Grouper as a natural biocontrol of invasive lionfish

Lionfish (Pterois volitans/miles) have invaded the majority of the Caribbean region within five years. As voracious predators of native fishes with a broad habitat distribution, lionfish are poised to cause an unprecedented disruption to coral reef diversity and function. Controls of lionfish densities within its native range are poorly understood, but they have been recorded in the stomachs of large-bodied Caribbean groupers. Whether grouper predation of lionfish is sufficient to act as a biocontrol of the invasive species is unknown, but pest biocontrol by predatory fishes has been reported in other ecosystems. Groupers were surveyed along a chain of Bahamian reefs, including one of the region's most successful marine reserves which supports the top one percentile of Caribbean grouper biomass. Lionfish biomass exhibited a 7-fold and non-linear reduction in relation to the biomass of grouper. While Caribbean grouper appear to be a biocontrol of invasive lionfish, the overexploitation of their populations by fishers, means that their median biomass on Caribbean reefs is an order of magnitude less than in our study. Thus, chronic overfishing will probably prevent natural biocontrol of lionfishes in the Caribbean.     

Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities

The recent irruption of Pacific red lionfish (Pterois volitans) on Caribbean and Atlantic coral reefs could prove to be one of the most damaging marine invasions to date. Invasive lionfish are reaching densities much higher than those reported from their native range, and they have a strong negative effect on the recruitment and abundance of a broad diversity of native coral-reef fishes. Otherwise, little is known about how lionfish affect native coral-reef communities, especially compared to ecologically similar native predators. A controlled field experiment conducted on small patch-reefs in the Bahamas over an 8-week-period demonstrated that (1) lionfish caused a reduction in the abundance of small native coral-reef fishes that was 2.5?±?0.5 times (mean?±?SEM) greater than that caused by a similarly sized native piscivore, the coney grouper Cephalopholis fulva (93.7 vs. 36.3?% reduction); (2) lionfish caused a reduction in the species richness of small coral-reef fishes (loss of 4.6?±?1.6 species), whereas the native piscivore did not have a significant effect on prey richness; (3) the greatest effects on the reef-fish community, in terms of both abundance and richness, occurred when both native and invasive predators were present; and (4) lionfish grew significantly faster (>6 times) than the native predator under the same field conditions. These results suggest that invasive lionfish have stronger ecological effects than similarly sized native piscivores, and may pose a substantial threat to native coral-reef fish communities.     

Indo-Pacific lionfish are larger and more abundant on invaded reefs: a comparison of Kenyan and Bahamian lionfish populations

The invasion by Indo-Pacific lionfish (Pterois volitans and P. miles) of the western Atlantic, Caribbean and Gulf of Mexico is emerging as a major threat to coral reef communities across the region. Comparing native and introduced populations of invasive species can reveal shifts in ecology and behaviour that can accompany successful invasions. Using standardized field surveys replicated at multiple sites in Kenya and the Bahamas, we present the first direct comparisons of lionfish density, body size, biomass and behaviour between native and invaded coral reefs. We found that lionfish occur at higher densities with larger body sizes and total biomass on invaded Bahamian coral reefs than the ecologically equivalent species (P. miles) does on native Kenyan reefs. However, the combined average density of the five lionfish species (Pterois miles, P. antennata, P. radiata, Dendrochirus brachypterus and D. zebra) on Kenyan reefs was similar to the density of invasive lionfish in the Bahamas. Understanding the ecological processes that drive these differences can help inform the management and control of invasive lionfish.     

What are the characteristics of lionfish and other fishes that influence their association in diurnal refuges?

In Caribbean reefs, the lionfish Pterois volitans is an invasive species that causes severe negative ecological effects, especially as this crepuscular predator consumes very diverse prey. Lionfish are not active during the day and stay in their refuges, sharing these spaces with various other fishes. The aim of this study is to determine which fishes are associated with the lionfish in their shelters, and what characteristics of both the invasive and native species may influence and explain such coexistence between a predator and its potential prey. Through diving and snorkelling, we visited 141 lionfish refuges, mostly caves, where we observed 204 lionfish and 494 other fish from 16 native species. We recorded species and abundance, as well as lionfish size and abundance. Half of the lionfish were observed in groups and the majority were large-sized. The association with most fish species seems fortuitous, but three species, Gramma loreto, Chromis cyanea and Canthigaster rostrata, were frequently observed in association with lionfish. Numerous fish juveniles, most likely Scarus coeruleus, were also observed together with the invasive predator. The more commonly associated fishes, particularly G. loreto, are mostly associated with large-sized lionfish that were found in groups. The associated fishes are also generally found in groups. Gramma loreto is a potential cleaner of the lionfish; the reasons for the association between these fish species and the invasive lionfish may be more complex than a simple predator-prey relationship and are discussed based on their biological traits and previously reported lionfish trophic ecology and predation behaviour.     

Native Predators Do Not Influence Invasion Success of Pacific Lionfish on Caribbean Reefs

Biotic resistance, the process by which new colonists are excluded from a community by predation from and/or competition with resident species, can prevent or limit species invasions. We examined whether biotic resistance by native predators on Caribbean coral reefs has influenced the invasion success of red lionfishes (Pterois volitans and Pterois miles), piscivores from the Indo-Pacific. Specifically, we surveyed the abundance (density and biomass) of lionfish and native predatory fishes that could interact with lionfish (either through predation or competition) on 71 reefs in three biogeographic regions of the Caribbean. We recorded protection status of the reefs, and abiotic variables including depth, habitat type, and wind/wave exposure at each site. We found no relationship between the density or biomass of lionfish and that of native predators. However, lionfish densities were significantly lower on windward sites, potentially because of habitat preferences, and in marine protected areas, most likely because of ongoing removal efforts by reserve managers. Our results suggest that interactions with native predators do not influence the colonization or post-establishment population density of invasive lionfish on Caribbean reefs.     

Environmental and Biotic Correlates to Lionfish Invasion Success in Bahamian Coral Reefs

Lionfish (Pterois volitans), venomous predators from the Indo-Pacific, are recent invaders of the Caribbean Basin and southeastern coast of North America. Quantification of invasive lionfish abundances, along with potentially important physical and biological environmental characteristics, permitted inferences about the invasion process of reefs on the island of San Salvador in the Bahamas. Environmental wave-exposure had a large influence on lionfish abundance, which was more than 20 and 120 times greater for density and biomass respectively at sheltered sites as compared with wave-exposed environments. Our measurements of topographic complexity of the reefs revealed that lionfish abundance was not driven by habitat rugosity. Lionfish abundance was not negatively affected by the abundance of large native predators (or large native groupers) and was also unrelated to the abundance of medium prey fishes (total length of 5–10 cm). These relationships suggest that (1) higher-energy environments may impose intrinsic resistance against lionfish invasion, (2) habitat complexity may not facilitate the lionfish invasion process, (3) predation or competition by native fishes may not provide biotic resistance against lionfish invasion, and (4) abundant prey fish might not facilitate lionfish invasion success. The relatively low biomass of large grouper on this island could explain our failure to detect suppression of lionfish abundance and we encourage continuing the preservation and restoration of potential lionfish predators in the Caribbean. In addition, energetic environments might exert direct or indirect resistance to the lionfish proliferation, providing native fish populations with essential refuges.     

Low Susceptibility of Invasive Red Lionfish (Pterois volitans) to a Generalist Ectoparasite in Both Its Introduced and Native Ranges

Escape from parasites in their native range is one of many mechanisms that can contribute to the success of an invasive species. Gnathiid isopods are blood-feeding ectoparasites that infest a wide range of fish hosts, mostly in coral reef habitats. They are ecologically similar to terrestrial ticks, with the ability to transmit blood-borne parasites and cause damage or even death to heavily infected hosts. Therefore, being highly resistant or highly susceptible to gnathiids can have significant fitness consequences for reef-associated fishes. Indo-Pacific red lionfish (Pterois volitans) have invaded coastal habitats of the western tropical and subtropical Atlantic and Caribbean regions. We assessed the susceptibility of red lionfish to parasitic gnathiid isopods in both their native Pacific and introduced Atlantic ranges via experimental field studies during which lionfish and other, ecologically-similar reef fishes were caged and exposed to gnathiid infestation on shallow coral reefs. Lionfish in both ranges had very few gnathiids when compared with other species, suggesting that lionfish are not highly susceptible to infestation by generalist ectoparasitic gnathiids. While this pattern implies that release from gnathiid infestation is unlikely to contribute to the success of lionfish as invaders, it does suggest that in environments with high gnathiid densities, lionfish may have an advantage over species that are more susceptible to gnathiids. Also, because lionfish are not completely resistant to gnathiids, our results suggest that lionfish could possibly have transported blood parasites between their native Pacific and invaded Atlantic ranges.     

Consumptive and non-consumptive effects of an invasive marine predator on native coral-reef herbivores

Invasive predators typically have larger effects on native prey populations than native predators, yet the potential roles of their consumptive versus non-consumptive effects (CEs vs. NCEs) in structuring invaded systems remains unclear. Invasive lionfish (Pterois volitans) may have ecosystem-level effects by altering native fish grazing on benthic algae that could otherwise displace corals. Lionfish could reduce grazing by decreasing the abundance of herbivorous fishes (CEs), and/or the predation risk posed by lionfish could alter grazing behavior of fishes (NCEs). To test for these CEs, we manipulated lionfish densities on large reefs in The Bahamas and surveyed fish populations throughout June 2009–2011. In July 2011, NCEs of lionfish were measured by observing fish grazing behavior on algal-covered substrata placed in microhabitats varying in lionfish presence at different spatial scales, and quantifying any resulting algal loss. Lionfish reduced small herbivorous fish density by the end of the 2010 summer recruitment season. Grazing by small and large fishes was reduced on high-lionfish-density reefs, and small fish grazing further decreased when in the immediate presence of lionfish within-reefs. Lionfish had a negative indirect effect on algal loss, with 66–80 % less algae removed from substrata in high-lionfish-density reefs. Parrotfishes were likely driving the response of herbivorous fishes to both CEs and NCEs of lionfish. These results demonstrate the importance of considering NCEs in addition to CEs of invasive predators when assessing the effects of invasions.     

Hot or not? Comparative behavioral thermoregulation,critical temperature regimes,and thermal tolerances of the invasive lionfish <Emphasis Type="Italic">Pterois</Emphasis> sp. versus native western North Atlantic reef fishes

Temperature influences the geographic range, physiology, and behavior of many ectothermic species, including the invasive lionfish Pterois sp. Thermal parameters were experimentally determined for wild-caught lionfish at different acclimation temperatures (13, 20, 25 and 32 °C). Preferences and avoidance were evaluated using a videographic shuttlebox system, while critical thermal methodology evaluated tolerance. The lionfish thermal niche was compared experimentally to two co-occurring reef fishes (graysby Cephalopholis cruentata and schoolmaster Lutjanus apodus) also acclimated to 25 °C. The physiologically optimal temperature for lionfish is likely 28.7 ± 1 °C. Lionfish behavioral thermoregulation was generally linked to acclimation history; tolerance and avoidance increased significantly at higher acclimation temperatures, but final preference did not. The tolerance polygon of lionfish shows a strong correlation between thermal limits and acclimation temperature, with the highest CT_max at 39.5 °C and the lowest CT_min at 9.5 °C. The tolerance range of invasive lionfish (24.61 °C) is narrower than those of native graysby (25.25 °C) and schoolmaster (26.87 °C), mostly because of lower thermal maxima in the former. Results show that lionfish display “acquired” thermal tolerance at higher and lower acclimation temperatures, but are no more eurythermal than other tropical fishes. Collectively, these results suggest that while lionfish range expansion in the western Atlantic is likely over the next century from rising winter sea temperatures due to climate change, the magnitude of poleward radiation of this invasive species is limited and will likely be equivalent to native tropical and subtropical fishes with similar thermal minima.     

Ultimate Predators: Lionfish Have Evolved to Circumvent Prey Risk Assessment Abilities

Invasive species cause catastrophic alterations to communities worldwide by changing the trophic balance within ecosystems. Ever since their introduction in the mid 1980''s common red lionfish, Pterois volitans, are having dramatic impacts on the Caribbean ecosystem by displacing native species and disrupting food webs. Introduced lionfish capture prey at extraordinary rates, altering the composition of benthic communities. Here we demonstrate that the extraordinary success of the introduced lionfish lies in its capacity to circumvent prey risk assessment abilities as it is virtually undetectable by prey species in its native range. While experienced prey damselfish, Chromis viridis, respond with typical antipredator behaviours when exposed to a common predatory rock cod (Cephalopholis microprion) they fail to visibly react to either the scent or visual presentation of the red lionfish, and responded only to the scent (not the visual cue) of a lionfish of a different genus, Dendrochirus zebra. Experienced prey also had much higher survival when exposed to the two non-invasive predators compared to P. volitans. The cryptic nature of the red lionfish has enabled it to be destructive as a predator and a highly successful invasive species.     

Abundance estimates of the Indo-Pacific lionfish <Emphasis Type="Italic">Pterois volitans</Emphasis>/<Emphasis Type="Italic">miles</Emphasis> complex in the Western North Atlantic

Less than a decade after being observed off Florida, the invasive Indo-Pacific lionfish is now widely distributed off the southeast coast of the United States. As a step towards measuring invasion impacts to native communities, we examine the magnitude and extent of this invasion by first, compiling reports of lionfish to provide range information and second, estimate lionfish abundance from two separate studies. We also estimate native grouper (epinepheline serranids) abundance to better assess and compare lionfish abundances. In the first study we conducted SCUBA diver visual transect surveys at 17 different locations off the North Carolina coast in water depths of 35–50 m. In the second study, we conducted 27 Remote Operated Vehicle (ROV) transect surveys at five locations from Florida to North Carolina in water depths of 50–100 m. In both studies, lionfish were found to be second in abundance only to scamp (Mycteroperca phenax). Lionfish were found in higher abundance in the shallower North Carolina SCUBA surveys ( ha⁻¹) than in the deep water ROV surveys ( ha⁻¹). Lionfish reports continue to expand most recently into the Bahamas, raising the specter of further spread into the Caribbean and Gulf of Mexico. The potential impacts of lionfish to native communities are likely to be through direct predation, competition and overcrowding. The high number of lionfish present in the ecosystem increases the potential for cascading impacts throughout the food chain. Within the southeast region the combined effects of climate change, overfishing and invasive species may have irreversible consequences to native communities in this region. An erratum to this article can be found at     

What Doesn't Kill You Makes You Wary? Effect of Repeated Culling on the Behaviour of an Invasive Predator

As a result of being hunted, animals often alter their behaviour in ways that make future encounters with predators less likely. When hunting is carried out for conservation, for example to control invasive species, these behavioural changes can inadvertently impede the success of future efforts. We examined the effects of repeated culling by spearing on the behaviour of invasive predatory lionfish (Pterois volitans/miles) on Bahamian coral reef patches. We compared the extent of concealment and activity levels of lionfish at dawn and midday on 16 coral reef patches off Eleuthera, The Bahamas. Eight of the patches had been subjected to regular daytime removals of lionfish by spearing for two years. We also estimated the distance at which lionfish became alert to slowly approaching divers on culled and unculled reef patches. Lionfish on culled reefs were less active and hid deeper within the reef during the day than lionfish on patches where no culling had occurred. There were no differences at dawn when removals do not take place. Lionfish on culled reefs also adopted an alert posture at a greater distance from divers than lionfish on unculled reefs. More crepuscular activity likely leads to greater encounter rates by lionfish with more native fish species because the abundance of reef fish outside of shelters typically peaks at dawn and dusk. Hiding deeper within the reef could also make remaining lionfish less likely to be encountered and more difficult to catch by spearfishers during culling efforts. Shifts in the behaviour of hunted invasive animals might be common and they have implications both for the impact of invasive species and for the design and success of invasive control programs.     

Invasive lionfish drive Atlantic coral reef fish declines

Indo-Pacific lionfish (Pterois volitans and P. miles) have spread swiftly across the Western Atlantic, producing a marine predator invasion of unparalleled speed and magnitude. There is growing concern that lionfish will affect the structure and function of invaded marine ecosystems, however detrimental impacts on natural communities have yet to be measured. Here we document the response of native fish communities to predation by lionfish populations on nine coral reefs off New Providence Island, Bahamas. We assessed lionfish diet through stomach contents analysis, and quantified changes in fish biomass through visual surveys of lionfish and native fishes at the sites over time. Lionfish abundance increased rapidly between 2004 and 2010, by which time lionfish comprised nearly 40% of the total predator biomass in the system. The increase in lionfish abundance coincided with a 65% decline in the biomass of the lionfish's 42 Atlantic prey fishes in just two years. Without prompt action to control increasing lionfish populations, similar effects across the region may have long-term negative implications for the structure of Atlantic marine communities, as well as the societies and economies that depend on them.     

Density-dependent colonization and natural disturbance limit the effectiveness of invasive lionfish culling efforts

Culling can be an effective management tool for reducing populations of invasive species to levels that minimize ecological effects. However, culling is labour-intensive, costly, and may have unintended ecological consequences. In the Caribbean, culling is widely used to control invasive Indo-Pacific lionfish, Pterois volitans and P. miles, but the effectiveness of infrequent culling in terms of reducing lionfish abundance and halting native prey decline is unclear. In a 21-month-long field experiment on natural reefs, we found that culling effectiveness changed after the passage of a hurricane part-way through the experiment. Before the hurricane, infrequent culling resulted in substantial reductions in lionfish density (60–79%, on average, albeit with large uncertainty) and slight increases in native prey species richness, but was insufficient to stem the decline in native prey biomass. Culling every 3 months (i.e., quarterly) and every 6 months (i.e., biannually) had similar effects on lionfish density and native prey fishes because of high rates of lionfish colonization among reefs. After the hurricane, lionfish densities were greater on all culled reefs compared to non-culled reefs, and prey biomass declined by 92%, and species richness by 71%, on biannually culled reefs. The two culling frequencies we examined therefore seem to offer a poor trade-off between the demonstrated conservation gains that can be achieved with frequent culling and the economy of time and money realized by infrequent culling. Moreover, stochastic events such as hurricanes can drastically limit the effectiveness of culling efforts.     

Ecological impacts of an invasive mesopredator do not differ from those of a native mesopredator: lionfish in Caribbean Panama

Coral Reefs - The impacts of invasive lionfish (Pterois volitans/miles) on native coral reef populations in the Western Atlantic Ocean and Caribbean Sea can be enormous. However, how much lionfish...     

Feeding ecology of invasive lionfish (<Emphasis Type="Italic">Pterois volitans</Emphasis>) in the Bahamian archipelago

Feeding ecology of the lionfish (Pterois volitans), an invasive species in the Western North Atlantic, was examined by collecting stomach content data from fishes taken throughout the Bahamian archipelago. Three relative metrics of prey quantity, including percent number, percent frequency, and percent volume, were used to compare three indices of dietary importance. Lionfish largely prey upon teleosts (78% volume) and crustaceans (14% volume). Twenty-one families and 41 species of teleosts were represented in the diet of lionfish; the top 10 families of dietary importance were Gobiidae, Labridae, Grammatidae, Apogonidae, Pomacentridae, Serranidae, Blenniidae, Atherinidae, Mullidae, and Monacanthidae. The proportional importance of crustaceans in the diet was inversely related to size with the largest lionfish preying almost exclusively on teleosts. Lionfish were found to be diurnal feeders with the highest predation occurring in the morning (08:00–11:00).     

Parasite-mediated enemy release and low biotic resistance may facilitate invasion of Atlantic coral reefs by Pacific red lionfish (<Emphasis Type="Italic">Pterois volitans</Emphasis>)

Successful invasions are largely explained by some combination of enemy release, where the invader escapes its natural enemies from its native range, and low biotic resistance, where native species in the introduced range fail to control the invader. We examined the extent to which parasites may mediate both release and resistance in the introduction of Pacific red lionfish (Pterois volitans) to Atlantic coral reefs. We found that fewer lionfish were parasitized at two regions in their introduced Atlantic range (The Bahamas and the Cayman Islands) than at two regions in their native Pacific range (the Northern Marianas Islands and the Philippines). This pattern was largely driven by relatively high infection rates of lionfish by didymozoan fluke worms and parasitic copepods (which may be host-specific to Pterois lionfishes) in the Marianas and the Philippines, respectively. When compared with sympatric, native fishes in the Atlantic, invasive lionfish were at least 18 times less likely to host a parasite in The Bahamas and at least 40 times less likely to host a parasite in the Cayman Islands. We found no indication that lionfish introduced Pacific parasites into the Atlantic. In conjunction with demographic signs of enemy release such as increased density, fish size, and growth of invasive lionfish, it is possible that escape from parasites may have contributed to the success of lionfish. This is especially true if future studies reveal that such a loss of parasites has led to more energy available for lionfish growth, reproduction, and/or immunity.     

Regional Variation in Parasite Species Richness and Abundance in the Introduced Range of the Invasive Lionfish,Pterois volitans

Parasites can play an important role in biological invasions. While introduced species often lose parasites from their native range, they can also accumulate novel parasites in their new range. The accumulation of parasites by introduced species likely varies spatially, and more parasites may shift to new hosts where parasite diversity is high. Considering that parasitism and disease are generally more prevalent at lower latitudes, the accumulation of parasites by introduced hosts may be greater in tropical regions. The Indo-Pacific lionfish (Pterois volitans) has become widely distributed across the Western Atlantic. In this study, we compared parasitism across thirteen locations in four regions, spanning seventeen degrees of latitude in the lionfish''s introduced range to examine potential spatial variation in parasitism. In addition, as an initial step to explore how indirect effects of parasitism might influence interactions between lionfish and ecologically similar native hosts, we also compared parasitism in lionfish and two co-occurring native fish species, the graysby grouper, Cephalopholis cruentata, and the lizardfish, Synodus intermedius, in the southernmost region, Panama. Our results show that accumulation of native parasites on lionfish varies across broad spatial scales, and that colonization by ectoparasites was highest in Panama, relative to the other study sites. Endoparasite richness and abundance, on the other hand, were highest in Belize where lionfish were infected by twice as many endoparasite species as lionfish in other regions. The prevalence of all but two parasite species infecting lionfish was below 25%, and we did not detect an association between parasite abundance and host condition, suggesting a limited direct effect of parasites on lionfish, even where parasitism was highest. Further, parasite species richness and abundance were significantly higher in both native fishes compared to lionfish, and parasite abundance was negatively associated with the condition index of the native grouper but not that of the lionfish or lizardfish. While two co-occurring native fishes were more heavily parasitized compared to lionfish in Panama any indirect benefits of differential parasitism requires further investigation. Future parasitological surveys of lionfish across the eastern coast of North America and the Lesser Antilles would further resolve geographic patterns of parasitism in invasive lionfish.     

A stage-based matrix population model of invasive lionfish with implications for control

The rapid invasion of lionfish into the Western North Atlantic and Caribbean will undoubtedly affect native reef fishes via processes such as trophic disruption and niche takeover, yet little is known about the dynamics of this invasion. We constructed a stage-based, matrix population model in which matrix elements were comprised of lower-level parameters. Lionfish vital rates were estimated from existing literature and from new field and laboratory studies. Sensitivity analysis of lower-level parameters revealed that population growth rate is most influenced by larval mortality; elasticity analysis of the matrix indicated strong influence of the adult and juvenile survival elements. Based on this model, approximately 27% of an invading adult lionfish population would have to be removed monthly for abundance to decrease. Hierarchical modeling indicated that this point estimate falls within a broad uncertainty interval which could result from imprecise estimates of life-history parameters. The model demonstrated that sustained removal efforts could be substantially more effective by targeting juveniles as well as adults.     

Age-dependent strategies related to lionfish activities in the Mexican Caribbean

Lionfish are successful invasive predators in the Caribbean region and inhabit a large range of habitats. Our study in the Caribbean has focused on the relationships between the biological characteristics of lionfish particularly their size, their activities and use of those different habitats. In this study, we observed a high number of lionfish individuals, focusing on the behavioural activities and biological traits in relation to different habitats and environmental characteristics. We monitored 793 individuals, recording their activities, biological traits, and habitat characteristics. Our results report that lionfish are not solitary, but frequently form groups for many activities. We provide evidence of differences between lionfish habitat use according to activity, and the size of individual fish. Considering the size is correlated with age, coral reefs appear to be the preferred habitat of older individuals, whereas the youngest lionfish use a diversity of habitats, ranging from mangroves to coral reefs. In addition, this study suggests that predation of lionfish is age-dependent strategy, and depends on time and the tone of the environment. Lionfish do not only use the head-down posture to catch prey but also horizontal and head-up postures. The youngest lionfish hunt mainly in dark areas and during the night while the older fish were observed hunting mostly during the day and in clear areas. These new aspects of lionfish ecology and behaviour are discussed in light of their invasive success.