Research Article |
Corresponding author: Jeffrey E. Hill ( jeffhill@ufl.edu ) Academic editor: Emili García-Berthou
© 2016 Jeffrey E. Hill.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hill JE (2016) Collapse of a reproducing population of non-native African jewelfish (Hemichromis letourneuxi) in a Florida lake. NeoBiota 29: 35-52. https://doi.org/10.3897/neobiota.29.7213
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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 (
Predators, pathogens, or competitors can prevent establishment of non-natives, reduce their range or abundance, or eliminate local populations (
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 (
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 small-bodied (75–100 mm TL) African jewelfish (Cichlidae) was first introduced near Miami, Florida in the early 1960s (
Observations were made from 2003 to 2013 at Lake St. Clair, Hillsborough County, Florida, a 23.5-ha suburban borrow lake within the Bullfrog Creek basin of the Tampa Bay watershed (lake center near 27°46'23"N, 82°21'57"W). The water was relatively clear, with mean Secchi disk depths of 203 cm (n = 3, SD = 3) in 2012. Substrates in the littoral zone consisted mostly of sand. The littoral zone had emergent vegetation (mostly Hydrocotyle sp. [in 2003 only], Panicum repens, Pontederia cordata, and Sagittaria lancifolia), with submersed vegetation intermixed (mostly Luziola fluitans, with small patches of Potamogeton illinoensis) and a few small areas with filamentous algae. Rising water levels occasionally inundated terrestrial vegetation. Most of the lake was deep (~4–6.5 m) outside the littoral zone with a steep drop-off and little habitat complexity. Soft sediments dominated the open water zone substrate. A water control structure in the north end of the lake maintains pool level and discharges via underground pipe to the Bullfrog Creek basin.
Water levels fluctuated more than 2 m during the study period. An unusual low-water period occurred in the lake for six to seven months in 2007 as a result of an extended drought during 2005–2007. Whole-lake visual surveys showed that the water level had dropped below the littoral zone such that almost no aquatic vegetation was submerged. An area of Scirpus sp. (~100 m long × 4 m wide) remained inundated in the northwest portion of the lake. Other structures such as docks were completely or nearly above the water level. Shorelines during low water were typically bare sand with a thin margin of shallow water rapidly dropping off into the deepest zone.
Quantitative field observations were done in three 25-m littoral zone transects along the southeastern (n = 60 samples; 2003 to 2012) and southern shoreline (two transects; n = 41 samples each; 2005–2012). Sample numbers by year were 2003 = 2, 2004 = 2, 2005 = 16, 2006 = 24, 2007 = 27, 2008 = 14, 2009 = 14, 2010 = 4, 2011 = 8, 2012 = 15, and 2013 = 16. The two southernmost transects included the public access area with the lake’s only boat ramp. The transect locations were fixed because of constraints regarding legal property access along the private lake shore. Habitat complexity, number of African jewelfish, abundance of other small fish, specifically juvenile bluegill (Lepomis macrochirus Rafinesque) and eastern mosquitofish (Gambusia holbrooki Girard), and abundance of larger fish, specifically adult bluegill (>100 mm TL) and largemouth bass were noted during each sample.
The complexity of aquatic macrophytes or inundated terrestrial vegetation in each transect was estimated using a ranked, categorical scale. Complexity was assigned a score of 0 if absent, 1 if sparse cover (<33% areal coverage), 2 if moderate cover (33–66% areal coverage), and 3 if dense cover (>66% areal coverage). These data estimate trends in refuge availability during the study.
Visual surveys for fish were made during daylight hours with the aid of polarized sunglasses and high water clarity. These surveys were done by slowly walking along the shoreline during daylight hours. Fish occasionally responded by moving away into vegetation or deeper water, but generally did not overtly react to the observer. Surveys were not conducted during the brief, cold winter periods (usually December through February) or during windy weather.
African jewelfish were counted. Though small-bodied, this species is active and brightly colored which facilitated observations. In practice, counting large numbers of small-bodied native fishes was difficult and inaccurate. Therefore, estimates of juvenile bluegill (<100 mm TL) and eastern mosquitofish abundance were made using a ranked, categorical scale. These species were scored according to the number observed, 0 if none were observed, 1 for 1–19, 2 for 20–99, and 3 for ≥100. Estimates of largemouth bass and adult bluegill (>100 mm TL) were made using a ranked, categorical scale where 0 was assigned if the species was absent, 1 if 1–5 individuals were observed, and 2 if more than 5 were observed. Category ranges were chosen based on preliminary observations in the case of small fishes and frequencies observed during the study for larger species. Largemouth bass was the main predatory species in the lake. Bluegill habitat use frequently differs with body size, with juveniles closely associated with structurally complex habitat in the presence of predatory fishes and less vulnerable adults capable of using more open water habitats (
Whole-lake presence/absence surveys were done for African jewelfish to determine the spatial distribution of the species during the study. These surveys included the entire littoral zone (~3,370 m of shoreline) and were made from a slow-moving kayak. Eight surveys were completed prior to the lowest water levels of 2007 (5 surveys in 2005, 2 in 2006, and 1 in early 2007). Seven surveys were done during the low water in 2007. The 25 post-drought surveys included 5 in 2008, 4 in 2009, 2 in 2010, 4 in 2011, 6 in 2012, and 4 in 2013. Two whole-lakeshore boat electrofishing surveys (Smith-Root GPP 9.0; Smith-Root, Vancouver, WA) were done during daylight hours in 2013 (July and August) to survey for African jewelfish and to attempt to collect additional fish species to those observed during visual sampling if present.
Two tank experiments were done to test the hypothesis that predation may have played a key role in the collapse of African jewelfish abundance in Lake St. Clair. The first experiment tested for differences in survival of African jewelfish under predation threat from largemouth bass across a range of habitat complexity (largemouth bass challenge). The other experiment tested the effects of eastern mosquitofish on African jewelfish (eastern mosquitofish challenge). Largemouth bass and eastern mosquitofish are common native species in Florida, are thought to resist invasion by non-native fishes (
The largemouth bass challenge had three treatments that varied by the strength of the predation refuge provided by habitat—(1) strong which simulated conditions prior to the low-water period when thick stands of submersed and emergent aquatic macrophytes were present, (2) weak which simulated a transitional period when most complex habitat was stranded but some vegetation remained underwater, and (3) none which simulated low-water conditions where virtually no complex habitat remained inundated. The strong refuge treatment had artificial vegetation (645 stems/m2) consisting of black plastic strips tied to a plastic lighting grate that covered 50% of the tank bottom (
The experiment was done in concrete tanks (221 cm × 79 cm × 58 cm; water depth 30 cm) on a re-circulating system in a greenhouse at the UF/IFAS Tropical Aquaculture Laboratory, Ruskin, Florida. Water parameters were: dissolved oxygen = > 8 ppm, temperature = 24–30 °C, pH = 7.9–8.1, total ammonia nitrogen < 1.0 ppm, nitrite < 0.02 ppm, total alkalinity = 188 ppm, and total hardness = 342 ppm. Four replicates of each treatment were randomly assigned to tanks in the system. Ten African jewelfish (mean TL ± SD = 64 ± 12 mm) were stocked into each tank and a single largemouth bass (205 ± 21 mm TL) was stocked 3 days later. The African jewelfish were morphologically vulnerable to the largemouth bass based on prey body depth and predator gape size (
The eastern mosquitofish challenge was done in oval polyethylene tanks with an area of about 1.2 m2 at the base and 1.4 m2 at the water surface (water depth 25 cm). Tanks were on a flow-through system receiving aerated well water. Water parameters were: dissolved oxygen = 7–8 ppm, temperature = 26–28 °C, pH = 8.0, unionized ammonia nitrogen undetectable, nitrite < 0.05 ppm, total alkalinity = 170 ppm, and total hardness = 459 ppm. Artificial vegetation (216 stems/m2) was centrally located to cover 49% of the tank bottom (
Habitat complexity within the littoral zone was high before and after the low water period and was low during the drought (Fig.
Trends in habitat complexity and fish abundance in Lake St. Clair. Abundance (± SE) of a African jewelfish (circles), b juvenile bluegill (circles) and eastern mosquitofish (triangles), and c adult bluegill (circles) and largemouth bass (triangles) in visual transects across years in Lake St. Clair, Florida. Scales for fish abundance vary by panel. Mean habitat complexity (± SE; bars) across years is on the secondary y-axis (0 = absent, 1 = <33% coverage, 2 = 33–66% coverage, and 3 = >66% coverage). African jewelfish abundance is number per transect. Abundance for juvenile bluegill and eastern mosquitofish is on a categorical scale (0 = absent, 1 = 1–19, 2 = 20–99, and 3 = 100 or more observed per transect). Abundance for adult bluegill and largemouth bass is on a categorical scale (0 = absent, 1 = 1–5, and 2 = 6 or more observed per transect)
African jewelfish were observed in quantitative samples each year from 2003 until the low-water period of 2007 (Fig.
Abundance of small-bodied native fishes declined substantially during the low water period but rebounded quickly following increases in water levels and habitat complexity (Fig.
Whole lake presence/absence surveys revealed African jewelfish throughout the littoral zone prior to the drought, but none were observed post-drought until 2012. Presence of small numbers of African jewelfish was noted in the south and southeast portions of the lake in five of six surveys in 2012 and in the south, southeast, and southwest portions in all surveys in 2013. No African jewelfish were noted in other sections of the lake post-drought. Native bluegill, eastern mosquitofish, and largemouth bass were noted in all sections of the lake in all surveys.
Native fishes observed during this study, in relative order of abundance, were eastern mosquitofish, bluegill, largemouth bass, channel catfish (Ictalurus punctatus Rafinesque), golden shiner (Notemigonus crysoluecas Mitchill), warmouth (Lepomis gulosus Cuvier), black crappie (Pomoxis nigromaculatus Lesueur), and golden topminnow (Fundulus chrysotus Gunther). Non-native fishes besides African jewelfish were not observed during visual sampling but walking catfish (Clarias batrachus Linnaeus; n = 2) and Asian swamp eel (Monopterus albus Zuiew; n = 1) were collected by boat electrofishing in 2013. Of these species, channel catfish likely exerted considerable predation pressures on small fishes during the low water period (Hill personal observations) but was uncommon in surveys. Channel catfish individuals were frequently observed near docks and along shorelines when lake residents provided feed and were common in angler catches (Hill personal observations).
African jewelfish survival varied with habitat in the largemouth bass challenge and positively correlated with habitat complexity (F2,11 = 27.93, P = 0.0001; Fig.
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 (
Structurally complex habitat may not be sufficient refuge from predators for some fish species (
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
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 (
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.,
Management options may be few once non-native fishes establish (
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.