Scott A. Heppell

Prey Patch Patterns Predict Habitat Use by Top Marine Predators with Diverse Foraging Strategies

Spatial coherence between predators and prey has rarely been observed in pelagic marine ecosystems. We used measures of the environment, prey abundance, prey quality, and prey distribution to explain the observed distributions of three co-occurring predator species breeding on islands in the southeastern Bering Sea: black-legged kittiwakes (Rissa tridactyla), thick-billed murres (Uria lomvia), and northern fur seals (Callorhinus ursinus). Predictions of statistical models were tested using movement patterns obtained from satellite-tracked individual animals. With the most commonly used measures to quantify prey distributions - areal biomass, density, and numerical abundance - we were unable to find a spatial relationship between predators and their prey. We instead found that habitat use by all three predators was predicted most strongly by prey patch characteristics such as depth and local density within spatial aggregations. Additional prey patch characteristics and physical habitat also contributed significantly to characterizing predator patterns. Our results indicate that the small-scale prey patch characteristics are critical to how predators perceive the quality of their food supply and the mechanisms they use to exploit it, regardless of time of day, sampling year, or source colony. The three focal predator species had different constraints and employed different foraging strategies – a shallow diver that makes trips of moderate distance (kittiwakes), a deep diver that makes trip of short distances (murres), and a deep diver that makes extensive trips (fur seals). However, all three were similarly linked by patchiness of prey rather than by the distribution of overall biomass. This supports the hypothesis that patchiness may be critical for understanding predator-prey relationships in pelagic marine systems more generally.

Models To Compare Management Options For A Protogynous Fish

Populations of gag (Mycteroperca microlepis), a hermaphroditic grouper, have experienced a dramatic shift in sex ratio over the past 25 years due to a decline in older age classes. The highly female-skewed sex ratio can be predicted as a consequence of increased fishing mortality that truncates the age distribution, and raises some concern about the overall fitness of the population. Management efforts may need to be directed toward maintenance of sex ratio as well as stock size, with evaluations of recruitment based on sex ratio or male stock size in addition to the traditional female-based stock-recruitment relationship. We used two stochastic, age-structured models to heuristically compare the effects of reducing fishing mortality on different life history stages and the relative impact of reductions in fertilization rates that may occur with highly skewed sex ratios. Our response variables included population size, sex ratio, lost egg fertility, and female spawning stock biomass. Population growth rates were highest for scenarios that reduced mortality for female gag (nearshore closure), while improved sex ratios were obtained most quickly with spawning reserves. The effect of reduced fertility through sex ratio bias was generally low but depended on the management scenario employed. Our results demonstrate the utility of evaluation of fishery management scenarios through model analysis and simulation, the synergistic interaction of life history and response to changes in mortality rates, and the importance of defining management goals.

Active acoustic examination of the diving behavior of murres foraging on patchy prey

During the 2008 and 2009 breeding seasons of murres Uria spp., we combined visual observations of these predators with active acoustics (sonar), fish trawls, zooplankton net tows, and hydrographic measurements in the area surrounding breeding colonies in the southeastern Bering Sea. We acoustically detected thousands of bubble trails that were strongly correlated with the number of visually detected murres, providing a new tool for quantitatively studying the foraging ecology of diving birds. At the regional scale, the number of acoustically detected bubble trails, which served as a proxy for diving murre abundance, was related to the combined availability and vertical accessibility of squid, krill, and pollock. There were, however, no clear relationships at this scale between diving murres and any individual prey taxon, highlighting the importance of prey diversity to these animals. Individual krill patches targeted by murres had higher krill density and were located shallower than the mean depth of krill patches, but were similar in total krill abundance and overall size. The diving depth of murres within krill patches was highly correlated to the depth of the upper edge of these patches, whereas murres found outside of krill patches showed a depth distribution similar to that of juvenile pollock. Throughout the study area, murres showed strong diel patterns in their diving behavior in response to the diel migrations of their prey. These results suggest that murres select prey with specific patch characteristics implying effective information gathering about prey by murres. The high proportion of diving murres in aggregations and their consistent inter-individual spacing support the hypothesis that intraspecific local enhancement may facilitate foraging in these predators.

Enzyme‐Linked Immunosorbent Assay (ELISA) of Vitellogenin in Temperate Basses (Genus Morone): Plasma and In Vitro Analyses

Abstract Blood levels of the egg yolk precursor vitellogenin (VTG) can be used as a definitive marker for the onset and progress of maturation in female teleosts. In the present study, an enzyme-linked immunosorbent assay (ELISA) was developed to measure VTG in blood plasma from three species of temperate basses. The antigen capture, competitive ELISA is based on a rabbit antiserum raised against striped bass Morone saxatilis VTG and uses purified striped bass VTG as standard and in the final antigen capture step. The assay was validated for detecting VTG in the plasma of maturing female striped bass, white perch M. americana and white bass M. chrysops. Serial dilutions of blood plasma from vitellogenic females of all three species yielded VTG curves that paralleled the standard curve in the ELISA, whereas no cross reactivity was observed for plasma obtained from males of any Morone species. The working range of the ELISA was 33–1,118 ng/mL (90–10% of binding), and the intra- and interassay coefficients o...

Benthic Habitat Modification through Excavation by Red Grouper, Epinephelus morio, in the Northeastern Gulf of Mexico

Red grouper (Epinephelus morio) is an economically important species in the reef fish community of the south- eastern United States, and especially the Gulf of Mexico. It is relatively common in karst regions of the Gulf and is asso- ciated with low-relief rocky features devoid of overlying sediments. Working both inshore in Florida Bay, Florida (U.S.A.), and offshore in the Gulf of Mexico shelf-edge fishery reserves, Madison Swanson and Steamboat Lumps, we characterized red-grouper habitat and the associated faunal assemblages and demonstrated through a series of experiments that red grouper expose rocky habitat by excavating with their mouths and fanning with their fins to clear away surficial sediment, thereby providing habitat for themselves as well as other reef-dwelling organisms. They also maintain this habi- tat by periodically clearing away sediment and debris. Such maintenance provides a clean rocky substrate for the attach- ment of sessile invertebrates, thereby modifying habitat features to provide refuge for many other species of fish and mo- tile invertebrates. We demonstrated increased biodiversity and abundance associated with habitat structured by red grou- per, and we speculate here as to its fishery importance as habitat for other economically important species such as spiny lobster (Panulirus argus) and vermilion snapper (Rhomboplites aurorubens).

Population Structure and Phylogeography in Nassau Grouper (Epinephelus striatus), a Mass-Aggregating Marine Fish

To address patterns of genetic connectivity in a mass-aggregating marine fish, we analyzed genetic variation in mitochondrial DNA (mtDNA), microsatellites, and single nucleotide polymorphisms (SNPs) for Nassau grouper (Epinephelus striatus). We expected Nassau grouper to exhibit genetic differentiation among its subpopulations due to its reproductive behavior and retentive oceanographic conditions experienced across the Caribbean basin. All samples were genotyped for two mitochondrial markers and 9 microsatellite loci, and a subset of samples were genotyped for 4,234 SNPs. We found evidence of genetic differentiation in a Caribbean-wide study of this mass-aggregating marine fish using mtDNA (FST = 0.206, p<0.001), microsatellites (FST = 0.002, p = 0.004) and SNPs (FST = 0.002, p = 0.014), and identified three potential barriers to larval dispersal. Genetically isolated regions identified in our work mirror those seen for other invertebrate and fish species in the Caribbean basin. Oceanographic regimes in the Caribbean may largely explain patterns of genetic differentiation among Nassau grouper subpopulations. Regional patterns observed warrant standardization of fisheries management and conservation initiatives among countries within genetically isolated regions.

A physiological approach to quantifying thermal habitat quality for Redband Rainbow Trout (Oncorhynchus mykiss gairdneri) in the south Fork John Day River, Oregon

We examined tissue-specific levels of heat shock protein 70 (hsp70) and whole body lipid levels in juvenile redband trout (Oncorhynchus mykiss gairdneri) from the South Fork of the John Day River (SFJD), Oregon, with the goal of determining if these measures could be used as physiological indicators of thermal habitat quality for juvenile redband trout. Our objectives were to determine the hsp70 induction temperature in liver, fin, and white muscle tissue and characterize the relation between whole body lipids and hsp70 for fish in the SFJD. We found significant increases in hsp70 levels between 19 and 22°C in fin, liver, and white muscle tissue. Maximum hsp70 levels in liver, fin, and white muscle tissue occurred when mean weekly maximum temperatures (MWMT) exceeded 20–22°C. In general, the estimated hsp70 induction temperature for fin and white muscle tissue was higher than liver tissue. Whole body lipid levels began to decrease when MWMT exceeded 20.4°C. There was a significant interaction between temperature and hsp70 in fin and white muscle tissue, but not liver tissue. Collectively, these results suggest that increased hsp70 levels in juvenile redband trout are symptomatic of thermal stress, and that energy storage capacity decreases with this stress. The possible decrease in growth potential and fitness for thermally stressed individuals emphasizes the physiological justification for thermal management criteria in salmon-bearing streams.

Foraging responses of black-legged kittiwakes to prolonged food-shortages around colonies on the Bering Sea shelf.

We hypothesized that changes in southeastern Bering Sea foraging conditions for black-legged kittiwakes (Rissa tridactyla) have caused shifts in habitat use with direct implications for population trends. To test this, we compared at-sea distribution, breeding performance, and nutritional stress of kittiwakes in three years (2008–2010) at two sites in the Pribilof Islands, where the population has either declined (St. Paul) or remained stable (St. George). Foraging conditions were assessed from changes in (1) bird diets, (2) the biomass and distribution of juvenile pollock (Theragra chalcogramma) in 2008 and 2009, and (3) eddy kinetic energy (EKE; considered to be a proxy for oceanic prey availability). In years when biomass of juvenile pollock was low and patchily distributed in shelf regions, kittiwake diets included little or no neritic prey and a much higher occurrence of oceanic prey (e.g. myctophids). Birds from both islands foraged on the nearby shelves, or made substantially longer-distance trips overnight to the basin. Here, feeding was more nocturnal and crepuscular than on the shelf, and often occurred near anticyclonic, or inside cyclonic eddies. As expected from colony location, birds from St. Paul used neritic waters more frequently, whereas birds from St. George typically foraged in oceanic waters. Despite these distinctive foraging patterns, there were no significant differences between colonies in chick feeding rates or fledging success. High EKE in 2010 coincided with a 63% increase in use of the basin by birds from St. Paul compared with 2008 when EKE was low. Nonetheless, adult nutritional stress, which was relatively high across years at both colonies, peaked in birds from St. Paul in 2010. Diminishing food resources in nearby shelf habitats may have contributed to kittiwake population declines at St Paul, possibly driven by increased adult mortality or breeding desertion due to high foraging effort and nutritional stress.

Hepatic heat shock protein 70 and plasma cortisol levels in rainbow trout after tagging with a passive integrated transponder

Abstract This study examined the potentially stressful effects of tagging juvenile rainbow trout Oncorhynchus mykiss with passive integrated transponder (PIT) tags by measuring short-term (<120-h) changes in plasma concentrations of cortisol and hepatic heat shock protein 70 (hsp70). In a laboratory experiment, plasma cortisol levels were measured in fish before they were tagged (0 h) and at 2, 6, 24, and 120 h after being tagged. Hepatic hsp70 levels were measured at 0, 24, and 120 h. All results were compared with those for fish that were handled but not tagged. Plasma cortisol levels were significantly higher in both treatment groups (tagged and handled but not tagged) at 2 h than in the pretreatment groups (0 h). Plasma cortisol levels in the treatment groups returned to near pretreatment levels by 6 h. However, there was a significant difference in plasma cortisol levels between treatment groups at 6 h. There were no significant differences in hepatic hsp70 levels among the two treatment groups, and ...

Who's Your Momma? Recognizing Maternal Origin of Juvenile Steelhead Using Injections of Strontium Chloride to Create Transgenerational Marks

Abstract We sought to determine whether a strontium chloride injection could be used to create a transgenerational otolith mark in steelhead Oncorhynchus mykiss. Two strontium injection trials and a survey of strontium: calcium (Sr:Ca) ratios in juvenile steelhead from various steelhead hatcheries were conducted to test the feasibility of the technique. In both trials, progeny of fish injected with strontium had significantly higher Sr:Ca ratios in the primordial region of their otoliths, as measured by an electron wavelength dispersive microprobe. In trial 1, the 5,000-mg/L treatment level showed that 56.8% of the otoliths were correctly classified, 12.2% being misclassified as belonging to the 0-mg/L treatment. In trial 2, the 20,000-mg/L treatment level showed that 30.8% of the otoliths were correctly classified, 13.5% being misclassified as belonging to the 0-mg/L treatment. There were no differences in the fertilization rates of eggs or survival rates of fry between the treatment and control groups. ...