefs. On Guam, P. volitans was more abundant in areas of low water visibility (reef channels and river mouths) compared to reefs with high water clarity. Lionfish in their native range are habitat generalists that occupy various environments, including areas with low salinity and high sediment loads. This plasticity in habitat use helps explain invasive success, given that ecological generalization is recognized as a major factor accounting for the successful establishment of invasive species. KEY WORDS: Lionfish distribution · Native density · Habitat use · Invasion success · Western Pacific Resale or republication not permitted without written consent of the publisher INTRODUCTION habitats with low native biodiversity (Vila-Gispert et al. 2005, Duggan et al. 2006). Invasions are also usu- Many species have intentionally and unintention- ally accompanied by the invasive species being facil- ally been delivered into new ecosystems, where they itated by ecological release from predation, competi- have the possibility to establish viable populations tion, or parasite infestation in its native range (Pimentel et al. 2000). Successful invasions most (Williamson 1997, Mack et al. 2000, Crooks & Rilov often involve species with a generalist diet and high 2009). Once established, invasive species can cause tolerance to diverse environmental conditions, espe- negative economic and ecological impacts (Grosholz cially when they have been introduced to degraded 2002, Clavero & Garcia-Berthou 2005), such as spe- *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 244 Mar Ecol Prog Ser 506: 243–253, 2014 cies replacements, loss of diversity, and alterations of MATERIALS AND METHODS community and ecosystem structure and function (Fritts & Rodda 1998, Semmens et al. 2004, Dierking Survey methods et al. 2009). Introduced to the Western Atlantic in the vicinity of Lionfish density and distribution were estimated at Florida via the aquarium trade, Pacific red lionfish 23 sites on Guam and 24 sites in the Philippines using Pterois volitans and its congener P. miles reached stratified surveys that mainly targeted habitat pre- reproductive population densities during the 1990s ferred by lionfish (Fig. 1). Sites were chosen based on (Semmens et al. 2004, Meister et al. 2005, Freshwater either preliminary surveys which indicated lionfish et al. 2009) and are now distributed in tropical and presence or local reports of the occurrence of lionfish subtropical coastal environments throughout the in a particular area. Each transect covered an area Western Atlantic, Gulf of Mexico, and Caribbean approximately 5000 m2 (500 × 10 m). Transect width (Schofield 2010), despite local attempts at manual was always 10 m, but specific transect length was removal. The dramatic increase in lionfish density variable and determined by a towed GPS attached to since their introduction (Green & Côté 2008, Morris a float. Therefore, transect area was variable and et al. 2009, Albins & Hixon 2013) has raised consider- individually estimated for each transect. Surveys at able concern over the ecological and economic dam- all sites were undertaken at 5 to 15 m depth, each age to coral reef fish communities in the region. Lion- along one particular habitat type (i.e. reef slope, reef fish have caused substantial reductions in the channel, sandy slope), to evaluate potential differ- abundance of newly settled coral reef fishes (Albins ences among habitats. Long transects were chosen & Hixon 2008, Albins 2013) and may compete with to increase the probability of encounter, as lionfish native fishery species, such as small grouper (Albins are uncommon (Kulbicki et al. 2012) and have patchy 2013). distributions, such that traditional visual census Red lionfish feed on a variety of small fishes and methods shorter in length (e.g. 50 m) tend to under- crustaceans (Harmelin-Vivien & Bouchon 1976, estimate abundance (Brock 1982, Jones et al. 2006, Myers 1999, Albins & Hixon 2008, Morris & Akins Green et al. 2013). These methods were chosen to 2009) and are the only piscivorous species of mirror those used by re searchers in the invaded lionfish (Myers 1999). They have few identified range (Whitfield et al. 2007, Green & Côte 2008) to predators in both their native and invaded range, ensure robust comparisons between native and inva- presumably because of the protection provided by sive populations. Counts along transects were per- multiple venomous spines (Allen & Eschmeyer 1973, formed by 2 divers (5 m belt transect each) swimming Bernadsky & Goulet 1991, Maljkovic & Van Leeu- side by side. As lionfish are cryptic in nature, the wen 2008). Published records on parasite loads of divers made systematic searches of reef holes and lionfish are scarce but suggest low parasite loads in overhangs within the transect boundary to maximize the invaded range (Ruiz-Carus et al. 2006, Bullard accuracy in lionfish abundance estimates (Morris et al. 2011). Such characteristics of red lionfish et al. 2009). This modification of the usual visual make it an ideal species for establishing viable pop- census method follows recent recommendations ulations in new environments (Albins & Hixon 2013, for accurate assessment of lionfish density (Green Côté et al. 2013). et al. 2013). Density estimates (number per transect Understanding the underlying processes which area) were converted to number per hectare to shape the distribution and abundance of lionfish in allow comparison with published estimates of lion- their native range may provide further insight into fish density for both the invaded and native ranges the causes of their successful invasion of the At - (Whitfield et al. 2007, Green & Côté 2008, Grubich et lantic. By examining distribution patterns and lion- al. 2009, Kulbicki et al. 2012). Body size as total fish density at 2 locations in the Western Pacific, length (TL) to the nearest centimeter was estimated together with a series of environmental correlates, for every individual encountered. All surveys were we assessed some of the underlying environmental conducted during the morning (be tween 06:00 and and habitat-associated factors which could be 11:00 h), which previous observations showed as the responsible for the observed low densities of lionfish optimal time for ‘encountering’ lionfish because of in their native range (Kulbicki et al. 2012) compared their heightened foraging activity during this time to those reported for the invaded range (e.g. North (Cure et al. 2012). Surveys were conducted during Carolina: Whitfield et al. 2007, Bahamas: Green & April to June 2010 on Guam and June to July 2010 in Côté 2008). the Philippines. Cure et al.: Habitat plasticity in native lionfish 245 a bc Panglao Marianas Negros Philippines d e Fig. 1. General regions of lionfish survey sites (a) in the Philippines and Marianas and (b) in the central Philippines. Specific locations of lionfish survey sites at (c) the island of Guam (n = 23), and (d) Negros and (e) Panglao in the Philippines (n = 24). PPB and BBC: names given to local dive sites. Sites were classified as either reef slope (black circles) or non-reef slope (grey triangles). Transects per site varied from 1 to 4 on Guam and from 1 to 2 in the Philippines To investigate potential correlations between lion- Furthermore, abundances of other predators that fish and environmental characteristics, 10 environ- could potentially consume or compete for food with mental variables were measured during the course of lionfish were recorded on the same 5 m belt transects the surveys (Table 1). These variables are known to as lionfish (see Table S2 in the Supplement,
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