Length‐weight and length‐length relationships of the invasive red lionfish [Pterois volitans (Linnaeus, 1758): Scorpaenidae] in the Parque Nacional Arrecife Alacranes,Southern Gulf of Mexico

Described are the length–weight (LW) and length–length (LL) relationships of the Indo–Pacific, red lionfish [Pterois volitans (Linnaeus, 1758): Scorpaenidae] – an invasive fish introduced into the coral reefs of the Western Atlantic. Volunteer diver‐fishers speared a total of 455 red lionfish (range 9–35 cm TL) from July 2010 to December 2011 in the Parque Nacional Arrecife Alacranes, off the northern coast of the Yucatan Peninsula, Mexico. The LWR obtained in the combined data was W = 0.104TL^3.309.     

Habitat complexity and fish size affect the detection of Indo-Pacific lionfish on invaded coral reefs

A standard approach to improving the accuracy of reef fish population estimates derived from underwater visual censuses (UVCs) is the application of species-specific correction factors, which assumes that a species’ detectability is constant under all conditions. To test this assumption, we quantified detection rates for invasive Indo-Pacific lionfish (Pterois volitans and P. miles), which are now a primary threat to coral reef conservation throughout the Caribbean. Estimates of lionfish population density and distribution, which are essential for managing the invasion, are currently obtained through standard UVCs. Using two conventional UVC methods, the belt transect and stationary visual census (SVC), we assessed how lionfish detection rates vary with lionfish body size and habitat complexity (measured as rugosity) on invaded continuous and patch reefs off Cape Eleuthera, the Bahamas. Belt transect and SVC surveys performed equally poorly, with both methods failing to detect the presence of lionfish in >50 % of surveys where thorough, lionfish-focussed searches yielded one or more individuals. Conventional methods underestimated lionfish biomass by ~200 %. Crucially, detection rate varied significantly with both lionfish size and reef rugosity, indicating that the application of a single correction factor across habitats and stages of invasion is unlikely to accurately characterize local populations. Applying variable correction factors that account for site-specific lionfish size and rugosity to conventional survey data increased estimates of lionfish biomass, but these remained significantly lower than actual biomass. To increase the accuracy and reliability of estimates of lionfish density and distribution, monitoring programs should use detailed area searches rather than standard visual survey methods. Our study highlights the importance of accounting for sources of spatial and temporal variation in detection to increase the accuracy of survey data from coral reef systems.     

Habitat-Specific Density and Diet of Rapidly Expanding Invasive Red Lionfish,Pterois volitans,Populations in the Northern Gulf of Mexico

Invasive Indo-Pacific red lionfish, Pterois volitans, were first reported in the northern Gulf of Mexico (nGOM) in summer 2010. To examine potential impacts on native reef fish communities, lionfish density and size distributions were estimated from fall 2010 to fall 2013 with a remotely operated vehicle at natural (n = 16) and artificial (n = 22) reef sites. Lionfish (n = 934) also were sampled via spearfishing to examine effects of habitat type, season, and fish size on their diet and trophic ecology. There was an exponential increase in lionfish density at both natural and artificial reefs over the study period. By fall 2013, mean lionfish density at artificial reefs (14.7 fish 100 m⁻²) was two orders of magnitude higher than at natural reefs (0.49 fish 100 m⁻²), and already was among the highest reported in the western Atlantic. Lionfish diet was significantly different among habitats, seasons, and size classes, with smaller (<250 mm total length) fish consuming more benthic invertebrates and the diet of lionfish sampled from artificial reefs being composed predominantly of non-reef associated prey. The ontogenetic shift in lionfish feeding ecology was consistent with δ¹⁵N values of white muscle tissue that were positively related to total length. Overall, diet results indicate lionfish are generalist mesopredators in the nGOM that become more piscivorous at larger size. However, lionfish diet was much more varied at artificial reef sites where they clearly were foraging on open substrates away from reef structure. These results have important implications for tracking the lionfish invasion in the nGOM, as well as estimating potential direct and indirect impacts on native reef fish communities in this region.     

Chimpanzee identification and social network construction through an online citizen science platform

Citizen science has grown rapidly in popularity in recent years due to its potential to educate and engage the public while providing a means to address a myriad of scientific questions. However, the rise in popularity of citizen science has also been accompanied by concerns about the quality of data emerging from citizen science research projects. We assessed data quality in the online citizen scientist platform Chimp&See, which hosts camera trap videos of chimpanzees (Pan troglodytes) and other species across Equatorial Africa. In particular, we compared detection and identification of individual chimpanzees by citizen scientists with that of experts with years of experience studying those chimpanzees. We found that citizen scientists typically detected the same number of individual chimpanzees as experts, but assigned far fewer identifications (IDs) to those individuals. Those IDs assigned, however, were nearly always in agreement with the IDs provided by experts. We applied the data sets of citizen scientists and experts by constructing social networks from each. We found that both social networks were relatively robust and shared a similar structure, as well as having positively correlated individual network positions. Our findings demonstrate that, although citizen scientists produced a smaller data set based on fewer confirmed IDs, the data strongly reflect expert classifications and can be used for meaningful assessments of group structure and dynamics. This approach expands opportunities for social research and conservation monitoring in great apes and many other individually identifiable species.     

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.     

Trying to collapse a population for conservation: commercial trade of a marine invasive species by artisanal fishers

Implementing new and effective control strategies to reduce populations of invasive species is needed to offset their negative impacts worldwide. The spread of Indo-Pacific lionfish (Pterois sp.) through much of the western Atlantic has been one of the most publicized marine invasions globally, and is considered a major biodiversity threat whose longer-term impacts are still uncertain. Marine managers have explored several strategies to control lionfish, such as fishing tournaments (derbies) and commercial fisheries. Commercial fisheries for invasive species are controversial because they could create perverse incentives to maintain these populations, and they have never been demonstrated to successfully control target populations. We analyzed the development and impacts of an opportunistic fishing operation aimed at commercializing invasive lionfish in the Mexican Caribbean. We examined official lionfish landings and compared them to catches from lionfish derbies and lionfish densities from locations in the state of Quintana Roo, Mexico. We found that commercial fishers, particularly from one fishing cooperative on Cozumel Island, were effective at catching lionfish, with landings peaking at 20,000 individuals in 2014. This number is comparable to the number of lionfish caught in derbies across the entire Caribbean in the same year. Ecological survey data suggest a?~?60% reduction in lionfish density on Cozumel reefs over two years (2013–2015), matching the peak landings in the lionfish fishing operation. However, the fishery’s apparent success as a control tool during the time window analyzed seemed to trigger its own demise: a decline in landings was followed by evaporating market interest and loss of economic viability. If fisheries are to be established and used as management strategies to control future invasions, managers must develop strategic collaboration plans with commercial fishing partners.

     

DNA barcoding significantly improves resolution of invasive lionfish diet in the Northern Gulf of Mexico

Invasive Indo-Pacific red lionfish (Pterois volitans) have become well-established residents within reef communities across the western Atlantic Ocean where they pose substantial threats to native fish communities and reef ecosystems. Species-specific identification of prey is necessary to elucidate predator–prey interactions, but can be challenging with traditional visual identification methods given prey are often highly digested, thus not identifiable visually. To supplement visual diet analysis of lionfish (n = 934) sampled in the northern Gulf of Mexico, we applied DNA barcoding to identify otherwise unidentifiable fish prey (n = 696) via amplification of the cytochrome c oxidase subunit I (COI) of the mitochondrial genome. Barcoding nearly doubled the number of identifiable fish prey, thereby greatly enhancing our ability to describe lionfish diet. Thirty-three fish prey species were identified via barcoding, twenty-four of which were not previously detected by traditional methods. Some exploited reef fishes were newly reported (e.g., red snapper, Lutjanus campechanus) or found to constitute higher proportions of lionfish diet than previously reported (e.g., vermilion snapper, Rhomboplites aurorubens). Barcoding added a significant amount of new dietary information, and we observed the highest prey diversity reported to date for invasive lionfish. Potential cannibalism on juveniles also was identified via DNA barcoding, with the highest incidence corresponding to high lionfish densities, thus suggesting density-dependent prey demand may have driven this response. Overall, DNA barcoding greatly enhanced our ability to describe invasive lionfish diet in this study, suggesting that even studies with relatively large diet sample sizes could benefit from barcoding analysis.     

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.     

Density-Dependent Growth in Invasive Lionfish (Pterois volitans)

Direct demographic density dependence is necessary for population regulation and is a central concept in ecology, yet has not been studied in many invasive species, including any invasive marine fish. The red lionfish (Pterois volitans) is an invasive predatory marine fish that is undergoing exponential population growth throughout the tropical western Atlantic. Invasive lionfish threaten coral-reef ecosystems, but there is currently no evidence of any natural population control. Therefore, a manipulative field experiment was conducted to test for density dependence in lionfish. Juvenile lionfish densities were adjusted on small reefs and several demographic rates (growth, recruitment, immigration, and loss) were measured throughout an 8-week period. Invasive lionfish exhibited direct density dependence in individual growth rates, as lionfish grew slower at higher densities throughout the study. Individual growth in length declined linearly with increasing lionfish density, while growth in mass declined exponentially with increasing density. There was no evidence, however, for density dependence in recruitment, immigration, or loss (mortality plus emigration) of invasive lionfish. The observed density-dependent growth rates may have implications for which native species are susceptible to lionfish predation, as the size and type of prey that lionfish consume is directly related to their body size. The absence of density-dependent loss, however, contrasts with many native coral-reef fish species and suggests that for the foreseeable future manual removals may be the only effective local control of this invasion.     

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.     

Citizen Science as a New Tool in Dog Cognition Research

Family dogs and dog owners offer a potentially powerful way to conduct citizen science to answer questions about animal behavior that are difficult to answer with more conventional approaches. Here we evaluate the quality of the first data on dog cognition collected by citizen scientists using the Dognition.com website. We conducted analyses to understand if data generated by over 500 citizen scientists replicates internally and in comparison to previously published findings. Half of participants participated for free while the other half paid for access. The website provided each participant a temperament questionnaire and instructions on how to conduct a series of ten cognitive tests. Participation required internet access, a dog and some common household items. Participants could record their responses on any PC, tablet or smartphone from anywhere in the world and data were retained on servers. Results from citizen scientists and their dogs replicated a number of previously described phenomena from conventional lab-based research. There was little evidence that citizen scientists manipulated their results. To illustrate the potential uses of relatively large samples of citizen science data, we then used factor analysis to examine individual differences across the cognitive tasks. The data were best explained by multiple factors in support of the hypothesis that nonhumans, including dogs, can evolve multiple cognitive domains that vary independently. This analysis suggests that in the future, citizen scientists will generate useful datasets that test hypotheses and answer questions as a complement to conventional laboratory techniques used to study dog psychology.     

More than an empty case: a non invasive technique for monitoring the Australian critically endangered golden sun moth, Synemon plana (Lepidoptera: Castniidae)

Monitoring programs for butterflies and moths are focused on the adult stage, rarely considering other life stages. Transect-based counts of adults and searches for empty pupal cases have been suggested as standard monitoring protocols for the critically endangered golden sun moth Synemon plana in Australia. To date, surveys and monitoring have focused only on counts of adults. However, undertaking such counts is constrained by the short adult life of the species (1–2 days), and the fact that prevailing weather conditions can seriously influence detectability. We tested whether empty pupal cases of S. plana can be used to supplement the monitoring of adults and whether this technique can be undertaken by citizen scientists. Volunteers from Canberra (Australia) collected 650 pupal cases from 11 grassland areas. The cases were found in native grasslands and in grassland comprised entirely of the exotic Chilean needle grass (Nassella neesiana). Pupal cases of S. plana were found to be durable, with most persisting in the field for greater than 3 weeks after first sighting, and exhibited a male biased sex ratio. This study demonstrates that detection of empty pupal cases provides a potential additional tool to monitor S. plana that is not dependent on the restrictions of prevailing weather conditions and time of day, and can be undertaken by citizen scientists.     

How to work with children and animals: A guide for school‐based citizen science in wildlife research

Engaging school students in wildlife research through citizen science projects can be a win–win for scientists and educators. Not only does it provide a way for scientists to gather new data, but it can also contribute to science education and help younger generations become more environmentally aware. However, wildlife research can be challenging in the best of circumstances, and there are few guidelines available to help scientists create successful citizen science projects for school students. This paper explores the opportunities and challenges faced when developing school‐based citizen science projects in wildlife research by synthesising two sources of information. First, we conducted a small, school‐based citizen science project that investigated the effects of supplementary feeding on urban birds as a case study. Second, we reviewed the literature to develop a database of school‐based citizen science projects that address questions in wildlife ecology and conservation. Based on these activities, we present five lessons for scientists considering a school‐based citizen science project. Overall, we found that school‐based citizen science projects must be carefully designed to ensure reliable data are collected, students remain engaged, and the project is achievable under the logistical constraints presented by conducting wildlife research in a school environment. Ultimately, we conclude that school‐based citizen science projects can be a powerful way of collecting wildlife data while also contributing to the education and development of environmentally aware students.     

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.     

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.     

First Record of Invasive Lionfish (Pterois volitans) for the Brazilian Coast

The invasion of the northwestern Atlantic by the Indo-Pacific lionfish has developed extraordinarily fast, and is expected to cause one of the most negative ecological impacts among all marine invasions. In less than 30 years, lionfish have dramatically expanded their distribution range to an area encompassing the eastern coast of the USA, Bermuda, the entire Caribbean region and the Gulf of Mexico. The rapidity of the lionfish spread has raised concerns in other parts of the Atlantic that may be under the reach of the invasion. Despite the anticipation that lionfish would eventually extend their range throughout most of the eastern coast of South America, it had not been recorded in Brazil until now. Here we report the first lionfish appearance for the Brazilian coast and show that the individual collected by us is genetically linked to the invasive Caribbean population. Since small-range endemics are found in several locations in Brazil and are among the species that are most vulnerable to extinction, we recommend urgent control, management and education measures aimed at minimizing the effects of this impending invasion.     

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.     

Forecasting lionfish sources and sinks in the Atlantic: are Gulf of Mexico reef fisheries at risk?

Invasive lionfish (Pterois volitans/miles complex) now permeate the entire tropical western Atlantic, Caribbean Sea, and Gulf of Mexico, but lionfish abundance has been measured only in select locations in the field. Despite its rapid range expansion, a comprehensive meta-population analysis of lionfish ‘sources’ and ‘sinks’ and consequentially the invader’s potential abundance and impacts on economically important, sympatric reef fishes have not been assessed. These data are urgently needed to spatially direct control efforts and to plan for and perhaps mitigate lionfish-caused damage. Here, we use a biophysical computer model to: (1) forecast larval lionfish sources and sinks that are also delineated as low to high lionfish ‘density zones’ throughout their invaded range, and (2) assess the potential vulnerability of five grouper and snapper species—Epinephelus morio, Mycteroperca microlepis, Epinephelus flavolimbatus, Lutjanus campechanus, and Rhomboplites aurorubens—to lionfish within these density zones in the Gulf of Mexico. Our results suggest that the west Florida shelf and nearshore waters of Texas, USA, and Guyana, South America, function both as lionfish sources and sinks and should be a high priority for targeted lionfish control. Furthermore, of the five groupers and snappers studied, the high fishery value E. morio (red grouper) is the Gulf of Mexico species most at risk from lionfish. Lacking a comprehensive lionfish control policy, these risk exposure data inform managers where removals should be focused and demonstrate the risk to five sympatric native groupers and snappers in the Gulf of Mexico that may be susceptible to dense lionfish aggregations, should control efforts fail.     

Generating spatial data for marine conservation and management

Do fishers know best when it comes to identifying areas with rare and depleted fish species? The global conservation crisis demands that managers marshal all available datasets to inform conservation management plans for depleted species, yet the level of trust placed in local knowledge remains uncertain. This study compares four methods for inferring species distributions of an internationally traded, rare and depleted genus of marine fishes (Hippocampus spp.): the use of (i) fisher interviews; (ii) government research trawls, (iii) scientific diving surveys, and (iv) citizen science contributions. We analyzed these four datasets at the genus and individual species levels to evaluate our conclusions about seahorse spatial occurrence, diversity of species present and the cost effectiveness of sampling effort. We found that fisher knowledge provided more information on our data-poor fish genus at larger spatial scales, with less effort, and for a cheaper price than all other datasets. One drawback was that fishers were unable to provide data down to the species level. People embarking on conservation endeavors for data-poor species may wish to begin with fisher interviews and use these to inform the application of government research, scientific diving, or citizen science programs.