Resource Patchiness as a Resolution to the Food Paradox in the Sea.

AbstractAverage concentrations of biota in the ocean are low, presenting a critical problem for ocean consumers. High-resolution sampling, however, demonstrates that the ocean is peppered with narrow hot spots of organism activity. To determine whether these resource aggregations could provide a significant solution to the ocean's food paradox, a conceptual graphical model was developed that facilitates comparisons of the role of patchiness in predator-prey interactions across taxa, size scales, and ecosystems. The model predicts that predators are more reliant on aggregated resources for foraging success when the average concentrations of resources is low, the size discrepancy between predator and prey is great, the predator has a high metabolic rate, and/or the predator's foraging time is limited. Size structure differences between marine and terrestrial food webs and a vast disparity in the overall mean density of their resources lead to the conclusion that high-density aggregations of prey are much more important to the survival of oceanic predators than their terrestrial counterparts, shaping the foraging decisions that are available to an individual and setting the stage on which evolutionary pressures can act. Patches of plenty may be rare, but they play an outsized role in behavioral, ecological, and evolutionary processes, particularly in the sea.

Using individual-based bioenergetic models to predict the aggregate effects of disturbance on populations: A case study with beaked whales and Navy sonar.

Anthropogenic activities can lead to changes in animal behavior. Predicting population consequences of these behavioral changes requires integrating short-term individual responses into models that forecast population dynamics across multiple generations. This is especially challenging for long-lived animals, because of the different time scales involved. Beaked whales are a group of deep-diving odontocete whales that respond behaviorally when exposed to military mid-frequency active sonar (MFAS), but the effect of these nonlethal responses on beaked whale populations is unknown. Population consequences of aggregate exposure to MFAS was assessed for two beaked whale populations that are regularly present on U.S. Navy training ranges where MFAS is frequently used. Our approach integrates a wide range of data sources, including telemetry data, information on spatial variation in habitat quality, passive acoustic data on the temporal pattern of sonar use and its relationship to beaked whale foraging activity, into an individual-based model with a dynamic bioenergetic module that governs individual life history. The predicted effect of disturbance from MFAS on population abundance ranged between population extinction to a slight increase in population abundance. These effects were driven by the interaction between the temporal pattern of MFAS use, baseline movement patterns, the spatial distribution of prey, the nature of beaked whale behavioral response to MFAS and the top-down impact of whale foraging on prey abundance. Based on these findings, we provide recommendations for monitoring of marine mammal populations and highlight key uncertainties to help guide future directions for assessing population impacts of nonlethal disturbance for these and other long-lived animals.

Oceanic giants dance to atmospheric rhythms: Ephemeral wind-driven resource tracking by blue whales.

Trophic transfer of energy through marine food webs is strongly influenced by prey aggregation and its exploitation by predators. Rapid aggregation of some marine fish and crustacean forage species during wind-driven coastal upwelling has recently been discovered, motivating the hypothesis that predators of these forage species track the upwelling circulation in which prey aggregation occurs. We examine this hypothesis in the central California Current Ecosystem using integrative observations of upwelling dynamics, forage species' aggregation, and blue whale movement. Directional origins of blue whale calls repeatedly tracked upwelling plume circulation when wind-driven upwelling intensified and aggregation of forage species was heightened. Our findings illustrate a resource tracking strategy by which blue whales may maximize energy gain amid ephemeral foraging opportunities. These findings have implications for the ecology and conservation of diverse predators that are sustained by forage populations whose behaviour is responsive to episodic environmental dynamics.

Fear dynamically structures the ocean's pelagic zone.

Fear of predation can have wide-ranging ecological effects.1-4 This is especially true in the ocean's pelagic zone, the Earth's largest habitat, where vertical gradients in light and primary productivity force numerous taxa to migrate vertically each night to feed at the surface while minimizing risk from visual predators.5-7 Despite its importance and the fact that it is driven by spatial differences in perceived risk,8 diel vertical migration (DVM) is rarely considered within the "landscape of fear"3,8,9 framework.10 It is also far from the only such process in the pelagic zone. We used continuous, year-long records from an upward-looking echosounder and broadband hydrophone at a cabled observatory off Central California, USA, to observe avoidance reactions by several groups of pelagic animals to the presence of their predators. As expected, vertical migration was ubiquitous, but we also observed behaviors at shorter and longer timescales that were best explained by fear of predation. The presence of foraging odontocetes induced immediate diving behavior in mesopelagic sound-scattering layers, and schools of epipelagic fishes induced similar reaction in layers of zooplankton and mesopelagic micronekton. At longer timescales, the presence of fish schools significantly deepened vertical migration, rearranging life throughout the water column. We argue that behavioral reactions to predation risk are common in the pelagic zone at a range of spatiotemporal scales and that our understanding of food webs and biogeochemical cycling in this immense biome will be incomplete unless we account for fear.

Remote acoustic detection and characterization of fish schooling behavior.

Many fish species form social aggregations or shoals. Understanding the conditions under which these groups sometimes coordinate their behavior in space and time, or "school," is important for understanding their ecology, their effects on the ecosystem, and effective management of their stocks. An automated approach to isolate acoustic aggregations in echosounder data relative to the local background scattering is introduced. Aggregations were then identified and characterized in a large dataset acquired from an autonomous platform and a research vessel. Fish schools were statistically distinct from other aggregations of fish, with differences in their geometry, frequency response, scattering intensity, and scattering distribution. The statistical distribution of acoustic scattering from fish shoals generally followed a Rayleigh distribution as predicted for a randomly organized aggregation of homogenous scatterers. Within fish schools, however, the distribution was distinct from Rayleigh, showing a consistent pattern with most values at low relative scattering levels followed by a sharp roll-off and long right tail. These differences in distribution provide the ability to remotely observe the polarized, organized behavior that defines schooling, a difficult to observe response to environmental and internal conditions, which has large implications for our understanding and management of schooling fish.

Exploring the promise of broadband fisheries echosounders for species discrimination with quantitative assessment of data processing effects.

It remains an open question how well the increased bandwidth afforded by broadband echosounders can improve species discrimination in fisheries acoustics. Here, an objective statistical approach was used to determine if there is information available in dual channel broadband data (45-170 kHz) to allow discrimination between in situ echoes obtained from monospecific aggregations of three species (hake, Merluccius productus: anchovy, Engraulis mordax; and krill, Euphausiia pacifica) using a remotely operated vehicle. These data were used to explore the effects of processing choices on the ability to statistically classify the broadband spectra to species. This ability was affected by processing choices including the Fourier transform analysis window size, available bandwidth, and the method and scale of data averaging. The approach to normalizing the spectra and the position of individual targets in the beam, however, had little effect. Broadband volume backscatter and single target spectra were both used to successfully classify acoustic data from these species with ∼6% greater success using volume backscatter data. Broadband data were effectively classified to species while simulated multi-frequency narrowband data were categorized at rates near chance, supporting the presumption that greater bandwidth increases the information available for the characterization and classification of biological targets.

Risso's dolphins plan foraging dives.

Humans remember the past and use that information to plan future actions. Lab experiments that test memory for the location of food show that animals have a similar capability to act in anticipation of future needs, but less work has been done on animals foraging in the wild. We hypothesized that planning abilities are critical and common in breath-hold divers who adjust each dive to forage on prey varying in quality, location and predictability within constraints of limited oxygen availability. We equipped Risso's dolphins with sound-and-motion recording tags to reveal where they focus their attention through their externally observable echolocation and how they fine tune search strategies in response to expected and observed prey distribution. The information from the dolphins was integrated with synoptic prey data obtained from echosounders on an underwater vehicle. At the start of the dives, whales adjusted their echolocation inspection ranges in ways that suggest planning to forage at a particular depth. Once entering a productive prey layer, dolphins reduced their search range comparable to the scale of patches within the layer, suggesting that they were using echolocation to select prey within the patch. On ascent, their search range increased, indicating that they decided to stop foraging within that layer and started searching for prey in shallower layers. Information about prey, learned throughout the dive, was used to plan foraging in the next dive. Our results demonstrate that planning for future dives is modulated by spatial memory derived from multi-modal prey sampling (echoic, visual and capture) during earlier dives.

Predator-guided sampling reveals biotic structure in the bathypelagic.

We targeted a habitat used differentially by deep-diving, air-breathing predators to empirically sample their prey's distributions off southern California. Fine-scale measurements of the spatial variability of potential prey animals from the surface to 1,200 m were obtained using conventional fisheries echosounders aboard a surface ship and uniquely integrated into a deep-diving autonomous vehicle. Significant spatial variability in the size, composition, total biomass, and spatial organization of biota was evident over all spatial scales examined and was consistent with the general distribution patterns of foraging Cuvier's beaked whales (Ziphius cavirostris) observed in separate studies. Striking differences found in prey characteristics between regions at depth, however, did not reflect differences observed in surface layers. These differences in deep pelagic structure horizontally and relative to surface structure, absent clear physical differences, change our long-held views of this habitat as uniform. The revelation that animals deep in the water column are so spatially heterogeneous at scales from 10 m to 50 km critically affects our understanding of the processes driving predator-prey interactions, energy transfer, biogeochemical cycling, and other ecological processes in the deep sea, and the connections between the productive surface mixed layer and the deep-water column.

Ecological Insights from Pelagic Habitats Acquired Using Active Acoustic Techniques.

Marine pelagic ecosystems present fascinating opportunities for ecological investigation but pose important methodological challenges for sampling. Active acoustic techniques involve producing sound and receiving signals from organisms and other water column sources, offering the benefit of high spatial and temporal resolution and, via integration into different platforms, the ability to make measurements spanning a range of spatial and temporal scales. As a consequence, a variety of questions concerning the ecology of pelagic systems lend themselves to active acoustics, ranging from organism-level investigations and physiological responses to the environment to ecosystem-level studies and climate. As technologies and data analysis methods have matured, the use of acoustics in ecological studies has grown rapidly. We explore the continued role of active acoustics in addressing questions concerning life in the ocean, highlight creative applications to key ecological themes ranging from physiology and behavior to biogeography and climate, and discuss emerging avenues where acoustics can help determine how pelagic ecosystems function.

A critical time window for organismal interactions in a pelagic ecosystem.

To measure organismal coherence in a pelagic ecosystem, we used moored sensors to describe the vertical dynamics of each step in the food chain in shelf waters off the west shore of Oahu, Hawaii. Horizontally extensive, intense aggregations of phytoplankton, zooplankton, and micronekton exhibited strong diel patterns in abundance and vertical distribution, resulting in a highly variable potential for interaction amongst trophic levels. Only around dusk did zooplankton layers overlap with phytoplankton layers. Shortly after sunset, micronekton ascended from the deep, aggregating on the island's shelf. Short-lived departures in migration patterns were detected in depth, vertical distribution, density, and total abundance of micronekton when zooplankton layers were present with typical patterns resuming within one hour. Layers of zooplankton began to disappear within 20 minutes of the arrival of micronekton with no layers present after 50 minutes. The effects of zooplankton layers cascaded even further up the food chain, affecting many behaviors of dolphins observed at dusk including their depth, group size, and inter-individual spacing. As a result of these changes in behavior, during a 30-minute window just after dusk, the number of feeding events observed for each dolphin and consequently the feeding time for each individual more than doubled when zooplankton layers were present. Dusk is a critical period for interactions amongst species in this system from phytoplankton to top predators. Our observations that short time windows can drive the structure and function of a complex suite of organisms highlight the importance of explicitly adding a temporal dimension at a scale relevant to individual organisms to our descriptions of heterogeneity in ocean ecosystems.

Extreme plasticity in life-history strategy allows a migratory predator (jumbo squid) to cope with a changing climate.

Dosidicus gigas (jumbo or Humboldt squid) is a semelparous, major predator of the eastern Pacific that is ecologically and commercially important. In the Gulf of California, these animals mature at large size (>55 cm mantle length) in 1-1.5 years and have supported a major commercial fishery in the Guaymas Basin during the last 20 years. An El Niño event in 2009-2010, was accompanied by a collapse of this fishery, and squid in the region showed major changes in the distribution and life-history strategy. Large squid abandoned seasonal coastal-shelf habitats in 2010 and instead were found in the Salsipuedes Basin to the north, an area buffered from the effects of El Niño by tidal upwelling and a well-mixed water column. The commercial fishery also relocated to this region. Although large squid were not found in the Guaymas Basin from 2010 to 2012, small squid were abundant and matured at an unusually small mantle-length (<30 cm) and young age (approximately 6 months). Juvenile squid thus appeared to respond to El Niño with an alternative life-history trajectory in which gigantism and high fecundity in normally productive coastal-shelf habitats were traded for accelerated reproduction at small size in an offshore environment. Both small and large mature squid, were present in the Salsipuedes Basin during 2011, indicating that both life- history strategies can coexist. Hydro-acoustic data, reveal that squid biomass in this study area nearly doubled between 2010 and 2011, primarily due to a large increase in small squid that were not susceptible to the fishery. Such a climate-driven switch in size-at-maturity may allow D. gigas to rapidly adapt to and cope with El Niño. This ability is likely to be an important factor in conjunction with longerterm climate-change and the potential ecological impacts of this invasive predator on marine ecosystems.

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.

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 Hawaii's 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.

Acoustic basis for fish prey discrimination by echolocating dolphins and porpoises.

The biosonar system of dolphins and porpoises has been studied for about 5 decades and much has been learned [Au, W. W. L. (1993). The Sonar of Dolphins (Springer, New York)]. Most experiments have involved human-made targets; little is known about odontocetes' echolocation of prey. To address this issue, acoustic backscatter from Atlantic cod (Gadus morhua), gray mullet (Chelon labrosus), pollack, (Pollachius pollachius), and sea bass (Dicentrarchus labrax) was measured using simulated biosonar signals of the Atlantic bottlenose dolphin and harbor porpoise. The fish specimens were rotated so that the effects of the fish orientation on the echoes could be determined. Echoes had the highest amplitude and simplest structure when the incident angle was perpendicular to the longitudinal axis of the fish. The complexity of the echoes increased as the aspect angle of the fish moved away from the normal aspect. The echoes in both the time and frequency domains were easily distinguishable among the four species of fish and were generally consistent within species. A cochlear model consisting of a bank of band-passed filters was also used to analyze the echoes. The overall results suggest that there are sufficient acoustic cues available to discriminate between the four species of fish based on the echoes received, independent of aspect angle.

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 prey's 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.

Phonation behavior of cooperatively foraging spinner dolphins.

Groups of spinner dolphins have been shown to cooperatively herd small prey. It was hypothesized that the strong group coordination is maintained by acoustic communication, specifically by frequency-modulated whistles. Observations of groups of spinner dolphins foraging at night within a sound-scattering layer were made with a multibeam echosounder while the rates of dolphin sounds were measured using four hydrophones at 6 m depth intervals. Whistles were only detected when dolphins were not foraging and when animals were surfacing. Differences in click rates were found between depths and between different foraging stages but were relatively low when observations indicated that dolphins were actively feeding despite the consistency of these clicks with echolocation signals. Highest click rates occurred within the scattering layer, during transitions between foraging states. This suggests that clicks may be used directly or indirectly to cue group movement during foraging, potentially by detecting other individuals' positions in the group or serving a direct communicative role which would be contrary to the existing assumption that echolocation and communication are compartmentalized. Communicating via clicks would be beneficial as the signal's characteristics minimize the chance of eavesdropping by competing dolphins and large fish. Our results are unable to support the established paradigm for dolphin acoustic communication and suggest an alternate coordination mechanism in foraging spinner dolphins.

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.

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.

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.

Testing the odontocete acoustic prey debilitation hypothesis: no stunning results.

The hypothesis that sounds produced by odontocetes can debilitate fish was examined. The effects of simulated odontocete pulsed signals on three species of fish commonly preyed on by odontocetes were examined, exposing three individuals of each species as well as groups of four fish to a high-frequency click of a bottlenose dolphin [peak frequency (PF) 120 kHz, 213-dB peak-to-peak exposure level (EL)], a midfrequency click modeled after a killer whale's signal (PF 55 kHz, 208-dB EL), and a low-frequency click (PF 18 kHz, 193-dB EL). Fish were held in a 50-cm diameter net enclosure immediately in front of a transducer where their swimming behavior, orientation, and balance were observed with two video cameras. Clicks were presented at constant rates and in graded sweeps simulating a foraging dolphin's "terminal buzz." No measurable change in behavior was observed in any of the fish for any signal type or pulse modulation rate, despite the fact that clicks were at or near the maximum source levels recorded for odontocetes. Based on the results, the hypothesis that acoustic signals of odontocetes alone can disorient or "stun" prey cannot be supported.