Kelly J. Benoit-Bird

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.

Cooperative prey herding by the pelagic dolphin, Stenella longirostris.

Sonar techniques were used to quantitatively observe foraging predators and their prey simultaneously in three dimensions. Spinner dolphins foraged at night in highly coordinated groups of 16-28 individuals using strict four-dimensional patterns to increase prey density by up to 200 times. Herding exploited the preys own avoidance behavior to achieve food densities not observed otherwise. Pairs of dolphins then took turns feeding within the aggregation that was created. Using a proxy estimate of feeding success, it is estimated that each dolphin working in concert has more access to prey than it would if feeding individually, despite the costs of participating in the group maneuvers, supporting the cooperation hypothesis. Evidence of a prey density threshold for feeding suggests that feedback from the environment may be enough to favor the evolution of cooperation. The remarkable degree of coordination shown by foraging spinner dolphins, the very strict geometry, tight timing, and orderly turn taking, indicates the advantage conferred by this strategy and the constraints placed upon it. The consistent appearance of this behavior suggests that it may be a critical strategy for energy acquisition by spinner dolphins in energy poor featureless environments in the tropical Pacific Ocean.

Target strength measurements of Hawaiian mesopelagic boundary community animals

A 200-kHz echosounder modified to digitize the envelope of the received echoes directly into a computer was used to measure the ex situ target strength (TS) of live animals from the Hawaiian mesopelagic boundary community as a function of animal size, tilt and roll angle, and biological classification. Dorsal aspect TS (in dB//1 m) at 200 kHz was related to the animal’s length: myctophid fish TS=20 log (standard length in cm)−58.8, r2=0.91, squid TS=18.8 log (mantle length in cm)−61.7, r2=0.81, shrimp TS=19.4 log (length in cm)−74.1, r2=0.83. Tilting the fish 5° and 10° changed the measured TS by up to 3.0 dB, decreasing TS as the fish was tilted forward and increasing TS as the fish was tilted backwards. In shrimp, forward tilt increased TS while backward tilt decreased TS by up to 3.3 dB. No consistent trend in squid TS change was observed with tilt angle. Roll angles of 5° and 10° increased the TS of all groups by up to 3.0 dB. Myctophid lateral aspect TS was consistently about 6 dB higher than the dor...

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.

Acoustic radiation from the head of echolocating harbor porpoises(Phocoena phocoena)

SUMMARY An experiment was conducted to investigate the sound pressure patterns on the melon of odontocetes by using four broadband hydrophones embedded in suction cups to measure echolocation signals on the surface of the forehead of two harbor porpoises (Phocoena phocoena). It has long been hypothesized that the special lipids found in the melon of odontocetes, and not in any other mammals, focus sounds produced in the nasal region that then propagate through the melon, producing a beam that is directional in both the horizontal and vertical planes. The results of our measurements supported the melon-focusing hypothesis, with the maximum click amplitude, representing the axis of the echolocation beam, located approximately 5.6-6.1 cm from the edge of the animals upper lip along the midline of the melon. The focusing is not sharp but is sufficient to produce a transmission beam of about 16°. Click amplitude dropped off rapidly at locations away from the location of site of maximum amplitude. Based on comparisons of forehead anatomy from similar sized porpoises, the beam axis coincided with a pathway extending from the phonic lips through the axis of the low-density/low sound velocity lipid core of the melon. The significant interaction between click number and hydrophone position suggests that the echolocation signals can take slightly different pathways through the melon, probably as a result of how the signals are launched by the production mechanism and the position of the acoustically reflective air sacs.

Modeling the detection range of fish by echolocating bottlenose dolphins and harbor porpoises

The target strength as a function of aspect angle were measured for four species of fish using dolphin-like and porpoise-like echolocation signals. The polar diagram of target strength values measured from an energy flux density perspective showed considerably less fluctuation with azimuth than would a pure tone pulse. Using detection range data obtained from dolphin and porpoise echolocation experiments, the detection ranges for the Atlantic cod by echolocating dolphins and porpoises were calculated for three aspect angles of the cod. Maximum detection ranges occurred when the fish was broadside to the odontocete and minimum detection ranges occurred when the cod was in the tail aspect. Maximum and minimum detection ranges for the bottlenose dolphin in a noise-limited environment was calculated to be 93 and 70 m, respectively. In a quiet environment, maximum and minimum detection ranges for the bottlenose dolphin were calculated to be 173 and 107 m, respectively. The detection ranges for the harbor porpoise in a quiet environment were calculated to be between 15 and 27 m. The primary reason for the large differences in detection ranges between both species was attributed to the 36 dB higher source level of the bottlenose dolphin echolocation signals.

Bottom-up regulation of a pelagic community through spatial aggregations

The importance of spatial pattern in ecosystems has long been recognized. However, incorporating patchiness into our understanding of forces regulating ecosystems has proved challenging. We used a combination of continuously sampling moored sensors, complemented by shipboard sampling, to measure the temporal variation, abundance and vertical distribution of four trophic levels in Hawaiis near shore pelagic ecosystem. Using an analysis approach from trophic dynamics, we found that the frequency and intensity of spatial aggregations—rather than total biomass—in each step of a food chain involving phytoplankton, copepods, mesopelagic micronekton and spinner dolphins (Stenella longirostris) were the most significant predictors of variation in adjacent trophic levels. Patches of organisms had impacts disproportionate to the biomass of organisms within them. Our results are in accordance with resource limitation—mediated by patch dynamics—regulating structure at each trophic step in this ecosystem, as well as the foraging behaviour of the top predator. Because of their high degree of heterogeneity, ecosystem-level effects of patchiness such as this may be common in many pelagic marine systems.

Controlled and in situ target strengths of the jumbo squid Dosidicus gigas and identification of potential acoustic scattering sources

This study presents the first target strength measurements of Dosidicus gigas, a large squid that is a key predator, a significant prey, and the target of an important fishery. Target strength of live, tethered squid was related to mantle length with values standardized to the length squared of -62.0, -67.4, -67.9, and -67.6 dB at 38, 70, 120, and 200 kHz, respectively. There were relatively small differences in target strength between dorsal and anterior aspects and none between live and freshly dead squid. Potential scattering mechanisms in squid have been long debated. Here, the reproductive organs had little effect on squid target strength. These data support the hypothesis that the pen may be an important source of squid acoustic scattering. The beak, eyes, and arms, probably via the sucker rings, also play a role in acoustic scattering though their effects were small and frequency specific. An unexpected source of scattering was the cranium of the squid which provided a target strength nearly as high as that of the entire squid though the mechanism remains unclear. Our in situ measurements of the target strength of free-swimming squid support the use of the values presented here in D. gigas assessment studies.

Broadband backscatter from individual Hawaiian mesopelagic boundary community animals with implications for spinner dolphin foraging

Broadband simulated dolphin echolocation signals were used to measure the ex situ backscatter properties of mesopelagic boundary community (MBC) in order to gain a better understanding of the echolocation process of spinner dolphins foraging on the MBC. Subjects were captured by trawling with a 2-m-opening Isaacs-Kidd Midwater Trawl. Backscatter measurements were conducted on the ship in a 2000 L seawater tank with the transducer placed on the bottom pointed upwards. Backscatter measurements were obtained in both the dorsal and lateral aspects for seven myctophids and only in the dorsal aspect for 16 more myctophids, six shrimps, and three squids. The echoes from the myctophids and shrimps usually had two highlights, one from the surface of the animal nearest the transducer and a second probably from the signal propagating through body of the subject and reflecting off the opposite surface of the animal. The squid echoes consisted mainly of a single highlight but sometimes had a low amplitude secondary highlight. The backscatter results were used to estimate the echolocation detection range for spinner dolphins foraging on the mesopelagic boundary community. The results were also compared with multi-frequency volume backscatter of the mesopelagic boundary community sound scattering layer.

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.