Habitat associations and impacts on a juvenile fish host by a temperate gnathiid isopod.

The distribution and abundance of organisms is typically shaped by multiple biotic and abiotic processes. Micropredators are parasite-like organisms that are smaller than their hosts and/or prey and feed on multiple hosts during a given life stage. Unlike typical parasites, however, they spend much or most of their time free-living, associating only temporarily with hosts. In the ocean, micropredators can impact multiple fish species, and in particular can have significant lethal and sub-lethal effects on newly settled fish. Although gnathiid isopods are abundant and primary micropredators in coral reef ecosystems, their impacts are relatively unexplored within sub-tidal temperate rocky reefs. We investigated the distribution of juvenile gnathiid isopods along sub-tidal temperate rocky reefs and tested trap methodology. We also quantified both the sub-lethal and lethal impacts of feeding-stage juvenile gnathiid isopods on juvenile, post-settlement reef fish, Heterostichus rostratus (giant kelpfish). We were most interested in determining the relationship between gnathiid infestation level and fish swimming performance, in particular swimming metrics relevant to predator avoidance maneuvers. We found that Gnathia tridens was present in rocky reefs rather than embayments along the Southern California coastline and that within rocky reefs, gnathiids occurred in the highest densities in lighted traps. Surprisingly, we observed almost no influence of fish size or gnathiid sub-lethal infestation level on ambient or burst swimming performance metrics. However, burst duration was reduced by gnathiid infestation, which is important in predator avoidance. There were significant differences in survivorship among small fish compared to large fish as a result of gnathiid infestation. Larger fish survived higher numbers of gnathiids than smaller fish, indicating that parasite-induced mortality is greater for smaller fish. Investigations of the effects of micropredators on subsequent predator-mediated mortality, including the susceptibility of fishes and their individual responses to micropredators, can further contribute to our understanding of processes affecting recruitment in resident reef fish populations. Further research, especially within temperate sub-tidal ecosystems, is needed to understand and highlight the overlooked importance of micropredation in shaping fish populations within a reefscape.

Combined effects of flow speed and sub-lethal insecticide exposure on predator-prey interactions between the California killifish and an infaunal polychaete.

Hydrodynamics and pollution affect estuarine populations, but their ecological effects have rarely been studied in combination. We conducted two laboratory experiments to quantify whether predator-prey interactions between California killifish, Fundulus parvipinnis, and the polychaete Polydora cornuta vary with flow speed and chlorpyrifos exposure. In one experiment, only F. parvipinnis was exposed to chlorpyrifos; in the other, only P. cornuta was exposed. The flume included a 300-cm2 area of sediment with 24 P. cornuta in a central patch (98 cm2). We videotaped groups of three killifish for 50 min at one of four flow speeds (6, 9, 12, or 15 cm/s) and recorded the proportion of bites directed at the prey patch. Unexposed killifish directed 70% of their bites at the prey patch at 6 cm/s, and prey-patch selection decreased as flow increased. Killifish exposed to chlorpyrifos directed 41% of their bites at the prey patch at 6 cm/s with reduced prey-patch selection relative to unexposed fish at 9 and 12 cm/s. At 15 cm/s, both exposed and unexposed fish displayed non-selective biting. Worms were videotaped to quantify their deposit- and suspension-feeding activities. Exposing worms to chlorpyrifos reduced total feeding activity by ~30%. Suspension feeding was more common at faster flow speeds, but the time worms spent suspension feeding relative to deposit feeding was unaffected by chlorpyrifos. No behavioral changes were noted in either species when the other was exposed to chlorpyrifos. This study highlights how hydrodynamic conditions can alter the relative importance of a toxicant's effects on predator-prey interactions.

Fish predators reduce kelp frond loss via a trait-mediated trophic cascade.

Although trophic cascades were originally believed to be driven only by predators eating prey, there is mounting evidence that such cascades can be generated in large part via non-consumptive effects. This is especially important in cascades affecting habitat-forming foundation species that in turn, influence associated communities. Here, we use laboratory and field experiments to identify a trait-mediated indirect interaction between predators and an abundant kelp in a marine temperate reef system. Predation risk from a microcarnivorous fish, the señorita, suppressed grazing by the host-specific seaweed limpet, which in turn, influenced frond loss of the habitat-forming feather boa kelp. This trophic cascade was pronounced because minor amounts of limpet grazing decreased the strength required to break kelp fronds. Cues from fish predators mitigated kelp loss by decreasing limpet grazing; we found 86% of this indirect interaction between predator and kelp was attributed to the non-consumptive effect in the laboratory and 56% when applying the same effect size calculations to the field. In field manipulations, the non-consumptive effect of señorita was as strong as the total predator effect and most importantly, as strong as the uncaged, "open" treatment with natural levels of predators. Our findings demonstrate that the mere presence of this fish reduces frond loss of the feather boa kelp through a trait-mediated trophic cascade. Moreover, despite large volumes of water, current flow, and wave energy, we clearly demonstrate a strong non-consumptive effect via an apparent chemical cue from señorita, suggesting that chemically mediated trait-driven cascades may be more prevalent in subtidal marine systems than we are currently aware.

Effects of a pesticide and a parasite on neurological, endocrine, and behavioral responses of an estuarine fish.

In coastal waters, pesticides and parasites are widespread stressors that may separately and interactively affect the physiology, behavior, and survival of resident organisms. We investigated the effects of the organophosphate pesticide chlorpyrifos and the trematode parasite Euhaplorchis californiensis on three important traits of California killifish (Fundulus parvipinnis): neurotransmitter activity, release of the stress hormone cortisol, and behavior. Killifish were collected from a population without E. californiensis, and then half of the fish were experimentally infected. Following a 30 day period for parasite maturation, infected and uninfected groups were exposed to four concentrations of chlorpyrifos (solvent control, 1-3ppb) prior to behavior trials to quantify activity, feeding behavior, and anti-predator responses. Water-borne cortisol release rates were measured non-invasively from each fish prior to infection, one-month post-infection, and following pesticide exposure. Killifish exposed to 3ppb chlorpyrifos exhibited a 74.6±6.8% and 60.5±8.3% reduction in brain and muscle acetylcholinesterase (AChE) activity relative to controls. The rate of cortisol release was suppressed by each chlorpyrifos level relative to controls. Killifish exposed to the medium (2ppb) and high (3ppb) pesticide concentrations exhibited reduced activity and a decrease in mean swimming speed following a simulated predator attack. Muscle AChE was positively related to swimming activity while brain AChE was positively related to foraging behavior. ​No effects of the parasite were observed, possibly because of low metacercariae densities achieved through controlled infections. We found that sublethal pesticide exposure has the potential to modify several organismal endpoints with consequences for reduced fitness, including neurological, endocrine, and behavioral responses in an ecologically abundant fish.

Intermittent Noise Induces Physiological Stress in a Coastal Marine Fish.

Anthropogenic noise in the ocean has increased substantially in recent decades, and motorized vessels produce what is likely the most common form of underwater noise pollution. Noise has the potential to induce physiological stress in marine fishes, which may have negative ecological consequences. In this study, physiological effects of increased noise (playback of boat noise recorded in the field) on a coastal marine fish (the giant kelpfish, Heterostichus rostratus) were investigated by measuring the stress responses (cortisol concentration) of fish to increased noise of various temporal dynamics and noise levels. Giant kelpfish exhibited acute stress responses when exposed to intermittent noise, but not to continuous noise or control conditions (playback of recorded natural ambient sound). These results suggest that variability in the acoustic environment may be more important than the period of noise exposure for inducing stress in a marine fish, and provide information regarding noise levels at which physiological responses occur.

Interactive effects of pesticide exposure and habitat structure on behavior and predation of a marine larval fish.

Coastal development has generated multiple stressors in marine and estuarine ecosystems, including habitat degradation and pollutant exposure, but the effects of these stressors on the ecology of fishes remain poorly understood. We studied the separate and combined effects of an acute 4 h sublethal exposure of the pyrethroid pesticide esfenvalerate and structural habitat complexity on behavior and predation risk of larval topsmelt (Atherinops affinis). Larvae were exposed to four nominal esfenvalerate concentrations (control, 0.12, 0.59, 1.18 µg/L), before placement into 12 L mesocosms with a three-spine stickleback (Gasterosteus aculeatus) predator. Five treatments of artificial eelgrass included a (1) uniform and (2) patchy distribution of eelgrass at a low density (500 shoots per m(2)), a (3) uniform and (4) patchy distribution of eelgrass at a high density (1,000 shoots per m(2)), and (5) the absence of eelgrass. The capture success of predators and aggregative behavior of prey were observed in each mesocosm for 10 min of each trial, and mortality of prey was recorded after 60 min. Exposure to esfenvalerate increased the proportion of larvae with swimming abnormalities. Surprisingly, prey mortality did not increase linearly with pesticide exposure but increased with habitat structure (density of eelgrass), which may have been a consequence of compensating predator behavior. The degree of prey aggregation decreased with both habitat structure and pesticide exposure, suggesting that anti-predator behaviors by prey may have been hampered by the interactive effects of both of these factors.

Top-down control of epifauna by fishes enhances seagrass production.

Predators can influence the structure and function of ecosystems by altering the composition or behavior of herbivore communities. Overexploitation of predators, therefore, may lead to habitat loss by altering important top-down interactions that facilitate habitat-forming species. In seagrass beds, top-down control of algal growth by mesograzers appears to facilitate seagrass production. The indirect consequences of higher-order trophic interactions, however, remain unclear. Although predators may limit the beneficial effects of algal mesograzers, it is also possible that they limit the abundance of invertebrates that consume and foul seagrasses. We used experimental enclosure and exclosure cages to explore the direct and indirect effects of microcarnivorous fishes on epifaunal invertebrates, epiphytic loads, and seagrass growth in a natural eelgrass (Zostera marina) bed in San Diego Bay, California, USA. Contrary to expectations, when fishes were excluded, invertebrate abundance increased by 300-1000%, fouling on eelgrass leaves increased by 600%, and eelgrass production declined by 50%. Despite high densities of predators in enclosures, subsequent effects did not differ from ambient conditions. When predators were excluded, however, abundances of epifauna (including tube-building crustaceans and an eelgrass-grazing limpet) increased dramatically, resulting in reduced seagrass production. Our results are supported by several studies of eelgrass communities in the northeastern Pacific, characterized by coastal upwelling, inverse estuaries, and a voracious seagrass-consuming limpet. These strong, positive, indirect effects of microcarnivores on seagrass production contrast with the beneficial mesograzer paradigm, highlighting the need for hypotheses to be tested across a variety of ecosystems with varying biophysical characteristics.

Functional responses and scaling in predator-prey interactions of marine fishes: contemporary issues and emerging concepts.

Predator-prey interactions are a primary structuring force vital to the resilience of marine communities and sustainability of the world's oceans. Human influences on marine ecosystems mediate changes in species interactions. This generality is evinced by the cascading effects of overharvesting top predators on the structure and function of marine ecosystems. It follows that ecological forecasting, ecosystem management, and marine spatial planning require a better understanding of food web relationships. Characterising and scaling predator-prey interactions for use in tactical and strategic tools (i.e. multi-species management and ecosystem models) are paramount in this effort. Here, we explore what issues are involved and must be considered to advance the use of predator-prey theory in the context of marine fisheries science. We address pertinent contemporary ecological issues including (1) the approaches and complexities of evaluating predator responses in marine systems; (2) the 'scaling up' of predator-prey interactions to the population, community, and ecosystem level; (3) the role of predator-prey theory in contemporary fisheries and ecosystem modelling approaches; and (4) directions for the future. Our intent is to point out needed research directions that will improve our understanding of predator-prey interactions in the context of the sustainable marine fisheries and ecosystem management.

Positive indirect effects of reef fishes on kelp performance: the importance of mesograzers.

It has been suggested that microcarnivorous reef fishes may play an important role in giant kelp forest communities by preventing infestations of mesograzers that could severely impact or potentially destroy recovering kelp forests after extreme disturbance events. However, these trophic linkages, specifically the direct and indirect effects of fishes on the biomass of mesograzers, grazing intensity, and the performance of giant kelp, have not been sufficiently quantified and evaluated as to their importance and in the absence of such disturbance events. We examined experimentally the effects of mesograzers on the growth and performance of giant kelp in the presence and absence of their fish predators near Santa Catalina Island, California (U.S.A.). Mesograzer biomass and grazing intensity were significantly higher when fishes were excluded from giant kelp, which in turn, lowered kelp performance. This pattern was consistent both on experimental plots of kelp as habitat isolates, and on a continuous reef. Moreover, the abundance of mesograzers was inversely related to the abundance of kelp perch among several kelp-forested reefs, suggesting that these effects can occur at larger spatial scales. Because of differences in the diet and behavior of two microcarnivorous fishes, the kelp perch and señorita, we conducted an experiment manipulating each species and its density independently to determine their separate effects on mesograzers and kelp performance. Concurrently we examined the growth and mortality of juvenile kelp. Grazing intensity decreased, estimates of kelp performance increased, and the growth of juvenile kelp increased with increasing densities of fish but with no detectable effects between fishes. Our results demonstrate that these microcarnivorous fishes have positive indirect effects on kelp performance by reducing mesograzer biomass and grazing intensity, and the early life stages of other fishes also may be important. More specifically, these fishes have a positive effect on the density of fronds of giant kelp that can result in greater recruitment success and the abundance of kelp-associated invertebrates and fishes. Indeed, this study suggests that mesograzers have the potential to be one of the most important herbivores in kelp forest ecosystems.

Biodiversity, population regulation, and the stability of coral-reef fish communities.

Unprecedented population declines and extinctions because of human activities, combined with a growing recognition that such losses affect the stability of ecosystems, underscore the need to better understand how populations persist naturally. We provide field experimental evidence that high biodiversity-in particular, the combined effects of predators and competitors-acts in a way that regulates the size of local fish populations within their coral-reef community. These results indicate that complex interactions among multiple species are necessary for the stability of a highly diverse community, and so forewarn that overexploiting such species may have cascading negative consequences for the entire system.