A human-bred aquarium fish prized for its bright colour and head hump has escaped into a Philippines crater lake, where scientists fear it may threaten native biodiversity

A human-bred aquarium fish prized for its bright gold colour and distinctive head hump has escaped into a volcanic crater lake in the Philippines, where scientists fear it is threatening native wildlife and spreading into local aquaculture. Flowerhorn cichlids, an artificial hybrid species created by crossbreeding various cichlid varieties for the ornamental pet trade, are believed to have entered Lake Sampaloc after escaping from nearby breeding facilities during a typhoon. The 104-hectare water body, located in San Pablo City, now hosts an established wild population of the invasive predator.Research conducted by Hannah Nicole C Gasmen and Dr Janice A Ragaza of Ateneo de Manila University reveals that the fish have successfully integrated into the lake’s ecosystem. Because flowerhorns are highly adaptable and can survive in harsh, degraded environments, local fish farmers are keeping individuals that enter tilapia cages and selling them back into the pet trade. Some residents have even begun stocking them intentionally in local waters.The researchers warn that deliberate stocking and resale will expand an already invasive wild population across the crater lake, creating a self-sustaining cycle that threatens the delicate balance of the local ecosystem. Lake Sampaloc was already suffering from heavy environmental pressure before the hybrid fish arrived. Untreated sewage, household runoff, agricultural nutrients, and plastic waste have caused severe eutrophication, making the water body particularly vulnerable to invasive species.Flowerhorns thrive in these polluted, nutrient-rich conditions, competing aggressively with local species for food, breeding grounds, and shelter. The native ayungin, or silver perch, which was once a common catch for local fishers and a staple of the regional diet, has become increasingly rare. The species is now classified as endangered by the International Union for Conservation of Nature.Rupert Collins, senior curator of fish at London’s Natural History Museum, said degraded environments often create ideal conditions for adaptable generalist species, allowing them to spread and replace native marine life.“Human-degraded habitats are generally the most vulnerable to invasion, and they are typically invaded by generalist species,” said Collins. “Cichlids are particularly successful in adapting. They are a textbook example of how new phenotypes can arise very quickly.”

Parasite risks and culinary use

Alongside ecological damage, the study highlights potential health risks to the surrounding human population. In captive settings, some flowerhorns have been found carrying Paracapillaria philippinensis, a parasitic roundworm capable of causing severe intestinal disease in humans. Local residents have been observed catching wild flowerhorns for recreation and cooking them for household meals. Although laboratory tests have not yet detected the parasite in Lake Sampaloc’s current flowerhorn population, Gasmen and Ragaza advise against promoting the fish for human consumption due to the inherent biological risks.The situation in Lake Sampaloc reflects a broader global environmental crisis involving the accidental or intentional release of domestic pets into wild habitats. As Collins pointed out, the release of non-native fish extends far beyond a single volcanic lake in the Philippines.“This is just one lake in the Philippines, but the release of species outside their natural ranges is a major contributor to biodiversity loss worldwide,” Collins said.

Shifting climates and changing lakes

Environmental scientists warn that climate pressures and changing weather patterns could make similar ecological disruptions far more frequent across global waterways. Dr Noël Juvigny-Khenafou, a lecturer in aquatic environmental science at the University of Stirling who was not involved in the Ateneo de Manila study, pointed out that changing weather patterns will alter how humans farm fish and where aquaculture systems can safely operate.“Climate change may alter where aquaculture takes place and what species people are able to raise,” Juvigny-Khenafou said. “That could mean production shifting between regions and more non-native species being introduced into new places.” He noted that the successful integration of human-bred hybrid fish into Lake Sampaloc raises fundamental questions about the future function of damaged freshwater ecosystems in an era of rapid environmental change.“What does that mean for the native species? What does that mean for the function of the ecosystem? Is the introduced species leading the ecosystem towards collapse, or is it simply becoming part of a new ecological community?” Juvigny-Khenafou said. Escaped or deliberately released aquarium fish have heavily impacted Philippine freshwater ecosystems. Notable invasive species include the Flowerhorn, Midas Cichlid, Janitor Fish, and Tinfoil Barb, which outcompete native species and degrade habitats in lakes like Taal and Sampaloc. Invasive aquarium fish threatens San Pablo’s Lake Sampaloc Sought after in the aquarium trade for their vibrant golden hue, Flowerhorn cichlids are becoming a concerning invasive presence in Lake Sampaloc. PHOTO COURTESY OF ADMU RESEARCH COMMUNICATIONS SECTION

MANILA, Philippines — A bright golden aquarium fish has become an invasive threat to biodiversity and aquaculture in Lake Sampaloc in San Pablo City, Laguna, researchers said.

Lake Sampaloc, the largest and most famous of the Seven Lakes of San Pablo, is a 104-hectare maar lake formed by a volcanic eruption.

Researchers from the Ateneo de Manila University Department of Biology and the Ateneo Aquatic and Fisheries Resources Laboratory said the flowerhorn cichlid is increasingly taking “an outsized role in both the natural ecosystem and local aquaculture operations.”

They documented the widespread presence of flowerhorn cichlids (Amphilophus spp.) in the volcanic crater lake, noting that their “fenced and feral” status is intensifying pressure on native biodiversity and posing potential risks to public health. Researchers Hannah Nicole Gasmen and Dr. Janice Ragaza found that the species “are no longer merely escaped ornamental fishes, but have become integrated into local aquaculture through intentional retention and sale.” They said this has had a sharp impact on native species, as flowerhorns, known for territorial aggression, tend to monopolize breeding grounds and feeding sites.

Consequently, the native ayungin (Leiopotherapon plumbeus), once a common local staple, is now rarely encountered and is listed as vulnerable by the International Union for Conservation of Nature. “Flowerhorns also display remarkable adaptability to a wide range of environmental conditions,” the researchers said.

While the lake is affected by nutrient runoff, microplastics and trace organic pollutants linked to untreated sewage, household runoff and aquaculture practices, the species’ phenotypic plasticity enables it to thrive and dominate in these anthropogenically stressed waters.

Beyond charting the flowerhorn’s spread, the researchers highlighted broader threats, including pollution, habitat degradation, declining native fish populations and public health concerns.

Previous research has shown that flowerhorns can host Paracapillaria philippinensis, a zoonotic parasite that can cause serious illness in humans, including intestinal capillariasis, an infection that can lead to abdominal pain, chronic diarrhea and malnutrition. “The species may serve as a possible reservoir of parasites, pathogens, and contaminants, providing a strong foundation for future ecological, parasitological, and aquaculture research aimed at developing evidence-based management strategies for invasive Flowerhorn populations,” Gasmen said.

To help manage flowerhorn populations, the researchers proposed a possible circular economy model: harvesting invasive flowerhorns and converting them into aquafeed, provided the biomass is screened for parasites, contaminants and microbiological safety.

Gasmen also pointed to the Aquatic Species Invasiveness Screening Kit (AS-ISK) as a promising tool for assessing invasion risks of nonnative freshwater fish, as demonstrated in a 2024 study of Lake Naujan.

“Applying AS-ISK to Lake Sampaloc and other Philippine lakes could help identify high-risk species early and inform targeted management actions,” she said.

Key Invasive Aquarium Fish in the Philippines

• Flowerhorn Cichlid (Amphilophus spp.): Prized for its bright head hump and coloration, this artificial hybrid escaped from breeding facilities into crater lakes like Lake Sampaloc. They survive exceptionally well in degraded environments, aggressively competing with native species for food and shelter.

A human-bred aquarium fish prized for its bright colour and head hump has escaped into a Philippines crater lake, where scientists fear it may threaten native biodiversity Turning invasive fish into a golden opportunity range of non-native fish species, including Midas cichlids, are now firmly established in the Philippines, but some enterprising farmers are beginning to capitalise on these invaders.

Midas Cichlid (Amphilophus citrinellus): Originally a common aquarium fish from Central America, this golden cichlid has overrun ecosystems like Lake Taal and Lake Sampaloc. Its prolific breeding and aggressive territorial behavior displace native species, though locals have adapted by catching them to sell as dried fish and ornamental pets.

If you gaze hard enough at the olive waters of Lake Sampaloc in the Philippines, you’ll notice darting specks of gold. They’re cichlids from South America, escapees from the aquarium trade and – for good or for naught – now part of the lake’s ecosystem.

Lake Sampaloc, located two hours south of the sprawling Philippine capital of Metro Manila, isn’t the first waterway colonised by non-native fish. Is the aquaculture of invasive and non-native species worth the risk? Is the aquaculture of invasive and non-native species worth the risk?

Following a recent report from the FAO on the threats posed by the production of invasive (potentially non-native) species in aquaculture, Gregg Yan and Jonah van Beijnen argue that a number of measures are needed to steer the global aquaculture sector away from this potential ecological catastrophe. Though now farmed worldwide, the most popular livestock all came from particular places. Sheep were first domesticated in the mountains of Iraq 11,000 years ago, pigs were first farmed in both China and Turkey 9,000 years ago, while wild Asian junglefowl were selectively bred to become chickens 1,000 years later.

The same rings true for many farmed fish: tilapia originally hailed from the creeks and lakes of Northeast Africa and the Middle East, most carps originate from the lakes of Asia, and Atlantic salmon were originally confined to the cool waters of the North Atlantic and the rivers that flow into it.

The systematic large-scale farming of seafood has many advantages. With the biology, husbandry, production and processing methods for most species being well-known and optimised over the years, potential guesswork has been eliminated, and production volumes have become stable, thereby improving both profitability for farmers and food security for the global population.

One major drawback is that foreign species can escape and take hold in many areas. Tilapia, for instance, are cultured in 85 countries, but are prone to escaping their pens and ponds.

The same qualities that have made them ideal candidates for farming – hardiness, adaptability and fecundity – means they can out compete many native fish. Tilapia are voracious and continually eat native plants, invertebrates and fish.

They also dig up the substrate, creating turbid water that obscures the light needed by many plants and animals to thrive. Some strains of tilapia can even survive in marine environments, establishing themselves along coastlines.

Invasive lionfish have reached the Mediterranean. Luckily they’re tasty venomous, highly opportunistic predators which spread rapidly and uncontrollably. The only solution found so far is the frying pan ran headlines in June this year, while marine biologists mumbled: “they’re venomous, not poisonous”.

Irrespective of their palatability (they’re actually delicious), lionfish have reached the Mediterranean, and the fears of conservationists and fishermen alike are set to come true. The fish, a highly opportunistic predator, is set to further impact an already threatened ecology, replicating the rapid spread of their cousins across the eastern Atlantic, from the Carolinas to Venezuela. Some would argue that this is not news, with sightings of the fish reported since the 1990s. However, recent observations around Cyprus have shown multiple individuals and breeding pairs. These are no longer isolated sightings.

Common lionfish and the similar red lionfish are now found in the eastern Atlantic, far from their native Indo-Pacific. One suggested explanation is that when Hurricane Andrew made landfall in 1992, a beachside aquarium in Florida containing half a dozen fish was smashed. The tale goes that divers later saw the group, and thus the story became accepted. There is though, a credible account of a lionfish spotted in Floridian waters in 1985, well before the presumed ancestors of the “invasion” ever found freedom. Release from home aquaria is now accepted as at least one point of introduction, with genetic evidence supporting the “multiple release” theory, along with the fact that there are two similar but distinct species involved.

In the Indo-Pacific, lionfish are controlled by predators; groupers and, on occasion, sharks take them at various stages of their growth. Elsewhere, however, predators seem not to recognise them as prey and ignore them, allowing lionfish numbers to grow at a startling rate at the expense of local fish stocks.

The route lionfish have taken to the Med seems straightforward; they have simply colonised through the Suez Canal from the Red Sea, and can be added to the growing list of Lessepsian species (named after Guy de Lesseps, the French engineer who oversaw the construction of the Canal). Whether fish released from aquaria are also present in the Mediterranean is unclear, though as sea temperatures rise, the survival of tropical species released by accident or design is more likely.

Some authorities suggest the Med, a less uniform environment than the Caribbean, will be harder for the fish to colonise, but given the lionfish’s prodigious breeding rate (a female can produce two million eggs a year), it is impossible to rule out the possibility of colonisation from North Africa even to the cooler shores of Europe.

If the lionfish invasion across the Atlantic is anything to go by, their spread will be rapid and uncontrollable – and there isn’t a “magic bullet” that can remove the fish from across their new range. Time will tell, of course; we’ll know eventually whether native predators add lionfish to their diet. Meanwhile, more immediate methods are being employed by the diving community and are receiving some support from state and national agencies. Time will tell, of course; we’ll know eventually whether native predators add lionfish to their diet. Meanwhile, more immediate methods are being employed by the diving community and are receiving some support from state and national agencies. The Florida Fish and Wildlife Commission, for example, regularly sponsors and promotes the culls, derbies and hunts that are organised by dive centres and diving organisations. In other locales, where resources and government interest may be reduced, individual dive centres have decided to take their own action to protect the fish life on their local reefs. One day, we might see similar events in the Med, and possibly lionfish on the menu in Mediterranean restaurants, especially given that it’s a region where spearfishing is considered a sport.

Catching lionfish is not that hard with the correct gear and a little experience. Variations on the theme of harpoons and spear guns are used. Lionfish are poor swimmers and can usually be approached: they’re relying on their camouflage and spines to deter unwanted attention.

I photographed a hunting session in the Windward Islands, where divers used a multiple-barbed harpoon to spear the fish. Some hunters then use another harpoon, ensuring it dies quickly and to allow the diver to manipulate the fish. Even though the fish is dead, its venom is not and if the spines puncture flesh, the pressure causes venom to move from glands along the spine, via ducts, into the victim’s flesh. Some hunters remove the spines underwater; others trim the fish on land.

Lionfish envenomation has been described as excruciatingly painful, though deaths are rare. Being a complex protein the venom is rapidly denatured and victims are encouraged to apply heat to the affected area, whether via hot water or a hair drier. Needless to say, caution should be exercised as otherwise scalds and burns may be more problematic than the venom. Urine or vinegar will have no effect, other than to add further unpleasant memories.

Lionfish behaviour may be shifting though, especially where they are hunted. Anecdotal evidence from some regions suggests they are altering their behaviour to the times dive centres operate, or moving to deeper waters. In their native range, lionfish will sometimes use divers as cover when hunting, benefitting from the confusion created amongst smaller prey species.

Lionfish hunting will not offer a complete solution, as only a fraction of the world’s reefs are visited by divers, making eradication unlikely. The hope is that local fauna will adapt, though it’s a long shot, particularly in the Med, where overfishing has reduced the population of potential predators to negligible levels.

So far, the only tactic that has had any noticeable (if small) impact on local lionfish populations has been that of encouraging the catching them for human consumption. Though control efforts face that most tricksy of problems: public perception. There are many fishing communities that are convinced lionfish are poisonous, leaving far more ecologically valuable fish, such as grouper and parrotfish, still on the catch list. If the Med is to face a full-scale lionfish invasion, concerned fishing communities and restaurateurs need to be reminded that the fish are not ppoisaonous and encouraged to add it to their menus and catch lists.

Humans despise the lionfish: each one that finds itself in foreign waters has a bounty on its head, there’s a campaign on Twitter to #KillTheLionfish, and now the US government is publicly supporting the hunt. In January, the US National Oceanic and Atmospheric Administration (Noaa) launched the massive resource on lionfish research, monitoring, and ecology, where hunting and eating the fish is also encouraged—once its venomous spines have been removed. The website launch follows on from Noaa’s and the several hunting derbies it has organised in recent years to get people spearing, basting, and frying for conservation’s sake.

Because behind this massive governmental thumbs-up is the fact that invasive lionfish are upending ecosystems along the eastern US and Caribbean shores, where they were introduced from the Indo-Pacific via the aquarium trade a few decades ago. They breed voraciously and have an insatiable appetite for fish and crustaceans. 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.
Nothing is currently known of lionfish larval behaviour. 3.2. Continuous reproduction and high fecundity Lionfish spawn in pairs and females produce 10,000–40,000 eggs per spawning event (Morris, 2009), which is lower than the per-event fecundity of many native Caribbean mesopredators (Table 1) that have been classified as ecologically similar to lionfish on the basis of similarity of diet at comparable body sizes on reefs in The Bahamas (Albins, 2013; Green et al., 2012). However, egg maturation in lionfish is asynchronous (Morris et al., 2011a), hence females can release eggs nearly continuously when conditions are favourable. In North Carolina and The Bahamas, female lionfish are likely to spawn approximately every 4 days during the summer months, with less frequent spawning during the colder months (Morris, 2009). Spawning is likely to occur more frequently in the southern parts of the introduced range. The annual fecundity of an average female lionfish may exceed 2 million eggs (Morris, 2009), which would place lionfish near the top end of the annual fecundity ranges in Table 1, since the per-event fecundity for most of these native species also represents annual fecundity. 3.3. High survival of eggs and larvae? During each spawning event, female lionfish produce two buoy- ant masses of eggs embedded in a gelatinous matrix, which are fertilised externally by the male (Fishelson, 1975; Morris et al., 2011a). This reproductive strategy offers numerous potential advantages. The gelatinous matrix may entrap the sperm, poten- tially enhancing fertilisation by preventing sperm dilution (Morris et al., 2011a). This matrix is also thought to contain a chemical deterrent to predation (Moyer and Zaiser, 1981). In addition, buoy- ant egg masses and larvae may facilitate broad and rapid dispersal by temporarily keeping the eggs near the surface where wind-dri- ven currents are stronger than they are at depth (Betancur-R et al., 2011; Freshwater et al., 2009). 3.4. Post-settlement dispersal Although movement at the egg and larval stages undoubtedly contribute the most to the overall geographic spread of marine invasive species, movement by post-settlement individuals can also increase distribution range (Kinlan and Hastings, 2005). There is so far limited information on the movements of lionfish, although this is an active area of current research. The only study published to date suggests that relatively small lionfish occupy small home ranges and are highly sedentary: three-quarters of the small (625 cm TL) lionfish tagged along the shore of an estua- rine river in Florida had moved less than 10 m from their tagging locations after 30 days at liberty (Jud and Layman, 2012). Fewer than 5% of tagged fish had moved more than 100 m, and the longest movement recorded was 420 m in 67 days by a 126 mm (standard length) lionfish (Jud and Layman, 2012). However, this high degree of site fidelity is perhaps not charac- teristic of larger lionfish, and of lionfish living in less linear habi- tats. Ongoing studies in The Bahamas suggest that adult lionfish associated with coral reef patches regularly roam considerable dis- tances (>200 m) over sand between reefs, with occasional very long-distance (2 km) travels (authors’ unpublished data). It remains to be seen whether extensive movement after settlement occurring at the patch scale can explain some of the discrepancy between the expected rate of lionfish spread based on current-driven larval dispersal and the observed distribution at the regional scale (Freshwater et al., 2009).
Moreover, lionfish do not exhibit the common flight response of most Atlantic fishes to perceived threat, but instead adopt a bold behaviour, with a defensive head-down pose with dorsal spines pointed forward (Green et al., 2011; Whitfield et al., 2007). Captive juvenile lionfish are relatively invulnerable to predation by wild-caught Atlantic predators, even when these predators are starved (Morris, 2009; Raymond et al., unpublished data), although small lionfish have occasionally been found in the stomachs of large Caribbean groupers (Maljkovic´ et al.,2008). However, top predators in the region have declined substantially as a result of overexploitation (Baum et al., 2003; Pad-dack et al., 2009; Stallings, 2009). While there is some evidence that abundant large groupers in a protected area in The Bahamas may be able to inhibit the invasion at an incipient stage (e.g., Mumby et al., 2011), this phenomenon is not observed throughout the region (Hackerott et al., unpublished data), even in areas with high predator densities. Moreover, it is not clear whether the effect reported by Mumby et al. (2011) is due to actual predation by groupers or to risk of predation, which might change lionfish behaviour and interfere with fitness-related functions such as foraging (i.e.,behaviourally mediated indirect interactions, sensu Dill et al.,2003; see also Section 5.1). The physical and behavioural defenses that make lionfish unlikely targets for consumption by Caribbean predators might be expected to be less effective in the native range because of co-evolution. However, there is only one report of predation on lionfish in the native range (Bernadsky and Goulet,1991), although lionfish have been poorly studied throughout the Indo-Pacific region.
There is currently little information on the diseases and parasites of lionfish, either in the native or in the introduced range. A total of eight species of parasites (three monogenoids, two trematodes, one leech, one copepod and one myxozoan; reviewed by Bullard et al. (2011)) have been recorded from P. volitans and P.miles in their native range, while one generalist buccal leech (Ruiz-Carus et al., 2006) and one generalist gut fluke (Bullardet al., 2011) have so far been documented in the introduced range. The best evidence so far for enemy release has been the finding that lionfish in the invaded range have lower ectoparasite loads than those in their native range, although one group of generalist parasites (gnathiid isopods) infect lionfish at equally low rates in both ranges (Sikkel et al., unpublished data).

Ecological impacts: observed and anticipated

As a mesopredator, lionfish are potentially prey of larger native predators, predators of smaller native fishes and invertebrates, and competitors with native mesopredators. With this central ecological role, invasive lionfish may potentially have both direct and indirect effects on native ecosystems at a variety of levels, the possible mechanisms being both lethal and nonlethal. Given that lionfish consume a broad diversity of native reef fishes (Albins and Hixon, 2008; Morris and Akins, 2009; Muñoz et al., 2011), and feed in the wild at rates that are much higher than in captivity (Côté and Maljkovic´, 2010; Green et al., 2011), the potential for widespread effects on native coral reef communities is substantial. The strength of direct predatory interactions suggests that related indirect effects may also be considerable. Unfortunately, there have been no comparative studies of the ecological effects of lionfish in their native Indo-Pacific range, probably because they are usually uncommon there (Kulbicki et al., 2012).
5.1. Direct effects
Invasive lionfish can cause substantial declines in the abundance of native small reef fishes, including adults of small species (e.g., gobies) and recruits of larger species that would otherwise eventually outgrow lionfish (e.g., parrotfishes). Albins and Hixon(2008) demonstrated experimentally on small patch reefs in The Bahamas that a single lionfish can reduce the abundance of small native fish by nearly 80% in just 5 weeks. In a subsequent experiment on similar reefs, Albins (2013) documented a 94% decline in small fish abundance over 8 weeks, and Albins (unpublished data) showed that such reductions over longer periods eventually lead to local extinctions. Elsewhere in The Bahamas, Green et al.(2012) observed a 65% decline, on average, in prey fish biomass over 2 years following the invasion. These observed declines are consistent with those predicted by ecosystem simulation models (e.g., Arias-González et al., 2011). The severity of predation impacts is unlikely to be uniform across taxa. Green and Côté (unpublished data) found that small, non-cleaning fishes with shallow bodies. Comparison of prey fish species richness in the diets of invasive Indo-Pacific lionfish and native Caribbean mesopredators. The line shows the accumulation curve of prey species identified visually for a sample of 130 lionfish captured in The Bahamas. Labels show the number of prey species recorded through visual identification, and the number of specimens examined, for nine ecologically similar native reef fishes (data derived from Randall (1967)).
Beyond reductions in native prey density, a key question is whether predation by lionfish destabilizes or otherwise alters the population dynamics of native prey species. Proximally, the issue is whether mortality caused by lionfish is appreciably greater than that caused by native mesopredators (e.g., small groupers). The answer is yes. In two separate field experiments in The Bahamas, Al-bins (2013) showed that lionfish caused nearly three times the overall prey mortality caused by native coney grouper, and Pusacket al. (unpublished data) found that lionfish caused nearly twice the mortality of bridled goby (Coryphopterus glaucofraenum) compared to the native graysby grouper (C. cruentata). Ultimately, the issue is whether invasive lionfish destabilize mechanisms that naturally regulate the local population dynamics of native prey. Field experiments in The Bahamas conducted before the invasion had demonstrated that a variety of future lionfish prey underwent regulating density-dependent per capita mortality caused by native predators. These native prey included blue chromis (Chromiscyanea, Hixon and Carr, 1997), gobies (C. glaucofraenum: Forrester and Steele, 2000, 2004; Steele and Forrester, 2005; Gnatholepis thompsoni: Forrester et al., 2008), bicolor damselfish (Stegastes partitus, Anderson et al., 2007; Carr et al., 2002; Johnson, 2008; Hixonet al., 2012), and fairy basslet (Gramma loreto, Webster, 2003, 2004). Ingeman and Webster (unpublished data) provided evidence that the strength of density dependence in fairy basslet reality was not altered by lionfish predation because lionfish simply added density-independent mortality to the underlying density- dependent mortality caused by native predators. (That is, the slope of the density-dependent mortality curve was not altered, but the y-intercept increased significantly.) Nonetheless, the fact that some local populations of fairy basslet were pushed toward 100% mortality in the presence of lionfish is indicative of the danger posed by the additional mortality imposed by the invader. Indeed, on small patch reefs in The Bahamas, a single lionfish can reduce local prey richness by about 5 species of native fish in just 8 weeks (Albins, 2013). Thus, while predation by native mesopredators has been generally reduced in most of the invaded region due to over-exploitation (Paddack et al., 2009; Stallings, 2009), it is becoming clear that lionfish predation does not replace regulating density-dependent mortality in prey fishes formerly provided by native predators. In fact, the high mortality imposed by lionfish, whether density-dependent or not, is pushing prey populations toward extirpation. Given that lionfish are now ubiquitous across coral reefs in the region, mortality caused by lionfish predation may have serious effects on prey population persistence.
Besides consuming native prey, lionfish could conceivably also be prey of native predators, yet to date, there is no evidence that native predators (sharks, large groupers, etc.) consume substantial numbers of lionfish (see Section 4.3 above). High densities of grouper may nonetheless interfere behaviourally with the ability of lionfish to forage effectively. Pusack (unpublished data) demonstrated experimentally in The Bahamas that patch reefs with high densities of large Nassau grouper Epinephelus striatus, which do not eat and otherwise ignore new recruits of other species, had significantly greater recruitment of native fishes in the presence of lion fish than did nearby reefs with fewer groupers and the same number of lionfish.
Although invasive lionfish may be behaviourally displaced by large groupers, they may nonetheless compete effectively with smaller native predators. In a cross-factored field experiment in The Bahamas, Albins (2013) demonstrated that, on the same patch reefs starting at the same body size, lionfish grew six times as fast as native coney grouper. Time will tell whether competition between invasive lionfish and native mesopredators substantially alters the abundance of these species. In addition to competing for food, lionfish can potentially compete for shelter with native species. Henderson and Côté (unpublished data) found that the shelters used by lionfish and by commercially important Caribbean spiny lobster Panulirus argus differed in height above the substratum when the two species co-occurred but not when one of the species was absent from a site. Nevertheless, suitable shelters appeared abundant, suggesting that competition is probably weak if it does occur.
5.2. Indirect effects
Indirect effects occur when a strong interactor directly alters the abundance of another species, which in turn alters the abundance of a third species that interacts directly with the second species (but not directly with the strong interactor). As a strong predator and potential competitor, lionfish may indirectly affect native species that directly interact with the species they consume or otherwise displace. Albins and Hixon (2011) described a possible cascade of effects that could manifest if lionfish greatly decrease the density of herbivorous fishes. In response to reduced herbivory, macroalgae could potentially increase and overgrow corals, contributing to the degradation of reefs. Lesser and Slattery (2011) provided circumstantial evidence consistent with this possibility from deep reefs in The Bahamas.
Another possibility is that lionfish could consume or interfere with the activities of native cleaning gobies (Elacatinus spp.), there-by indirectly causing an increase in the ectoparasite loads of native
reef fishes. Côté and Maljkovic´ (2010) observed lionfish approaching and disrupting cleaning stations, including consumption of a facultative cleaner, the bluehead wrasse Thalassoma bifasciatum.
It is unknown whether such interactions substantially disrupt cleaning mutualism to a level that affects parasite loads.