Mark A. Steele

Recent Region-wide Declines in Caribbean Reef Fish Abundance

Profound ecological changes are occurring on coral reefs throughout the tropics, with marked coral cover losses and concomitant algal increases, particularly in the Caribbean region. Historical declines in the abundance of large Caribbean reef fishes likely reflect centuries of overexploitation. However, effects of drastic recent degradation of reef habitats on reef fish assemblages have yet to be established. By using meta-analysis, we analyzed time series of reef fish density obtained from 48 studies that include 318 reefs across the Caribbean and span the time period 1955-2007. Our analyses show that overall reef fish density has been declining significantly for more than a decade, at rates that are consistent across all subregions of the Caribbean basin (2.7% to 6.0% loss per year) and in three of six trophic groups. Changes in fish density over the past half-century are modest relative to concurrent changes in benthic cover on Caribbean reefs. However, the recent significant decline in overall fish abundance and its consistency across several trophic groups and among both fished and nonfished species indicate that Caribbean fishes have begun to respond negatively to habitat degradation.

PREDATORS, PREY REFUGES, AND THE SPATIAL SCALING OF DENSITY-DEPENDENT PREY MORTALITY

We tested the biological cause of density-dependent mortality in the bridled goby (Coryphopterus glaucofraenum), a small coral reef fish, and evaluated whether this knowledge allowed us to detect density dependence at different spatial scales in natural habitats. To identify the biological cause of density dependence, we manipulated both population density and the availability of shelter (crevices used as refuges from predators) in small plots of continuous reef. We detected strong density-dependent mortality in plots with few refuges, but mortality was density independent in plots with abundant refuges, indicating that limited shelter causes density dependence. Predator density was unrelated to the density of gobies and refuges, suggesting that predators displayed a type III functional response in patches with few refuges. In a second experiment, we manipulated goby density within replicate plots of three sizes (4, 16, and 64 m2) that varied naturally in the availability of refuges. If refuge availability was ignored, mortality appeared to be density independent at all scales. If, however, plots were grouped by refuge availability, mortality was density dependent in plots with few refuges, but low and density independent in plots with many refuges at all spatial scales. Understanding the mechanism of density dependence (refuge shortage) was thus required to measure the strength of density dependence in natural, spatially variable, habitat. We suggest that density dependence was detectable in plots of different sizes because the relationships between the densities of gobies, refuges, and goby predators were similar across the spatial scales we studied. Our work demonstrates that identifying the biological interactions that cause density dependence, and characterizing the spatial domains at which those interactions operate, will be important to accurately assess the effects of density dependence on population dynamics.

Spatio-temporal and interspecific variation in otolith trace-elemental fingerprints in a temperate estuarine fish assemblage

Abstract We tested whether estuarine fishes have site-specific differences in the concentrations of trace elements in their otoliths that can be used as ‘fingerprints’ to identify them to their estuary of origin. To evaluate the robustness of this approach, we tested whether elemental fingerprints were consistent among individuals of five species that were collected in 1996 from three temperate estuaries in southern California. We also tested whether elemental fingerprints were consistent between spring and autumn 1996 for three species in one of the sites, Carpinteria Marsh. The species evaluated comprised a mid-water-dwelling smelt ( Atherinops affinis ), two benthic gobies ( Clevelandia ios and Ilypnus gilberti ), and two flatfish ( Paralichthys californicus and Hypsopsetta guttulata ). The concentrations of six elements (Mn, Cu, Zn, Sr, Ba, and Pb) were determined in the otoliths using inductively coupled plasma-mass spectrometry (ICP-MS). Within estuaries, the five species exhibited strong variation in elemental concentration, indicating substantial interspecific differences in otolith environmental history. When the five fish species were considered separately, multivariate (MANOVA) and univariate (ANOVA) analyses of variance indicated that the elemental composition of otoliths differed significantly among the estuaries in four of the five species. Based on linear discriminant function analyses (DFA), differences were strong enough that trace element composition could be used to accurately assign fish to their site of origin [mean (range): 93.5% (74–100%)]. However, elemental signatures within Carpinteria Marsh were not consistent between spring and autumn 1996, and this was reflected in a substantial reduction in the accuracy of assigning fish to their true site of origin. When we compared site differences between fish species (site×species interactions), the elemental fingerprints were most similar between closely related species (e.g. the two gobies and the two flatfish) and most dissimilar between distantly related species, both phylogenetically and ecologically. Among the six elements analyzed, Sr and Ba exhibited the most inconsistent pattern among species, with significant differences in 80 and 70% of the pairwise species comparisons, respectively. The remaining four elements showed ≥70% consistency in the pattern of variation among sites for the different species. Thus, while otolith elemental fingerprinting can be a useful tool for inferring estuarine residency, such fingerprints may be temporally variable and species specific.

Effects of subcutaneous microtags on the growth, survival, and vulnerability to predation of small reef fishes

Marking reef fish with small, subcutaneous tags has proven to be a useful technique in ecological studies in both temperate and tropical systems. However, such tags may have adverse impacts on tagged individuals, possibly biasing estimates of demographic rates. We used field experiments on natural and artificial patch reefs to test for effects of subcutaneous acrylic paint and visual implant (VI) tags on the growth and mortality of the tropical goby Coryphopterus glaucofraenum (Gill). Growth of small ( ∼35 mm TL) fish was unaffected by tagging method. Neither acrylic paint, nor VI tags, influenced the mortality of C. glaucofraenum. We also conducted experiments in large outdoor tanks to test whether visual implant fluorescent elastomer (VIE) tags increased the susceptibility to predation of two temperate gobies, Coryphopterus nicholsii (Bean) and Lythrypnus dalli (Gilbert). For both goby species, tagged fish were no more susceptible to predatory kelp bass, Paralabrax clathratus (Girard) than untagged fish. Overall, with the exception of the slight reduction in growth of small C. glaucofraenum caused by acrylic paint tags, our results indicate that internal microtags can provide an effective means of marking small reef fish without introducing significant artifacts.

Effects of shelter and predators on reef fishes

Abstract The abundance of reef fishes is often influenced by the availability of potential shelter sites. The most prevalent hypothesis explaining this relationship between fish density and shelter is that post-settlement predation causes greater mortality in areas with little shelter vs. areas with abundant shelter. This hypothesis was tested with a set of field experiments, in which the availability of shelter and exposure to predators were manipulated orthogonally. The effects of shelter and predators were measured for recruitment and survival of two temperate reef fishes: the bluebanded goby ( Lythrypnus dalli Gilbert) and the blackeye goby ( Coryphopterus nicholsii Bean). Shelter was manipulated by creating isolated 1-m 2 reefs that were composed of three densities of rocks (16, 32 and 64 rocks/m 2 ), which both species of goby used for shelter. A preliminary set of experiments done on reefs exposed to predators revealed that recruitment and survival of both fishes were positively affected by the density of rocks. The main set of experiments revealed the proximate causes of these effects of shelter. Replicate reefs of all three shelter treatments were either kept free of predators (enclosed in predator-exclosure cages) or exposed to predators (enclosed in partial cages). In Coryphopterus , survival and recruitment varied among shelter treatments on reefs exposed to predators, but not on reefs free of predators. This result indicates that shelter influenced the density of Coryphopterus by altering the impact of predators, thus supporting the prevailing hypothesis. In contrast, the effects of shelter on Lythrypnus were not caused solely by altering the impact of predation: survival and recruitment both varied among shelter treatments even when predators were absent. For survival of Lythrypnus , differences among shelter treatments were larger on reefs exposed to predators than on reefs free of predators, indicating that shelter did also modify the impact of predation. However, recruitment of Lythrypnus was affected similarly by shelter treatments regardless of whether predators were present or absent. Therefore, the effects of shelter were not caused by altering the impact of predators, and instead, it appeared that recruits responded directly to the abundance of shelter. These results indicate that for some reef fishes, positive relationships between abundance and shelter may not be caused by lower rates of predation in areas with abundant shelter. Instead, such relationships between abundance and shelter may be driven by prey preferences (exerted at or after the time of settlement) for areas with abundant shelter, or by use of shelter sites for purposes other than refuge from predators. Therefore, in the absence of any other evidence supporting a role of predation, positive relationships between the density of reef fishes and the abundance of shelter should not be construed as proof of the importance of predation in determining the abundance of reef fishes.

EARLY POSTSETTLEMENT PREDATION ON THREE REEF FISHES: EFFECTS ON SPATIAL PATTERNS OF RECRUITMENT

Marine organisms suffer extensive mortality just after settling from the plankton, yet, little is known about the role that predators play in causing this mortality. We estimated the rates of predation in the first 24 h, and the first week, after settlement in three species of reef fish. To estimate these rates we compared the accumulation of recent settlers on plots from which predators were excluded (by caging) to settlement on unmanipulated control plots. The magnitude of predation varied greatly among our three focal species, even though they are ecologically similar (all are small gobies that inhabit the reef/sand interface). Within 24 h of settlement, predators apparently killed 92% of settled blackeye gobies, 26% of bridled gobies, and 6% of goldspot gobies. Within a week, predation had significantly reduced recruitment of all three species and was the main cause of death during this period. We also tested whether predation on new settlers affected spatial patterns of abundance at two scales. At sm...

Population regulation by post-settlement mortality in two temperate reef fishes

Abstract Input of individuals dispersing into open populations can be highly variable, yet the consequences of such variation for subsequent population densities are not well understood. I explored the influence of variable input (”supply”) on subsequent densities of juveniles and adults in open local populations of two temperate reef fishes, the bluebanded goby (Lythrypnus dalli) and the blackeye goby (Coryphopterus nicholsii). Variable recruitment was simulated by stocking a natural range of densities of young fishes on replicate patch reefs. Density and mortality of the stocked cohorts were followed over time, until the fishes reached maturity. Over the first day of the experiments, mortality of both species was significantly density-dependent; however, there was still a very strong relationship between density on day 1 and density on day 0 (i.e., simulated recruitment was still an excellent predictor of population density). At this point in the study, the main effects of density-dependent mortality were to reduce mean densities and variation about the mean. Over the period from the start of the experiments until the time when maturity was reached by each species (about 1 and 3 months for Lythrypnus and Coryphopterus, respectively), mortality was strongly density-dependent. Such strong density-dependent mortality virtually eliminated any linear relationship between adult density and ”recruit” density. However, for both species, the relationship between these two variables was well fit by an asymptotic curve, with the asymptotic density of adults equal to c. 3/m2 for Coryphopterus, and c. 10/m2 for Lythrypnus. Natural recruitment (via settlement of larvae) to the reefs over the period of the study (9 months) was above the asymptotic densities of adults for the two species, even though the study did not encompass the periods of peak annual recruitment of either species. This suggests that adult populations of these two gobies may often be limited, and regulated, by post-settlement processes, rather than by input of settlers. Other studies have shown that mortality of the two species is density-independent, or only weakly density-dependent, on reefs from which predators have been excluded. Hence, it appears that predators cause density-dependent mortality in these fishes.

Effects of predators on reef fishes: separating cage artifacts from effects of predation

Abstract Predators are thought to play prominent roles in determining population abundance and dynamics of many species, but it is often difficult to document effects of predators in the field. For lack of any other effective means of manipulating predator densities, many studies use predator exclosures, however, the results of these studies are difficult to interpret because the exclosures may introduce artifacts that cannot be separated from predatory effects. Using a design common in tests of predatory effects, exclosure cages (− predators), “cage controls” = partial cages ( + predators), and no cages ( + predators), patterns of survival were found for two reef fishes that were consistent with both predator and cage effects. To separate cage artifacts from effects of predators, direct tests of cage effects in an environment free of predators were conducted, within a large predator exclosure. Cage artifacts had dramatic effects on one fish species but not the other. Moreover, the way the affected species responded to cages was exactly what would be expected if predators had strong negative effects on these fish: growth and survivorship were much lower on uncaged reefs than on caged reefs. To circumvent the cage effects, rather than compare uncaged reefs ( + predators) to reefs in exclosure cages (− predators), exclosures were compared to partial cages ( + predators). In the absence of predators, the partial cages did not differ from exclosure cages in their effects on the prey. Using the partial cages and exclosure cages in an area where predators were present, predator effects on the two fishes were tested. Survivorship of one species was greatly reduced by predators, but the other species was not affected. The lack of a predator effect on the one species was apparently an artifact of comparing completely caged reefs to partially caged reefs; another experiment documented strong predator effects on this species. Partial cages probably greatly reduced the ability of predators to consume the “unaffected” species. When cage artifacts affect prey, partial cages may be usefully employed to avoid confounding predator effects with cage effects at the cost of underestimating the magnitude of predator effects. Direct tests of cage effects are necessary to interpret the results of any study that uses cages to test for predatory effects.

THE RELATIVE IMPORTANCE OF PROCESSES AFFECTING RECRUITMENT OF TWO TEMPERATE REEF FISHES

Local population densities of most benthic marine organisms are determined by a variety of processes that act before, during, and after settlement of planktonic propagules to the benthos. Considerable disagreement exists over the relative contribution of each process to patterns of abundance. Using multifactorial experiments, I assessed the effects of resident conspecifics, potential interspecific competitors, predators, and reef location on patterns of recruitment of two temperate reef fishes. Recruitment of bluebanded gobies (Lythrypnus dalli) and blackeye gobies (Coryphopterus nicholsii) consistently increased with distance from a nearby large reef. Recruitment of Lythrypnus was enhanced by the presence of older resident conspecifics. I found no strong evidence of any competitive effects between the two species. Predators had a variety of important effects on the density of recruits. Recruitment of Lythrypnus was halved by predators; this was the result of direct and indirect effects of predators: in addition to directly reducing recruit density, predators also reduced recruitment indirectly by reducing the density of older residents to which recruits responded. I developed two related methods for quantifying the contributions of the direct and indirect components of the predator effect. The effect of predation was spatially variable for both species: the net effect of this variability was the elimination of recruitment patterns related to reef location. Hence, the effects of spatially variable input of recruits was dependent upon the presence of predators, and thereby, predation altered the relative importance of the other factors that affected recruitment of the gobies. I argue that a much broader understanding of the “relative importance” of multiple causal processes will be gained by striving to understand how the contribution of each process is modified by other processes than by attempting to quantify the “importance” of each process.

VARIATION IN THE PRESENCE AND CAUSE OF DENSITY-DEPENDENT MORTALITY IN THREE SPECIES OF REEF FISHES

Determining the mechanisms by which natural populations are regulated is a key issue in ecology. Identifying the biological causes of density dependence has, however, proved difficult in many systems. In this study we tested whether adults of three species of reef fish (all gobies) suffered density-dependent mortality, and whether the density-dependent component of mortality was caused by predation. We used field experiments to test for density dependence in each prey species, manipulating the presence of predators and prey density in a factorial design. Prey were stocked on replicate patches of reef constructed of natural materials, with each reef receiving a different density of gobies. Predatory fishes were excluded from half of the reefs using a combination of removals and exclusion cages. Survival of the first species, Lythrypnus dalli, was high and density-independent on reefs free of predators, but declined rapidly with increasing density on reefs to which predators had access. Density dependence in L. dalli was thus a result of mortality inflicted by predatory fishes. In the second species, Coryphopterus nicholsii, predators caused a large reduction in the survival in one experiment but had a negligible effect in a second experiment. More importantly, though, survival of C. nicholsii was always independent of its density, regardless of predator presence. In the final species, Coryphopterus glaucofraenum, two separate experiments showed that natural changes in adult abundance (experiment 1) and survival of stocked adults (experiment 2) were density-dependent regardless of predator presence. Both experiments thus indicated that the density-dependent component of loss in C. glaucofraenum was caused, at least in part, by an interaction other than predation. The presence, intensity, and biological cause of density-dependent survival were thus strikingly different for each of these three fishes, despite the fact that they are taxonomically closely related and ecologically similar. These findings suggest a need for further studies aimed at predicting under what circumstances different mechanisms of population regulation will operate.