Sally J. Holbrook

COMPETITION FOR SHELTER SPACE CAUSES DENSITY‐DEPENDENT PREDATION MORTALITY IN DAMSELFISHES

The long-standing interest in density dependence in demographic rates of organisms stems from its influence in bounding population fluctuations and in shaping spatial patterns of abundance. Despite growing evidence that early mortality of marine reef fishes can be density dependent and can involve predation, the underlying biological mech- anisms have not as yet been fully explored in any system. Here we examine the causes of density-dependent juvenile mortality for two tropical damselfishes, Dascyllus flavicaudus and D. trimaculatus. These species shelter in branching corals or anemones, and they feed on plankton above their microhabitats during the day. Field experiments confirmed that density-dependent juvenile mortality of both Dascyllus species arose from predation and that most of the density-dependent loss could be attributed to small-bodied, resident piscivores (e.g., sandperch, squirrelfish) rather than larger, tran- sient species (e.g., jacks). Over the diel cycle, mortality was strongly density dependent during the dark when damselfish were sheltering but not during daylight when fish were actively foraging. Infrared video recordings revealed the species of predators responsible for most losses and indicated that most predatory events occurred from late twilight to early night, when damselfishes were in shelters and not feeding. Individuals were most at risk when located near or just outside the perimeter of a shelter. The proportion of a cohort in the riskiest areas of a microhabitat increased with density. The cause of the increased fraction of individuals at risk with increasing density was intraspecific interactions among sheltering fish jostling for space in the safest regions; this resulted in the displacement of less aggressive individuals to riskier locations. Thus, density-dependent mortality in both damselfishes arose from interference competition for refuge space from crepuscular and nocturnal predators.

THE COMBINED EFFECTS OF PREDATION RISK AND FOOD REWARD ON PATCH SELECTION

Experiments were performed to examine the effects of predation risk on selection of food patches by a mobile forager, young black surfperch (Embiotocajacksoni). The goals were to investigate (1) how predation risk affected relative selectivity among patches that differed in density of food, and (2) whether the foragers response depended on how variations in food level and predation risk were encountered. In the experiments, density of food (crustaceans on algae) was manipulated among spatially uniform patches of a foliose alga. Safety of the forager was varied by manipulating the presence in patches of kelp bass (Paralabrax clathratus), a principal predator of young surfperch. Patch choice was determined for an array of situations where food and risk were varied separately and together in space and time. The response of foragers to variation in food level and risk depended upon the specific manner in which the factors were encountered. When patches with a high food level contained a predator, foragers shunned the risky food-rich areas for safe food-poor patches. When food was equal between safe and risky patches, the degree to which patches with a predator were avoided remained constant over a range of absolute food densities. By contrast, selectivity between patches of different food densities was dampened when all available patches contained a predator. Finally, predators enhanced relative selectivity for food-rich areas when foragers had simultaneous access to the complete combination of variation in risk and food level. Heightened selectivity in the presence of predators resulted from two hierarchical responses: foragers always took less risk to feed in the food-poor patch, and, when the difference in comparable value of available food patches was suffi- ciently great, they took more risk to eat where the density of food was higher. Overall, these results indicate that juvenile black surfperch possess an array of responses to food and predators, which together may act to minimize the sublethal effect of predators on feeding at a minimal increase in probability of death. Such plasticity may be a general characteristic of foragers that experience variation in food and risk at several spatial scales and temporal combinations.

Spatial patterns in abundance of a damselfish reflect availability of suitable habitat

Abstract For species with metapopulation structures, variation in abundance among patches can arise from variation in the input rate of colonists. For reef fishes, variability in larval supply frequently is invoked as a major determinant of spatial patterns. We examined the extent to which spatial variation in the amount of suitable habitat predicted variation in the abundance of the damselfish Dascyllus aruanus, an abundant planktivore that occupies live, branched coral throughout the Indo-Pacific. Reef surveys established that size, branching structure and location (proximity to sand) of the coral colonies together determined the ”suitability” of microhabitats for different ontogenetic stages of D. aruanus. Once these criteria were known, patterns of habitat use were quantified within lagoons of five Pacific islands. Availability of suitable habitat generally was an excellent predictor of density, and patterns were qualitatively consistent at several spatial scales, including among different lagoons on the same island, among different islands and between the central (French Polynesia and Rarotonga) and western (Great Barrier Reef, Australia) South Pacific. A field experiment that varied the amount of suitable coral among local plots indicated that habitat for settlers accounted for almost all of the spatial variation in the number of D. aruanus that settled at that location, suggesting that spatial patterns of abundance can be established at settlement without spatial variation in larval supply. Surveys of four other species of reef-associated fish revealed that a substantial fraction of their spatial variation in density also was explained by availability of suitable reef habitat, suggesting that habitat may be a prevalent determinant of spatial patterns. The results underscore the critical need to identify accurately the resource requirements of different species and life stages when evaluating causes of spatial variation in abundance of reef fishes.

CHANGES IN AN ASSEMBLAGE OF TEMPERATE REEF FISHES ASSOCIATED WITH A CLIMATE SHIFT

Substantial changes have occurred in assemblages of nearshore reef fishes in the Southern California Bight during the past two decades. At two sites off Los Angeles, California, species richness of reef fishes fell 15-25%, and composition shifted from dom- inance by northern to southern species. Additionally, by 1993, 95% of the fish species had declined in abundance by an average of 69%. Concurrent declines of similar magnitude were observed for several trophic levels of the benthic ecosystem farther north at Santa Cruz Island where populations of surfperches (Pisces: Embiotocidae), the standing stock of their crustacean prey, and the biomass of understory macroalgae all declined by -80%. Abundances of fishes fell because declining recruitment of age-0 fish was insufficient to compensate for losses of older age classes. Annual levels of recruitment of age-0 fishes at all reefs examined fell more than one order of magnitude over two decades and was correlated among years with a broad indicator of Bight-wide productivity, the biomass of macrozooplankton in the California Current. Lower productivity of the coastal marine ecosystem, associated with a climate regime shift in 1976-1977, likely caused large, but unforeseen, impacts on population abundances and trophic structure in nearshore benthic communities.

MORTALITY OF JUVENILE DAMSELFISH: IMPLICATIONS FOR ASSESSING PROCESSES THAT DETERMINE ABUNDANCE

We examined the effects of variation in intra- and intercohort density on the magnitude and form of per capita juvenile mortality rates of three species of damselfish (Dascyllus spp.) at Moorea, French Polynesia. Patterns of mortality over a 2-wk period were estimated from daily counts of new settlers and of the next older age class (<1 mo old) following a natural settlement pulse to standard amounts of suitable microhabitat. Two spatial scales were explored: among 11 lagoon sites dispersed evenly around the 60-km perimeter of the island and among microhabitats within a site. For each species at both spatial scales, per capita mortality rates of new settler cohorts increased monotonically with density, whereas those of the next older cohort were density independent. Intra- and especially intercohort processes induced density-dependent mortality in new settler cohorts. Despite experimental densities that were only 15–25% of ambient, ∼50% of the spatial variance in settler abundance was reduced by density-dependent mortality in 2 wk. The relative contributions of primary recruitment limitation and subsequent density-dependent loss in setting the average abundance of 2-wk-old recruits were estimated to be ∼70% and ∼12%, respectively. Our findings demonstrate that density-dependent mortality may only occur for a brief period immediately after settlement of at least some reef fishes and that its influence can be relatively large at comparatively low densities. These results have major implications for current assessments of the relative importance of the processes that drive abundance and dynamics of species with demographically open populations.

Patch selection by juvenile black surfperch (Embiotocidae) under variable risk: Interactive influence of food quality and structural complexity

Abstract The influence of risk on the selection of foraging patches by young-of-year black surfperch, Embiotoca jacksoni Agassiz, was investigated by laboratory and field experiments. These foragers harvest crustacean prey from a variety of benthic algal substrata. In field environments, patch types vary in two ways. First, substrata differ in structural complexity and probably afford different degrees of protection from predators. Second, substratum types vary in prey richness. There was no correlation between structural complexity and prey richness, and either or both factors could be a component of foraging patch value. Each patch is small and individual foragers are simultaneously confronted with arrays of patches encompassing the full range of variation in structure and prey richness. Furthermore, a major predator of young-of-year black surfperch, the kelp bass, Paralabrax clathratus (Girard), is patchily distributed in space and time. Thus similar arrays of patch types can be characterized by different levels of overall risk. Risk to foragers is dependent on light level as well as the presence and density of predators. The interplay between food quality and shelter potential in influencing patch choice was examined under different regimes of risk. Both laboratory and field experiments indicated patch preference was based primarily on food quality. However, the physical structure of a patch did become a component of patch choice as risk increased. The relative value of physical structure under high risk was dependent on the prey richness of a patch; food-poor substrata with high shelter potential remained unfavored even in situations of high risk.

Gape-limitation, foraging tactics and prey size selectivity of two microcarnivorous species of fish

SummaryPatterns of prey size selectivity were quantified in the field for two species of marine microcarnivorous fish, Embiotoca jacksoni and Embiotoca lateralis (Embiotocidae) to test Scott and Murdochs (1983) size spectrum hypothesis. Two mechanisms accounted for observed selectivity: the relative size of a fish in relation to its prey, and the type of foraging behavior used. Juvenile E. jacksoni were gape limited and newborn individuals achieved highest selectivity for the smallest prey size by using a visual picking foraging strategy. As young E. jacksoni grew, highest preference shifted to the next larger prey sizes. When E. jacksoni reached adulthood, the principal mode of foraging changed from visual picking to relatively indiscriminant winnowing behavior. The shift in foraging behavior by adults was accompanied by a decline in overall preference for prey size; sizes were taken nearly in proportion to their relative abundance. Adult E. lateralis retained a visual picking strategy and achieved highest selectivity for the largest class of prey. These differences in selectivity patterns by adult fish were not explained by gape-limination since adults of both species could ingest the largest prey items available to them. These results support Scott and Murdochs (1983) hypothesis that the qualitative pattern of size selectivity depends largely on the range of available prey sizes relative to that a predator can effectively harvest.

HABITAT‐LIMITED RECRUITMENT OF CORAL REEF DAMSELFISH

Spatial variation in abundance of reef fishes with dispersing larvae often has been attributed to variation in the supply of new colonists from the plankton, which we term “supply determination.” We conducted field experiments with three species of planktivorous damselfishes (Dascyllus flavicaudus, D. trimaculatus, and Amphiprion chrysopterus) to distinguish between the influence of supply determination and spatial variation in suitable microhabitat (“habitat determination”) on patterns of abundance, and to evaluate whether habitat became limited. In experiments where the abundance of initially unoccupied habitat suitable for these fishes was manipulated among a series of plots, colonization and population trajectories were followed for up to six years. Additional experiments explored the effect that the densities reached on colonization plots had on settlement. Colonization experiments revealed positive linear relationships between the time-averaged abundance of adults and of new colonists among experime...

Settlement and recruitment of three damselfish species: larval delivery and competition for shelter space

Abstract Spatial patterns of settlement and abundance of older life stages were examined for three species of damselfish in the genus Dascyllus by monitoring natural colonization of standard amounts of initially empty juvenile microhabitat (anemones for D. trimaculatus; branching coral for D. flavicaudus and D. aruanus) transplanted to a series of sites within lagoons of Moorea, French Polynesia. Large spatial differences in larval colonization were observed, which were temporally consistent but different among the species. At the whole-island scale, D. trimaculatus settled primarily on the northern shore, while settlement of the other two species was greatest at the southern end. The three species also showed different patterns of settlement within lagoons: D. aruanus settled mainly nearer to shore, D. flavicaudus primarily on offshore lagoon portions and D. trimaculatus colonized equally across the lagoons. Among sites around the island, the relative abundance of older juveniles after 10 months was a curvilinear function of the relative abundance of settlers for two species (D. trimaculatus and D. flavicaudus). There was no relationship between patterns of settlement and abundance of older juveniles for D. aruanus, although juvenile abundance was inversely related to that of juvenile D. flavicaudus. At the within-lagoon scale, settlement mirrored almost exactly the relative abundance of older lifestages of D. trimaculatus and D. flavicaudus, whereas there was just a qualitative match for D. aruanus. A competition experiment revealed that juvenile D. flavicaudus had a greater effect on population growth of D. aruanus than vice versa, and this mechanism helped explain why the modification of settlement patterns was greatest in D. aruanus. Interspecific variation in abundance of older stages was shaped to differing extents by both patterns of larval delivery and subsequent density-dependent processes involving competition for shelter space.

Resource overlap, prey dynamics, and the strength of competition

Patterns of resource use and the strength of interspecific competition were explored for two temperate marine reef fishes, black surfperch (Embiotoca jacksoni) and striped surfperch (E. lateralis). These species occupy a depth—related gradient in abundance of food (crustaceans) and preferred foraging microhabitats (species of foliose algae that contain food items). Field experiments revealed that the intensity of competition varied greatly along the resource gradient. At the shallow end of the gradient, which contains seasonally high food levels and large amounts of the most preferred foraging microhabitat (the red alga Gelidium), interspecific competition was intense during seasons when food was scarce. This was accompanied by low overlap in use of feeding microhabitats. We detected no competition in deep areas that lacked Gelidium. In this portion of the resource gradient, low overlap occurred because there was no preferred microhabitat that both fishes could share. Low overlap in the deep habitat was not a consequence of competition but rather of the slightly different foraging adaptations of each species. In the surfperch system, static, among—habitat patterns of resource overlap provided little insight into the existence or strength of competition. High overlap occurred when competition was dampened by abundant food (in the shallow zone during food—rich seasons). Low overlap was either associated with strong competition (during periods of relative scarcity of food in the shallow zone) or its absence (deep areas which lacked the shared, preferred microhabitat). Spatial and temporal variation in the strength of interspecific competition was better predicted by dynamic (seasonal) patterns of microhabitat overlap, but only when coupled with knowledge of food dynamics, foraging adaptations of the competitors, and availability of preferred shared microhabitat.