Effects of invasive Pacific red lionfish Pterois volitans vs. 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 wk 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% reductions); (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.Keywords: predation, marine fishes, piscivory, community structure, coral reefs, invasive specie

Effects of the invasive Pacific red lionfish Pterois volitans on native Atlantic coral-reef fish communities

Predatory lionfishes (Pterois volitans and P. miles) were introduced to Florida waters during the mid to late 1980s, and eventually established self-sustaining breeding populations in the tropical western Atlantic. These invasive species are now widespread along the southeastern seaboard of the United States, across the Caribbean Sea, and in the Gulf of Mexico. In these regions, lionfish reach larger maximum sizes and higher abundances than they do in their native Pacific, suggesting that they have undergone ecological release. Invaded marine communities have thus far provided little if any biotic resistance. Lionfish are generalist predators with high consumption rates, inhabit a broad range of habitats, are defended from predation by venomous spines, and are capable of long-range larval dispersal. It is possible that lionfish have direct effects on native communities, through consumption of native fishes and competition with native predators, as well as indirect effects, such as overconsumption of herbivorous fishes that prevent seaweeds from outcompeting reef-building corals. There is also serious concern that invasive lionfish could act additively, or even synergistically, with existing stressors of coral-reef systems, such as overfishing and ocean warming, resulting in substantial negative consequences for native ecosystems and economically valuable fisheries. The primary goal of this dissertation was to conduct a set of controlled, replicated field experiments to rigorously examine and measure the effects of lionfish on native reef-fish communities across a range of spatial and temporal scales. In the first experiment (Chapter 2), the net recruitment of native fishes to twenty small patch reefs was compared in the presence (n = 10) and absence (n = 10) of lionfish. This study demonstrated that lionfish reduced net recruitment, or change in abundance of small native fishes, by an average (± SEM) of 78.9 ± 32.2 % over 5 weeks, affecting 23 of 38 species recruiting to reefs in both treatments. In a second experiment (Chapter 4), I examined the effects of lionfish on patch-reef communities of small native fishes relative to, and in combination with, those of a similarly sized native predator, the coney grouper (Cephalopholis fulva). Four different predator treatments were established by transplanting predators (n = 5 reefs each). Treatments included a single small invasive lionfish, a single small native grouper, a grouper and a lionfish together, and predator-free controls. Compared to controls, invasive lionfish caused reductions (mean ± SEM) in abundance (93.7 ± 17.8 %) and species richness (4.6 ± 1.6 species) of small native fishes. The negative effect of lionfish on abundance was 2.6 ± 0.5 times stronger than that of the native grouper. The greatest negative effects on abundance, species richness, evenness, and diversity of native fishes occurred when both lionfish and native grouper were present. Additionally, lionfish grew more than six times faster in both length and mass than did native grouper. A third experiment (Chapter 6) assessed the effects of lionfish on native reef-fish communities at spatial and temporal scales directly relevant to management and conservation efforts. Subsequent to baseline surveys, high- and low-density lionfish treatments were established on 10 large (1400 to 4000 m²) isolated coral reefs. After initiation of treatments, quarterly surveys of the native reef-fish communities were conducted for approximately 14 months. Lionfish caused significant reductions (mean ± SEM) in density (up to 3.22 ± 0.95 fish m⁻²), biomass (3.26 ± 1.10 g m⁻²), and species richness (4.92 ± 2.09 species) of small (<10 cm TL) native fishes. However, these negative effects on prey-sized fishes had not yet translated into declines in larger size classes during the first 14 months of this experiment. In addition to field experiments, this dissertation describes field and aquarium observations of a previously undocumented piscivorous behavior by invasive lionfish - blowing jets of water at prey fish - which may confer a high degree of predation efficiency, thus contributing to the dramatic success of the invasion (Chapter 5). Also provided is a review of the current state of knowledge about the lionfish invasion, with speculation on the long-term effects of the invasion on coral-reef communities, and a brief discussion of potential mitigation measures (Chapter 3). In sum, this research demonstrated that invasive lionfish have substantial negative effects on native communities of coral-reef fishes. In all cases, numerical reductions in small (prey-sized) native fishes caused by lionfish were substantial. Additionally, lionfish caused considerable reductions in native reef-fish species richness (via predation on rare species). These findings indicate that the lionfish invasion may have long-term, broad-scale impacts on the structure and function of coral-reef communities as a whole, potentially reducing the resilience of these systems to a myriad of existing stressors as well as their capacity to provide valuable ecosystem goods and services to humans

Worst case scenario: Potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities

The Pacific red lionfish has recently invaded Western Atlantic and Caribbean coral reefs, and may become one of the most ecologically harmful marine fish introductions to date. Lionfish possess a broad suite of traits that makes them particularly successful invaders and strong negative interactors with native fauna, including defensive venomous spines, cryptic form, color and behavior, habitat generality, high competitive ability, low parasite load, efficient predation, rapid growth, and high reproductive rates. With an eye on the future, we describe a possible “worst case scenario” in which the direct and indirect effects of lionfish could combine with the impacts of preexisting stressors -- especially overfishing -- and cause substantial deleterious changes in coral-reef communities. We also discuss management actions that could be taken to minimize these potential effects by, first, developing targeted lionfish fisheries and local removals, and second, enhancing native biotic resistance, particularly via marine reserves that could conserve and foster potential natural enemies of this invader. Ultimately, the lionfish invasion will be limited either by starvation -- the worst end to the worst case scenario -- or by some combination of native pathogens, parasites, predators, and competitors.This is an author's peer-reviewed final manuscript, as accepted by the publisher. The published article is copyrighted by Springer and can be found at: http://link.springer.com/journal/10641.Keywords: Ecological release, Invasive species, Coral-reef fishes, Biological invasions, Biotic resistanc

Habitat Associations and Co-Occurrence Patterns of Two Estuarine-Dependent Predatory Fishes

Estuarine-dependent fishes experience a wide range of environmental conditions, and most species exhibit distinct associations with particular habitats. However, similar species or multiple conspecifics often overlap spatiotemporally, which can result in ecological interactions that have consequences for behaviors that can shape the structure and function of ecosystems. We used a long-term gill-net data set (2001–2015) to investigate the habitat associations and cooccurrence patterns of two estuarine-dependent predatory fishes, Red Drum Sciaenops ocellatus and Spotted Seatrout Cynoscion nebulosus, in coastal Alabama, USA. Both species were associated with similar environmental conditions, primarily low dissolved oxygen and low salinity, especially when temperature was low. However, differences emerged between the species with respect to the effects of interacting environmental variables on their habitat use patterns, which were likely driven by physiological, biological, and ecological dissimilarities between them. Concerning their biogenic habitat use, extensive submerged aquatic vegetation (SAV) was an important habitat for both species, but Spotted Seatrout appeared to prefer high-salinity SAV beds, while Red Drum associated with SAV regardless of salinity. Spotted Seatrout were associated with extensive emergent marsh edges, and the positive relationship between Red Drum and SAV was diminished when marsh edge was abundant. Co-occurrence was observed primarily in habitats with which both species were associated, most frequently in shallow, prey-rich marsh edges and high-salinity seagrass beds. These observed habitat use patterns elucidate the subtle differences in resource use that allow these species to coexist and suggest potential areas where interactions between them may shape their roles as predators

Larval Connectivity in an Effective Network of Marine Protected Areas

Acceptance of marine protected areas (MPAs) as fishery and conservation tools has been hampered by lack of direct evidence that MPAs successfully seed unprotected areas with larvae of targeted species. For the first time, we present direct evidence of large-scale population connectivity within an existing and effective network of MPAs. A new parentage analysis identified four parent-offspring pairs from a large, exploited population of the coral-reef fish Zebrasoma flavescens in Hawai'i, revealing larval dispersal distances ranging from 15 to 184 km. In two cases, successful dispersal was from an MPA to unprotected sites. Given high adult abundances, the documentation of any parent-offspring pairs demonstrates that ecologically-relevant larval connectivity between reefs is substantial. All offspring settled at sites to the north of where they were spawned. Satellite altimetry and oceanographic models from relevant time periods indicated a cyclonic eddy that created prevailing northward currents between sites where parents and offspring were found. These findings empirically demonstrate the effectiveness of MPAs as useful conservation and management tools and further highlight the importance of coupling oceanographic, genetic, and ecological data to predict, validate and quantify larval connectivity among marine populations

Larval Connectivity in an Effective Network of Marine Protected Areas

Acceptance of marine protected areas (MPAs) as fishery and conservation tools has been hampered by lack of direct evidence that MPAs successfully seed unprotected areas with larvae of targeted species. For the first time, we present direct evidence of large-scale population connectivity within an existing and effective network of MPAs. A new parentage analysis identified four parent-offspring pairs from a large, exploited population of the coral-reef fish Zebrasoma flavescens in Hawai'i, revealing larval dispersal distances ranging from 15 to 184 km. In two cases, successful dispersal was from an MPA to unprotected sites. Given high adult abundances, the documentation of any parent-offspring pairs demonstrates that ecologically-relevant larval connectivity between reefs is substantial. All offspring settled at sites to the north of where they were spawned. Satellite altimetry and oceanographic models from relevant time periods indicated a cyclonic eddy that created prevailing northward currents between sites where parents and offspring were found. These findings empirically demonstrate the effectiveness of MPAs as useful conservation and management tools and further highlight the importance of coupling oceanographic, genetic, and ecological data to predict, validate and quantify larval connectivity among marine populations

Names, codes, and characteristics of species observed during reef surveys in the Bahamas (Lionfish Invasion project)

Dataset: species listNames, codes, and characteristics of species observed during reef surveys in the Bahamas (Lionfish Invasion project). For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/3896NSF Division of Ocean Sciences (NSF OCE) OCE-085116

AlbinsMarkA2011_Movie_5.1.avi

Predatory lionfishes (Pterois volitans and P. miles) were introduced to Florida waters during the mid to late 1980s, and eventually established self-sustaining breeding populations in the tropical western Atlantic. These invasive species are now widespread along the southeastern seaboard of the United States, across the Caribbean Sea, and in the Gulf of Mexico. In these regions, lionfish reach larger maximum sizes and higher abundances than they do in their native Pacific, suggesting that they have undergone ecological release. Invaded marine communities have thus far provided little if any biotic resistance. Lionfish are generalist predators with high consumption rates, inhabit a broad range of habitats, are defended from predation by venomous spines, and are capable of long-range larval dispersal. It is possible that lionfish have direct effects on native communities, through consumption of native fishes and competition with native predators, as well as indirect effects, such as overconsumption of herbivorous fishes that prevent seaweeds from outcompeting reef-building corals. There is also serious concern that invasive lionfish could act additively, or even synergistically, with existing stressors of coral-reef systems, such as overfishing and ocean warming, resulting in substantial negative consequences for native ecosystems and economically valuable fisheries. The primary goal of this dissertation was to conduct a set of controlled, replicated field experiments to rigorously examine and measure the effects of lionfish on native reef-fish communities across a range of spatial and temporal scales. In the first experiment (Chapter 2), the net recruitment of native fishes to twenty small patch reefs was compared in the presence (n = 10) and absence (n = 10) of lionfish. This study demonstrated that lionfish reduced net recruitment, or change in abundance of small native fishes, by an average (± SEM) of 78.9 ± 32.2 % over 5 weeks, affecting 23 of 38 species recruiting to reefs in both treatments. In a second experiment (Chapter 4), I examined the effects of lionfish on patch-reef communities of small native fishes relative to, and in combination with, those of a similarly sized native predator, the coney grouper (Cephalopholis fulva). Four different predator treatments were established by transplanting predators (n = 5 reefs each). Treatments included a single small invasive lionfish, a single small native grouper, a grouper and a lionfish together, and predator-free controls. Compared to controls, invasive lionfish caused reductions (mean ± SEM) in abundance (93.7 ± 17.8 %) and species richness (4.6 ± 1.6 species) of small native fishes. The negative effect of lionfish on abundance was 2.6 ± 0.5 times stronger than that of the native grouper. The greatest negative effects on abundance, species richness, evenness, and diversity of native fishes occurred when both lionfish and native grouper were present. Additionally, lionfish grew more than six times faster in both length and mass than did native grouper. A third experiment (Chapter 6) assessed the effects of lionfish on native reef-fish communities at spatial and temporal scales directly relevant to management and conservation efforts. Subsequent to baseline surveys, high- and low-density lionfish treatments were established on 10 large (1400 to 4000 m²) isolated coral reefs. After initiation of treatments, quarterly surveys of the native reef-fish communities were conducted for approximately 14 months. Lionfish caused significant reductions (mean ± SEM) in density (up to 3.22 ± 0.95 fish m⁻²), biomass (3.26 ± 1.10 g m⁻²), and species richness (4.92 ± 2.09 species) of small (<10 cm TL) native fishes. However, these negative effects on prey-sized fishes had not yet translated into declines in larger size classes during the first 14 months of this experiment. In addition to field experiments, this dissertation describes field and aquarium observations of a previously undocumented piscivorous behavior by invasive lionfish - blowing jets of water at prey fish - which may confer a high degree of predation efficiency, thus contributing to the dramatic success of the invasion (Chapter 5). Also provided is a review of the current state of knowledge about the lionfish invasion, with speculation on the long-term effects of the invasion on coral-reef communities, and a brief discussion of potential mitigation measures (Chapter 3). In sum, this research demonstrated that invasive lionfish have substantial negative effects on native communities of coral-reef fishes. In all cases, numerical reductions in small (prey-sized) native fishes caused by lionfish were substantial. Additionally, lionfish caused considerable reductions in native reef-fish species richness (via predation on rare species). These findings indicate that the lionfish invasion may have long-term, broad-scale impacts on the structure and function of coral-reef communities as a whole, potentially reducing the resilience of these systems to a myriad of existing stressors as well as their capacity to provide valuable ecosystem goods and services to humans

Fish species survey from the Bahamas from 2009-2012.

Dataset: Fish species surveyFish species survey from the Bahamas from 2009-2012. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/700226NSF Division of Ocean Sciences (NSF OCE) OCE-123302

AlbinsMarkA2011.pdf

Predatory lionfishes (Pterois volitans and P. miles) were introduced to Florida waters during the mid to late 1980s, and eventually established self-sustaining breeding populations in the tropical western Atlantic. These invasive species are now widespread along the southeastern seaboard of the United States, across the Caribbean Sea, and in the Gulf of Mexico. In these regions, lionfish reach larger maximum sizes and higher abundances than they do in their native Pacific, suggesting that they have undergone ecological release. Invaded marine communities have thus far provided little if any biotic resistance. Lionfish are generalist predators with high consumption rates, inhabit a broad range of habitats, are defended from predation by venomous spines, and are capable of long-range larval dispersal. It is possible that lionfish have direct effects on native communities, through consumption of native fishes and competition with native predators, as well as indirect effects, such as overconsumption of herbivorous fishes that prevent seaweeds from outcompeting reef-building corals. There is also serious concern that invasive lionfish could act additively, or even synergistically, with existing stressors of coral-reef systems, such as overfishing and ocean warming, resulting in substantial negative consequences for native ecosystems and economically valuable fisheries. The primary goal of this dissertation was to conduct a set of controlled, replicated field experiments to rigorously examine and measure the effects of lionfish on native reef-fish communities across a range of spatial and temporal scales. In the first experiment (Chapter 2), the net recruitment of native fishes to twenty small patch reefs was compared in the presence (n = 10) and absence (n = 10) of lionfish. This study demonstrated that lionfish reduced net recruitment, or change in abundance of small native fishes, by an average (± SEM) of 78.9 ± 32.2 % over 5 weeks, affecting 23 of 38 species recruiting to reefs in both treatments. In a second experiment (Chapter 4), I examined the effects of lionfish on patch-reef communities of small native fishes relative to, and in combination with, those of a similarly sized native predator, the coney grouper (Cephalopholis fulva). Four different predator treatments were established by transplanting predators (n = 5 reefs each). Treatments included a single small invasive lionfish, a single small native grouper, a grouper and a lionfish together, and predator-free controls. Compared to controls, invasive lionfish caused reductions (mean ± SEM) in abundance (93.7 ± 17.8 %) and species richness (4.6 ± 1.6 species) of small native fishes. The negative effect of lionfish on abundance was 2.6 ± 0.5 times stronger than that of the native grouper. The greatest negative effects on abundance, species richness, evenness, and diversity of native fishes occurred when both lionfish and native grouper were present. Additionally, lionfish grew more than six times faster in both length and mass than did native grouper. A third experiment (Chapter 6) assessed the effects of lionfish on native reef-fish communities at spatial and temporal scales directly relevant to management and conservation efforts. Subsequent to baseline surveys, high- and low-density lionfish treatments were established on 10 large (1400 to 4000 m²) isolated coral reefs. After initiation of treatments, quarterly surveys of the native reef-fish communities were conducted for approximately 14 months. Lionfish caused significant reductions (mean ± SEM) in density (up to 3.22 ± 0.95 fish m⁻²), biomass (3.26 ± 1.10 g m⁻²), and species richness (4.92 ± 2.09 species) of small (<10 cm TL) native fishes. However, these negative effects on prey-sized fishes had not yet translated into declines in larger size classes during the first 14 months of this experiment. In addition to field experiments, this dissertation describes field and aquarium observations of a previously undocumented piscivorous behavior by invasive lionfish - blowing jets of water at prey fish - which may confer a high degree of predation efficiency, thus contributing to the dramatic success of the invasion (Chapter 5). Also provided is a review of the current state of knowledge about the lionfish invasion, with speculation on the long-term effects of the invasion on coral-reef communities, and a brief discussion of potential mitigation measures (Chapter 3). In sum, this research demonstrated that invasive lionfish have substantial negative effects on native communities of coral-reef fishes. In all cases, numerical reductions in small (prey-sized) native fishes caused by lionfish were substantial. Additionally, lionfish caused considerable reductions in native reef-fish species richness (via predation on rare species). These findings indicate that the lionfish invasion may have long-term, broad-scale impacts on the structure and function of coral-reef communities as a whole, potentially reducing the resilience of these systems to a myriad of existing stressors as well as their capacity to provide valuable ecosystem goods and services to humans