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Gymnothorax spp. (Muraenidae) as natural predators of the lionfish Pterois miles in its native biogeographical range

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Lionfish (Pterois miles) were observed avoiding coral pinnacles inhabited by the moray eels Gymnothorax flavimarginatus and G. javanicus in the northern Red Sea, Egypt. Release of lionfish (Standard Length 93-104 mm) in such coral pinnacles in November 2016 resulted in almost immediate predation by large moray eels (Total Length > 1 m). Predation by moray eels may be the key control mechanism of population growth in the native biogeographical range of Pterois spp. and may indirectly explain the success of the invasive populations. This is the first videodocumented record of moray eels feeding on the lionfish P. miles.
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2017 Environ Biol Fish 100(6): 745748 DOI 10.1007/s10641-017-0600-7
745
The final publication is available at link.springer.com
Gymnothorax spp. (Muraenidae) as natural predators
of the lionfish Pterois miles in its native biogeographical range
Arthur R. Bos · Ashraf M. Sanad · Khamis Elsayed
1Department of Biology, American University in Cairo, P.O. Box 74, New Cairo 11835, Egypt
2Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, the Netherlands
3Dive Pro Academy, P.O. Box 94, Sahl Hasheesh, Hurghada, Egypt
E-mail: arbos@aucegypt.edu
Abstract Lionfish (Pterois miles) were observed avoiding
coral pinnacles inhabited by the moray eels Gymnothorax
flavimarginatus and G. javanicus in the northern Red Sea,
Egypt. Release of lionfish (Standard Length 93104 mm) in
such coral pinnacles in November 2016 resulted in almost
immediate predation by large moray eels (Total Length > 1
m). Predation by moray eels may be the key control
mechanism of population growth in the native
biogeographical range of Pterois spp. and may indirectly
explain the success of the invasive populations. This is the
first videodocumented record of moray eels feeding on the
lionfish P. miles.
Keywords Moray eel · Predation · Pterois · Red Sea ·
Scorpaenidae
Introduction
Indo-Pacific lionfishes, Pterois miles (Bennett, 1828) and P.
volitans (Linneaus, 1758), have become invasive in the coral
reefs of theWestern Central Atlantic region, from Bermuda to
Brazil including the Mexican Gulf and the Caribbean Sea,
after being introduced accidentally in the late 1980s (e.g.,
Johnston and Purkis 2011; Côté et al. 2013; Luiz et al. 2013).
Success of the lionfish populations of the invaded regions has
been attributed to its unique biology and feeding strategy, as
well as the lack of natural predators (Cure et al. 2012). In
their native ranges, lionfish live relatively secretive in coral
crevices during the day (Fishelson 1997) and forage at night.
In contrast, lionfish of the invaded regions are mostly
diurnally active (Morris and Akins 2009). Lionfish defend
themselves with venomous spines in their anterior dorsal and
pectoral fins and are, for most predators, a challenging prey.
Incidental observations of large fish ingesting lionfish
have been reported from the invasive populations. For
example, two lionfish were found in the stomach of the
Nassau grouper Epinephelus striatus (Bloch, 1792)
(Maljković et al. 2008) and Jud et al. (2011) reported an
individual of the moray eel Gymnothorax funebris Ranzani,
1839 ingesting a wounded lionfish. Hackerott et al. (2013)
concluded that some predatory fish may occasionally
consume lionfish, but an Atlantic predator controlling the
invasive populations may not exist. Although the magnitude
of grouper predation has intensively been discussed (Bruno et
al. 2013; Mumby et al. 2013) there is a general consensus that
groupers cannot fully control the invasive populations.
Lionfish research has been initiated and intensified during
the last two decades to understand the ecological impacts of
the invasive populations. In the native habitats in the Indo-
Pacific region, few studies have been conducted on lionfish
populations because (1) densities are naturally low (Kulbicki
et al. 2012) and (2) the ecological role of lionfish in coral
reefs is poorly understood (Donaldson et al. 2010). As a
consequence, little is known about the lifecycles of these fish,
hence natural enemies have not been identified in the native
biogeographical range. Only one incidental observation was
reported from the Red Sea, where a lionfish was found in the
stomach of an individual of Fistularia commersonii (Rüppel,
1838) (Bernadsky and Goulet 1991). Throughout native
habitats however, there must be effective population control
mechanisms in place because lionfish abundance is much
lower there compared to theWestern Central Atlantic region
(McTee and Grubich 2014). During reef surveys in the
northern Red Sea (unpublished data), we noticed that coral
pinnacles, used as diurnal shelter by large moray eels of the
genus Gymnothorax spp., were rarely inhabited by lionfish.
These coral pinnacles usually had abundant prey for lionfish
(Morris and Akins 2009), suggesting that lionfish absence
was the consequence of moray eel presence. The goal of the
present study was to explore the possibility that moray eels of
the genus Gymnothorax spp. are natural predators of the
lionfish P. miles.
2017 Environ Biol Fish 100(6): 745748 DOI 10.1007/s10641-017-0600-7
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Material and methods
Observations were made while SCUBA diving on a coral reef
off Hurghada, Egypt in the northern Red Sea between 9:30
and 16:00 h on 25 November 2016. At the beginning of each
dive a lionfish of appropriate size (90120 mm) was caught
with a handheld net. The standard length (SL) of the lionfish
was measured with a ruler at 1 mm accuracy. The behavior of
the lionfish and interactions with the moray eel were recorded
during the remaining dive time after releasing it near a coral
pinnacle occupied by a moray eel. The above procedure was
repeated with another lionfish during a second dive.
Moray eels were identified using Randall and Golani
(1995) and their total length (TL) was visually estimated to
the nearest 0.1 m. A Go-Pro camera in underwater housing
with red filter was used for documentation purposes. The
depth of the coral pinnacles was recorded to the nearest 1 m
using a depth gauge.
Results and discussion
A lionfish with a SL of 104 mm was released near a coral
pinnacle at 21 m depth inhabited by an individual of
Gymnothorax flavimarginatus (Rüppel, 1830) with an
estimated TL of 1.1 m. Initially the lionfish swam away from
the coral, but eventually settled within the pinnacle (Fig.
1).Within a couple of minutes, the moray eel noticed the
presence of the lionfish. Subsequently, the moray eel
positioned itself for attacking. Although the lionfish directed
its spines toward the predator, the moray eel swiftly attacked
the lionfish at the rear of its body (Online Resource 1). After
a short fight, the moray eel held the fish with the pectoral fins
and head protruding from its mouth, and pulled the fish
deeper into the crevice out of sight of the camera.
A second lionfish with a SL of 93 mm was released in a
coral pinnacle at 6 m depth inhabited by an individual of
Gymnothorax javanicus (Bleeker, 1859) with an estimated
TL of 1.7 m. Similarly as reported for the first release, the
lionfish initially swam away. While curiously being observed
by the moray eel, the lionfish was repeatedly returned to the
coral pinnacle by the divers. The moray eel seemed hesitant
to leave its shelter, most probably due to diver presence (e.g.,
Dickens et al. 2011). When the lionfish was presented right in
front of the protruding head of the moray eel, it struck as
soon as the lionfish swam out of the net (Online Resource 2).
At this occasion, the moray eel attacked the lionfish
frontally, which suggests that there may not be an optimal
strategy for approaching lionfish. However, the smaller
individual of the moray G. flavimarginatus seemed more
cautious, avoiding the spines by attacking at the rear end of
the prey. While holding the lionfish in its mouth, G.
javanicus pulled back into the crevice after striking and
briefly chewed on the lionfish. This is only partly visible on
the footage, because the camera housing did not fit into the
crevice (Online Resource 2). As soon as the lionfish was
swallowed, the moray eel returned to the net and curiously
investigated the camera.
Past studies have shown that moray eels tend to remain in
particular coral heads for one to several days up to seven
weeks depending of the species (Abrams et al. 1983; Abrams
and Schein 1986). We confirm, based on regular visits to
selected Red Sea coral pinnacles during the last 10 years, that
several moray eels of the genus Gymnothorax spp. have fixed
home bases (personal observation). Despite the abundance of
small fishes, such as representatives of the Anthiinae and
Apogonidae (Online Resources 1 and 2) that could serve well
as prey (Morris and Akins 2009; Green et al. 2012; McTee
and Grubich 2014), lionfish avoided coral pinnacles inhabited
by moray eels (unpublished data). The present observations
showed that lionfish released at such pinnacles initially swam
away. Whether the lionfish recognized the presence of moray
eels, or instinctively moved away from unfamiliar coral
heads, is unknown. Lionfish may avoid predation by not
frequenting pinnacles inhabited by moray eels, whereas those
who accidentally settle may be readily targeted. Our diurnal
Fig. 1 Individual of Pterois miles (SL = 104 mm) settling in
coral pinnacle at 21 m depth minutes before being preyed
upon by an individual of the moray eel Gymnothorax
flavimarginatus
2017 Environ Biol Fish 100(6): 745748 DOI 10.1007/s10641-017-0600-7
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observations of moray eels preying on lionfish may be
unique, because moray eels usually predate nocturnally
(Young and Winn 2003). However, the moray eels caught the
lionfish with minimal effort, possibly challenging their
normal feeding behavior.
Densities of moray eels have rarely been reported,
because it is difficult to get reliable numbers during the day
when they hide in crevices as well as during the night when
they are out hunting (Gilbert et al. 2005). As a result,
densities of hole-dwelling species, including moray eels, are
commonly underestimated (Willis 2001). In the Red Sea,
large moray eels (TL >1 m) are regularly encountered during
the day, either resting in crevices with their heads protruding
or, less frequently, free swimming (personal observation).
Moray eels may play a role in controlling the population size
of lionfishes in the Indo-Pacific region. Moreover, the role of
moray eels controlling the invasive populations may be
limited as a result of the much lower number of moray eel
species in the Western Central Atlantic region (Froese and
Pauly 2015).
Researchers have mainly concentrated on taxonomic
analyses of moray eels and the limited number of ecological
studies were mostly conducted in the Caribbean and tropical
Atlantic. Therefore, little is known about the ecology of Indo-
Pacific moray eels. Recently, lionfish were observed in
foraging association with individuals of the moray eel
Gymnothorax griseus (Lacepède, 1803) in the Red Sea
(Naumann and Wild 2013). Gymnothorax griseus grows to a
maximum TL of 0.65 m (Froese and Pauly 2015) and may
thus never pose a threat to lionfish. Only individuals of
Gymnothorax spp. growing well beyond 1 m in total length
may be able to prey on lionfish. Marine biodiversity is
exceptionally high in the tropical waters of the Indo-Pacific
region compared to any other sea on the planet (Carpenter
and Springer 2005; Hoeksema 2007). For example, in the
Western Central Pacific, the genus Gymnothorax is
represented by 63 species of which 16 have a maximum total
length of 1 m (Froese and Pauly 2015). In the Western
Indian Ocean, including the Red Sea, Gymnothorax is
represented by 51 species of which 14 grow larger than 1 m
(Froese and Pauly 2015). In contrast, in the Western Central
Atlantic region 12 species represent Gymnothorax of which
only five have a maximum total length of 1 m (Froese and
Pauly 2015). Considering the above, the potential predation
pressure on lionfish populations by Gymnothorax spp. is
much lower in the Western Central Atlantic region than in the
Indo-Pacific region and could have possibly contributed to
the success of the invasive populations. Nevertheless, one
individual of the moray eel G. funebris was reported feeding
on a wounded lionfish in Florida (Jud et al. 2011), confirming
that moray eels may potentially prey on lionfish in the
invasive range. Whether or not moray eels in the Western
Central Atlantic region actively prey on lionfish is presently
unknown. Although Hackerott et al. (2013) concluded that,
mainly referring to groupers, there may not be an effective
Atlantic predator, the quantification of the impact of moray
eels feeding on invasive lionfish may allow a different view
on the matter.
Acknowledgements All applicable international, national, and/or
institutional guidelines for the care and use of animals were followed.
Two anonymous reviewers provided valuable comments to improve the
manuscript.
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The silver-cheeked toadfish (Lagocephalus sceleratus, from the pufferfish family Tetraodontidae) and the Pacific red lionfish (Pterois miles, family Scorpaenidae) have recently invaded the Mediterranean Sea. Lagocephalus sceleratus has spread throughout this entire sea with the highest concentrations in the eastern basin, while more recently, Pterois miles has spread from the Eastern to the Central Mediterranean Sea. Their effects on local biodiversity and fisheries are cause for management concern. Here, a comprehensive review of predators of these two species from their native Indo-Pacific and invaded Mediterranean and Western Atlantic ranges is presented. Predators of Tetraodontidae in general were reviewed for their native Indo-Pacific and Western Atlantic ranges, as no records were found specifically for L. sceleratus in its native range. Tetraodontidae predators in their native ranges included mantis shrimp (Stomatopoda), lizardfish (Synodus spp.), tiger shark (Galeocerdo cuvier), lemon shark (Negaprion brevirostris), sea snakes (Enhydrina spp.), catfish (Arius spp.), cobia (Rachycentron canadum), skipjack tuna (Katsuwonus pelamis), and common octopus (Octopus vulgaris). The only reported predator of adult L. sceleratus in the Mediterranean was loggerhead turtle (Caretta caretta), whereas juvenile L. sceleratus were preyed by common dolphinfish (Coryphaena hippurus) and garfish (Belone belone). Conspecific cannibalism of L. sceleratus juveniles was also confirmed in the Mediterranean. Pufferfish predators in the Western Atlantic included common octopus, frogfish (Antennaridae), and several marine birds. Predators of all lionfish species in their native Indo-Pacific range included humpback scorpionfish (Scorpaenopsis spp.), bobbit worms (Eunice aphroditois), moray eels (Muraenidae), and bluespotted cornetfish (Fistularia commersonii). Lionfish predators in the Mediterranean included dusky grouper (Epinephelus marginatus), white grouper (Epinephelus aeneus), common octopus, and L. sceleratus, whereas in the Western Atlantic included the spotted moray (Gymnothorax moringa), multiple grouper species (tiger Mycteroperca tigris, Nassau Epinephelus striatus, black Mycteroperca bonaci, red Epinephelus morio, and gag Mycteroperca microleps; Epinephelidae), northern red snapper (Lutjanus campechanus), greater amberjack (Seriola dumerilli), and nurse shark (Ginglymostoma cirratum). The sparse data found on natural predation for these species suggest that population control via predation may be limited. Their population control may require proactive, targeted human removals, as is currently practiced with lionfish in the Western Atlantic.
Chapter
All aquatic ecosystems, and even some land‐based habitats, have been used by fish populations, with few ecological niches deprived of their presence, as evidenced by the examples of fish colonizing many different types of habitats. Reef corals create complex mineralized structures with an extreme diversity of habitats used by small fish whose size and morphology are perfectly adapted to the geometric structures created. The occupation of space by a species varies over time in accordance not only with the local hydrological fluctuations in its habitat during floods, low water levels, etc., but also the presence or absence of predators. Strong competition for food often occurs in natural environments between individuals of the same population, to the benefit of the largest, strongest and most dominant. The best, most nutritious and easily accessible prey is often its own congeners, especially if they are defenseless as they are early, in the egg, larvae and juvenile stages.
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Biotic resistance is the idea that native species negatively affect the invasion success of introduced species. We tested the hypothesis that native grouper are controlling the abundance of exotic lionfish on Caribbean coral reefs by assessing the relationship between the density and biomass of lionfish and native predators at 71 reefs in three biogeographic regions. Our results indicated that: (a) the abundance of lionfish and large grouper are not negatively related, and (b) lionfish abundance is controlled by a number of physical site characteristics, and possibly by culling. Taken together, our results suggest that managers cannot rely on native grouper populations to control the lionfish invasion. Mumby et al. (2013) objected to several aspects of our analysis and conclusions. Here we address their criticisms and argue that our original conclusions are valid.
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The invasion by lionfish Pterois volitans and P. miles throughout the western Atlantic and Caribbean is emerging as a serious ecological problem. While lionfish have been identified on coral reefs and in other marine systems, additional ecosystems may be affected as the invasion spreads. Here we identify the first estuarine intrusion by lionfish in their invasive range. Lionfish (n = 211) were captured in the Loxahatchee River estuary (Florida, USA) between August 2010 and April 2011, with some individuals located as far as similar to 5.5 km from the ocean. Multiple size classes were documented (standard lengths ranged from 23 to 185 mm), and post-settlement juveniles were present throughout the sampling period. All individuals were found in close association with anthropogenically created habitats (e. g. docks, sea walls, submerged debris), suggesting that human-driven changes in habitat availability may facilitate estuarine invasion. Fifteen prey taxa were found in lionfish stomachs, with diets dominated by small shrimp. Since estuaries are already highly threatened by human impacts, and provide critical habitat for numerous commercially, recreationally, and ecologically important species, establishment of lionfish in these ecosystems is of particular concern.
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As invasive lionfish populations continue to expand in the Western Atlantic and Ca - ribbean, understanding the ecology and foraging behavior of lionfish in their native habitats will help identify biotic constraints that may improve management of invaded reefs. The most comprehensive survey of lionfish, concluded to date, of native Red Sea lionfish was undertaken to identify potential differences in vertical distribution, density and diurnal cycles of foraging behavior. The overall, combined density of lionfish was estimated at 47.9 fish ha−1, the highest yet recorded throughout their native range. The most commonly encountered lionfish species were Pterois miles (26.4 fish ha−1) and P. radiata (20.8 fish ha−1). The density of P. miles was significantly greater at the northernmost site surveyed and also significantly greater at depths less than 15 m, with individuals often observed in aggregations. In contrast, P. radiata were often solitary and evenly distributed along the reef profile. Despite ecological differences between these 2 species, the majority of foraging activities for both P. miles and P. radiata occurred around or after sunset. These results validate that the shallow coral reef habitats of the Red Sea host the highest densities of lionfish in their native range and highlight areas of ecological variability among native lionfish species.
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Pacific red lionfish Pterois volitans have invaded Atlantic reefs and reached much greater population densities than on native reefs. We hypothesized that lionfish on invaded reefs would (1) experience higher kill rates and thus spend less time hunting, given the naivete of Atlantic prey, (2) consume a greater variety of prey, given the lack of native prey defenses, and (3) display less pronounced crepuscular patterns of hunting, given the ease of capturing Atlantic prey. Comparative behavioral observations were conducted in 2 native regions (Philippines and Guam) and 2 invaded regions (Cayman Islands and Bahamas) to assess lionfish time budgets and diurnal activity patterns and to explore correlations between environmental variables and lionfish behavior. Contrary to our first hypothesis, total time allocated to hunting and kill rates showed no difference between native and invaded reefs, despite considerable regional variation. However, Atlantic prey of lionfish were twice as large as Pacific prey, suggesting that despite similar hunting behavior, invasive lionfish ingest greater daily rations of prey biomass. Furthermore, consistent with our second hypothesis, lionfish on invaded reefs had broader diets, and also relied less on 'blowing' behavior for prey capture, pointing to substantial prey naivete in the invaded range. Importantly, only in the invaded range did we observe lionfish consuming parrotfishes, the decline of which could have indirect effects on interactions between seaweeds and corals. Finally, lionfish overall tended to exhibit a crepuscular pattern in behavior whereby hunting peaked at sunrise and/or sunset, with no differences attributable to native vs. invasive status.
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The invasion of western Atlantic marine habitats by two predatory Indo-Pacific lionfish, Pterois volitans and P. miles, has recently unfolded at an unprecedented rate, with ecological consequences anticipated to be largely negative. We take stock of recently accumulated knowledge about lionfish ecology and behaviour and examine how this information is contributing to our general understanding of the patterns and processes underpinning marine predator invasions, and to the specific issue of lionfish management. Lionfish were first reported off Florida in 1985. Since their establishment in The Bahamas in 2004, they have colonised 7.3 million km2 of the western Atlantic and Caribbean region, and populations have grown exponentially at many locations. These dramatic increases potentially result from a combination of life-history characteristics of lionfish, including early maturation, early reproduction, anti-predatory defenses, unique predatory behaviour, and ecological versatility, as well as features of the recipient communities, including prey naïveté, weak competitors, and native predators that are overfished and naïve to lionfish. Lionfish have reduced the abundance of small native reef fishes by up to 95% at some invaded sites. Population models predict that culling can reduce lionfish abundance substantially, but removal rates must be high. Robust empirical estimates of the cost-effectiveness and effects of removal strategies are urgently needed because lionfish management will require a long-term, labour-intensive effort that may be possible only at local scales. The ultimate causes of the invasion were inadequate trade legislation and poor public awareness of the effects of exotic species on marine ecosystems. The lionfish invasion highlights the need for prevention, early detection, and rapid response to marine invaders.
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The Indo-Pacific lionfish species Pterois volitans and P. miles are piscivorous predators that were introduced probably via aquarium release to the northwestern Atlantic approximately 15 yr ago and rapidly spread and established through the Greater Caribbean. Possible ecological impacts of this invasion on native species are a legitimate cause for concern. Despite predictions that lionfishes will extend their range throughout most of the eastern coast of South America, they are yet to be recorded in Brazil. We pres- ent a perspective analysis of the lionfish invasion in the southwestern Atlantic by investigating patterns of fish species movement across the Amazon-Orinoco plume (AOP), a large freshwater and sediment runoff between the Caribbean and the Brazilian Provinces that repre- sents a ‘porous’ barrier to dispersal for reef organisms. We analyzed records of species that have recently crossed the barrier and found that the Brazilian Pro- vince contributes a significantly higher proportion of its endemic fauna to the pool of crossers, indicating that movements of vagrant species across the AOP are more common from Brazil towards the Caribbean than vice versa. Nevertheless, despite infrequent migration south- wards against the currents, our analysis indicates that such migration has occurred historically and has re- sulted in the establishment of new populations. Our analysis indicates that a combination of the effects of the AOP and prevailing currents along northern Brazil may slow the pace of the potential invasion, which could help eradication programs if action is taken before lionfishes become widespread and established in Brazil.
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The Indo-Pacific lionfish, Pterois volitans , has invaded most of the Tropical Western Atlantic in the last few years. The degree to which populations of this invasive species can be controlled by native predatory fish (mostly grouper), is controversial with conflicting reports. Here, we review the evidence of two recent papers and point out some of the difficulties in inferring predator-limitation purely from observational data. A negative relationship has been found between large-bodied grouper and lionfish during early colonisation though the degree to which this is caused by direct predation versus behavioural mechanisms is unclear. Evidence to the contrary from a recent study suffers confounding effects of habitat quality, fishing, and dispersal and therefore remains equivocal.
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Rarity in tropical and subtropical coral reef fishes is an important ecological and biogeographical concept that has received little attention until recently. These studies have emphasized the relative lack of information about the processes that limit the distributions or abundances of rare species. This lack of information extends even to assumptions about ecological processes acting upon life history traits that may vary significantly from what might be seen in common species. Lionfishes (genus Pterois, family Scorpaenidae) of the Indo-West Pacific region are typically uncommon or rare throughout most of their native ranges. Two species, however, Pterois volitans and P. miles, both invasive species in the Caribbean and Gulf of Mexico, are anything but rare. Since their introduction to the western Atlantic region, both species, but especially P. volitans, have exploded in terms of patterns of distribution, colonization rates, and abundance. Shifts in the behavior of these lionfishes are apparent, as well, and the success of these invasive species is causing major negative impacts already. How and why these species have become successful within the western Atlantic is the subject of considerable research. The how and why of their rarity within their native ranges has drawn less attention. In this paper, we present the preliminary results of various surveys conducted within the western and central Pacific over the last thirty years in an attempt to understand patterns of lionfish (P. volitans, P. antennata, and P. radiata) abundance, distribu-tion, habitat association and behavior.