Established populations of non-natives may collapse without a clear causal mechanism. Hypothetically, fluctuations in habitat structural complexity may influence dynamics of invaders and the biotic resistance offered by predators. Herein I report observations of the collapse of a reproducing population of the non-native African jewelfish (Hemichromis letourneuxi) in a Florida lake concurrent with an unusual low-water period. I test the hypothesis that predation may have played a key role in the collapse using a combination of field surveys of habitat and fish abundance and predator-prey experiments. Habitat complexity was high before and after the low water period but virtually nonexistent during low water. The abundance of African jewelfish and native juvenile bluegill (Lepomis macrochirus) and eastern mosquitofish (Gambusia holbrooki) declined concurrently with decreasing complexity but the native species rebounded when lake levels increased. Large-bodied natives such as largemouth bass (Micropterus salmoides) and adult bluegill showed no pattern of fluctuation related to habitat complexity. African jewelfish survival was 1.6 times greater at high versus low complexity and over 7 times higher versus no complexity in the presence of largemouth bass. Conversely, eastern mosquitofish, a species that exerts strong effects on small-bodied fishes in structurally complex habitats had no effect on African jewelfish survival. Predation effects on susceptible non-natives should be considered as a potential control action. Population collapse is understudied but may provide insights into long-term dynamics of invaders and information useful for management of problematic species.

Population collapse, habitat complexity, drought, biotic resistance, predation, invasive, Cichlidae

Established populations of non-native species may decline or collapse without human intervention (Simberloff and Gibbons 2004). Some populations eventually rebound though others may remain at low levels or decline to extinction. Pathogens, small-population demographics, or stochastic events are frequent explanations for such fluctuations; however, the cause of the decline is unknown in many cases (Simberloff and Gibbons 2004). Boom-and-bust population cycles have been observed with non-native freshwater fishes in Florida, USA. Some declines are related to cold weather events impacting populations of non-natives of tropical origin (Snodgrass 1991, Trexler et al. 2000, Call et al. 2013). Nevertheless, reasons behind other examples are less clear (Loftus and Kushlan 1987, Fury and Morello 1994, Trexler et al. 2000, Shafland et al. 2008). Hypothetically a variety of abiotic and biotic factors might influence patterns of non-native fish abundance. Evaluating causes of observed population decline or collapse may provide insights into long-term dynamics of invaders and useful information for management of problematic species.

Predators, pathogens, or competitors can prevent establishment of non-natives, reduce their range or abundance, or eliminate local populations (Baltz and Moyle 1993, Byers 2002, Harvey et al. 2004). The influence of biotic resistance should vary spatially and temporally depending on changes in habitat features that mediate interactions among resident species and non-natives, potentially resulting in fluctuating abundance or population collapse of non-natives. Habitat structural complexity is an important factor influencing predator-prey dynamics and hence fish community structure (Savino and Stein 1982, MacRae and Jackson 2001). For example, large-bodied predatory fishes such as largemouth bass (Micropterus salmoides Lacepede) limit the use of open waters by small-bodied fishes (Werner and Hall 1988). Conversely, structurally complex habitat such as dense stands of aquatic macrophytes or other habitats that limit access of large-bodied species (e.g., shallows) reduce the effectiveness of predatory fishes and provide predation refuges for vulnerable species (Werner et al. 1983, Gotceitas and Colgan 1989, DeVries 1990). Differential vulnerability in structurally complex versus simple habitats may lead to the common observation of higher abundance of small-bodied fishes in complex habitats (Werner et al. 1978, Barrientos and Allen 2008). Decline in the density or area of structurally complex habitat generally results in reduced abundance of small-bodied fishes (Ware and Gasaway 1976, Bettoli et al. 1993, Colle and Shireman 1994, Sass et al. 2006) and should increase biotic resistance to susceptible invaders.

Little is known about the impact of biotic resistance on non-native freshwater fish abundance in Florida. Predation has been implicated anecdotally in the severe decline of only one reproducing non-native fish in the state, the silver dollar (Metynnis sp.), where elimination of dense stands of the submersed macrophyte Hydrilla verticilata was thought to have facilitated predation by largemouth bass (Shafland et al. 2008). Despite the lack of data on the influence of biotic resistance on field populations of non-native fishes in Florida, experimental evidence shows that predation and aggressive competition from natives offer resistance against establishment of many small-bodied (<150 mm total length [TL]) non-natives (Hill et al. 2011, Thompson et al. 2012). Such resistance is hypothesized to result in an overall lack of successful small-bodied invaders despite strong introduction pathways (Thompson et al. 2012). Additional investigation into the general importance of biotic resistance as an influence on invasion success is warranted.

Herein I report observations of the collapse of a reproducing population of the non-native African jewelfish (Hemichromis letourneuxi Sauvage) in a lake in west-central Florida concurrent with an unusual low-water period. A proposed mechanism of the collapse is predation facilitated by the loss of structurally complex refuge habitat. A combination of field observations and experiments were used to test this hypothesis. My objectives were to (1) document changes in habitat complexity in the littoral zone, (2) estimate the relative abundance of African jewelfish and select native fishes using visual sampling to document trends associated with changing habitat, and (3) experimentally investigate the hypothesis that predation may play a key role in the population collapse.

The collapse of African jewelfish abundance in Lake St. Clair was dramatic and rapid. African jewelfish were common in visual surveys for 4 years but were not observed for nearly 5 years following a major low-water event where virtually all structurally complex habitat was stranded above the water level. Abundance of native small-bodied fishes showed a similar though less dramatic pattern of decline as habitat complexity decreased. However, these species rapidly rebounded following a return of complex habitat. Larger-bodied natives showed little pattern relative to changing habitat complexity. The main predatory species in open waters, largemouth bass, was common throughout the study period. Predation experiments showed that the vulnerability of African jewelfish to a large-bodied, open-water predator increased with decreasing habitat complexity. Conversely, African jewelfish survival was not affected by a small-bodied native species within complex habitats. These results support the hypothesis that habitat-related changes in predation dynamics contributed to a marked decline in African jewelfish abundance in Lake St. Clair.

Prey persist in the environment because some portion of the population is invulnerable to predation at any one time (Matter and Mannan 2005). Morphological vulnerability of African jewelfish (Hill et al. 2006) suggests that this species must exploit behavioral or habitat refuges to escape predation. Structurally complex habitat limits access of large-bodied predators to smaller prey (Engle 1987), reduces the efficiency of predators (Savino and Stein 1982), and decreases the proportion of fish in predator’s diets (Bettolli et al. 1992). African jewelfish is highly associated with structurally-complex habitats such as aquatic macrophytes (Shafland 1996, Hill personal observations) and has declined dramatically in some south Florida canals concurrent with the near elimination of aquatic vegetation by water managers (Shafland et al. 2008, Hill unpublished data). African jewelfish in experimental tanks largely remained within the artificial vegetation and behind the barrier when these habitat features were available, an effective strategy to reduce vulnerability and increase survival. African jewelfish without effective cover were highly vulnerable to predation, suggesting the need for refuge habitat for persistence in the presence of open water predators. Normal water levels in Lake St. Clair provide considerable refuge habitat. Low water levels removed virtually all structurally complex habitat and exposed African jewelfish to open water predators.

Structurally complex habitat may not be sufficient refuge from predators for some fish species (MacRae and Jackson 2001). Research suggests that eastern mosquitofish harass and consume small-bodied non-native fishes and reduce refuge quality of shallows and structurally complex habitat via agonistic interactions (Hill et al. 2011, Thompson et al. 2012). Eastern mosquitofish had no effect on adult African jewelfish survival in experimental tanks and no observations suggest that eastern mosquitofish attack or displace African jewelfish from refuge habitat. These results imply little influence of eastern mosquitofish on biotic resistance against this non-native species, perhaps contributing to the nearly unique success among small-bodied fishes of African jewelfish as a widespread, established invader in Florida (see Thompson et al. 2012). Conversely, eastern mosquitofish and the highly similar western mosquitofish (Gambusia affinis Baird & Girard) frequently reduce the survival of larval or juvenile fishes by predation (Meffe 1985, Taylor et al. 2001, Thompson et al. 2012); eastern mosquitofish effects on early life stages of African jewelfish require additional investigation.

Unlike African jewelfish, small native fishes rapidly rebounded from their reduced abundance. Eastern mosquitofish were able to refuge from larger fishes during the low water period by exploiting the shallow lake margins (see DeVries 1990, Paterson and Whitfield 2000). This live-bearing fish has high reproductive output with sexual maturity at 1–2 months, gestation periods of 2–3 weeks, and brood sizes averaging up to 100 offspring (Pyke 2005). Reproduction is nearly year-round in Florida (Hill personal observations). Juvenile bluegills never disappeared entirely and were replenished by multiple yearly breeding cycles accomplished by relatively large, and therefore less vulnerable, adults which are capable of using open water habitats (Paukert and Willis 2002). Despite being robust and generally successful as an invader (Langston et al. 2010), the small and brightly colored adult African jewelfish were vulnerable to predators with the loss of refuge habitat and despite frequent spawning bouts and parental care their life history strategy apparently proved inadequate to maintain their abundance.

The results of the present study do not exclude other hypotheses that might partly explain the observed population collapse. Nevertheless, other factors potentially reducing African jewelfish abundance were not evident. Population size was fairly large and the species was distributed throughout the entire littoral zone where vegetation was present, suggesting that Allee effects and stochasticity of small population demographics were not important (Dennis 2002). Cold winter temperatures may eliminate this species from small, shallow aquaculture ponds in this region, though populations in nearby lakes of smaller surface area and lesser depth than Lake St. Clair persisted through a major cold event of the winter of 2009–2010 (Hill personal observations; see also Schofield et al. 2010). Moreover, African jewelfish were present in surveys done in early 2007 (late winter) prior to the extreme low-water conditions. Besides low water levels, no unusual water conditions were observed nor were fish kills of African jewelfish or any other species. African jewelfish is hardy and adaptable to a wide range of environmental conditions (Schofield et al. 2007, Langston et al. 2010) and occurs commonly in waters receiving road, residential, and agricultural runoff (Hill personal observations). Some unobserved disease might have affected the population, but, as recommended by Simberloff and Gibbons (2004), an unidentified pathogen is only an “explanation of last resort.”

Recovery of collapsed populations of non-natives is of as much interest as the collapse itself. Unfortunately, the origin of the African jewelfish observed in 2012 is unknown. A slow increase in abundance and spatial range of African jewelfish is evident since this time (present study, Hill personal observations). Re-colonization of Lake St. Clair from regional water bodies is unlikely because there are no direct water connections except for the overflow structure and pipe discharging into a small tributary stream. Access via this route is highly unlikely due to intermittent flow in both the discharge pipe and receiving stream, the large gap between lake levels and the overflow structure during the time period (usually 60–90 cm or more), and the large elevation difference between the structure and the outlet. Release by humans is a probable cause of re-establishment in the lake, especially at the public access area (e.g., Copp et al. 2005). Fishing for largemouth bass is common on the lake and live African jewelfish collected from other regional waters have been used as bait (illegally) in Lake St. Clair during the period between low water and their subsequent detection in surveys (2007–2012; Hill personal observations). It is also possible that some African jewelfish survived the low-water period and persisted at such low abundance that they were missed in surveys until 2012. Periodic monitoring would determine if African jewelfish returns to its former abundance or remains a minor component of the lake’s fish fauna. Similarly, surveys of regional waters with historic records would yield insights into the commonality of collapse in African jewelfish populations.

Management options may be few once non-native fishes establish (Kolar et al. 2010). For situations where non-natives are confined to small, closed water bodies, use of rotenone or other chemical treatments may be effective (e.g., Hill and Cichra 2005). Removals using active or passive capture techniques are seldom effective at eradication (Kolar et al. 2010, but see Hill and Sowards 2015). Predatory fishes are stocked in some situations to control non-native fishes (e.g., Shafland 1995), though eradication is not typical. Partial de-watering to strand structurally-complex refuge habitat or removal of aquatic vegetation could increase the effectiveness of resident or stocked predatory fishes in controlling or eliminating susceptible non-natives. For example, habitat simplification has been shown experimentally to increase the predatory effects of largemouth bass and other common predators (Savino and Stein 1982, Alexander et al. 2015). Elimination of aquatic vegetation may additionally remove preferred habitat and thus reduce abundance of vegetation-dependent species (e.g., Schofield and Nico 2007). Vegetation removal is a typical preliminary step to chemical application (Finlayson et al. 2010) and might be a sufficient action if the risk of the spread of the species is not unacceptable relative to the cost, collateral kill, and public relations challenge that may accompany fish toxicant application (Britton et al. 2011). The potential for effective control or eradication by predators also should be considered for water bodies where fish toxicant application is impractical. Use of manipulation of habitat complexity as a control measure for non-native fishes, just as with other control methods, would require a plan to monitor the water body for non-native persistence, taking into account the characteristics of the water body and the non-native species, and to reduce or eliminate re-introduction of the non-native from local dispersal or human activities.

Simberloff and Gibbons (2004) found little directed research investigating collapse of non-native species populations and concluded that this phenomenon is of little importance to invasion biology. However, since 2004 additional examples of population collapse have been observed in non-native taxa as diverse as ants (Cooling et al. 2012), crayfish (Sandstrom et al. 2014), and mammals (Sheehy and Lawton 2014). Few additional fish examples have been published but spontaneous collapse for unknown reasons has been noted for the widespread, invasive topmouth gudgeon (Pseudorasbora parva Temminck and Schlegel) in Europe (Copp et al. 2007). Predation by native species is seldom thought to be the cause of these newer examples (but see Sheehy and Lawton 2014). Boom-and-bust cycles and spontaneous population collapse for non-native fishes in Florida are mentioned in the literature but accounts are largely anecdotal (but see Harrison et al. 2013 and Boucek and Rehage 2014 for cold effects). Although cichlids are among the most numerous and successful established non-native fishes in Florida (Shafland et al. 2008), population abundance and range of several species have fluctuated considerably and some species have disappeared from the state, generally with no known cause (Shafland 1996, Shafland et al. 2008, USGS 2015). One of the most prevalent mechanisms to explain boom-and-bust cycles of native fishes is the effect of the interaction of environmental factors and life history traits on annual recruitment (e.g., Lobon-Cervia 2009, Matthews and Marsh-Matthews 2011). This is likely a rich area of future research investigating population fluctuations of Florida non-natives (e.g., the influence of major cold events; Schofield et al. 2010, Harrison et al. 2013, Boucek and Rehage 2014). As suggested by the present study, biotic resistance through predation likewise may prove an important mechanism. If population collapse is indeed as common, yet understudied, as suggested by a casual review of the literature for Florida, much additional research is warranted. A parallel can be drawn between population collapse and failed invasions, a more widely acknowledged yet similarly understudied phenomenon in the literature (Zenni and Nunez 2013). Greater attention to these occurrences can give insight into processes linked to invasion success, thus providing a more complete picture of the importance of population collapse and its potential use in risk analysis and non-native species management.

I thank Susan Hill and Katelyn Lawson, Emily Haug, and Jared Ritch (Tropical Aquaculture Laboratory, University of Florida) for assistance, Kelly Gestring and Bill Pouder (Florida Fish and Wildlife Conservation Commission) for information, Joel Trexler (Florida International University) and Pam Schofield (U.S. Geological Survey) for constructive comments, and the University of Florida’s Institute of Food and Agricultural Sciences and the Florida Fish and Wildlife Conservation Commission for funding. All applicable institutional guidelines for the care and use of animals were followed: UF IACUC #201004511.