Environmental impact on visual perception modulates behavioral responses of schooling fish to looming predators.

Aggregation in social fishes has evolved to improve safety from predators. The individual interaction mechanisms that govern collective behavior are determined by the sensory systems that translate environmental information into behavior. In dynamic environments, shifts in conditions impede effective visual sensory perception in fish schools, and may induce changes in the collective response. Here, we consider whether environmental conditions that affect visual contrast modulate the collective response of schools to looming predators. By using a virtual environment to simulate four contrast levels, we tested whether the collective state of minnow fish schools was modified in response to a looming optical stimulus. Our results indicate that fish swam slower and were less polarized in lower contrast conditions. Additionally, schooling metrics known to be regulated by non-visual sensory systems tended to correlate better when contrast decreased. Over the course of the escape response, schools remained tightly formed and retained the capability of transferring social information. We propose that when visual perception is compromised, the interaction rules governing collective behavior are likely to be modified to prioritize ancillary sensory information crucial to maximizing chance of escape. Our results imply that multiple sensory systems can integrate to control collective behavior in environments with unreliable visual information.

Taxonomical classification of reef fish with broadband backscattering models and machine learning approaches.

Commercially available broadband echosounders have the potential to classify acoustic targets based on their scattering responses, which are a function of their species-specific morphological and physiological properties. This is particularly important in complex environments with biologically diverse fish assemblages. Using theoretical acoustic scattering models among 130 fishes across six species, we examine the potential to classify reef fish based on the fine-scale gas-bearing swim bladder morphology quantified from three-dimensional computed-tomography models. Modeled echoes of the swim bladder for an incident broadband sound source (30-200 kHz) and across a range of orientation angles (±44°) are acoustically simulated using the boundary element method. Backscatter models present characteristics that are consistent within species and distinguishable among them. Broadband and multifrequency echoes are classified and compared with Bayesian, support vector machine, k-nearest neighbor, and convolutional neural network estimators. Classifiers have higher accuracies (>70%) when noise is not present and perform better when applied to broadband spectra than multifrequency data (42, 70, 100, 132, 160, 184 kHz). The modeling and classification approaches presented indicate that a taxonomic distinction based on morphologically dependent scattering responses is possible and may provide the capacity to acoustically discriminate among fish species.

Using unmanned aerial vehicle (UAV) surveys and image analysis in the study of large surface-associated marine species: a case study on reef sharks Carcharhinus melanopterus shoaling behaviour.

A novel image analysis-based technique applied to unmanned aerial vehicle (UAV) survey data is described to detect and locate individual free-ranging sharks within aggregations. The method allows rapid collection of data and quantification of fine-scale swimming and collective patterns of sharks. We demonstrate the usefulness of this technique in a small-scale case study exploring the shoaling tendencies of blacktip reef sharks Carcharhinus melanopterus in a large lagoon within Moorea, French Polynesia. Using our approach, we found that C. melanopterus displayed increased alignment with shoal companions when distributed over a sandflat where they are regularly fed for ecotourism purposes as compared with when they shoaled in a deeper adjacent channel. Our case study highlights the potential of a relatively low-cost method that combines UAV survey data and image analysis to detect differences in shoaling patterns of free-ranging sharks in shallow habitats. This approach offers an alternative to current techniques commonly used in controlled settings that require time-consuming post-processing effort.

Predator identity and time of day interact to shape the risk-reward trade-off for herbivorous coral reef fishes.

Non-consumptive effects (NCEs) of predators occur as prey alters their habitat use and foraging decisions to avoid predation. Although NCEs are recognized as being important across disparate ecosystems, the factors influencing their strength and importance remain poorly understood. Ecological context, such as time of day, predator identity, and prey condition, may modify how prey species perceive and respond to risk, thereby altering NCEs. To investigate how predator identity affects foraging of herbivorous coral reef fishes, we simulated predation risk using fiberglass models of two predator species (grouper Mycteroperca bonaci and barracuda Sphyraena barracuda) with different hunting modes. We quantified how predation risk alters herbivory rates across space (distance from predator) and time (dawn, mid-day, and dusk) to examine how prey reconciles the conflicting demands of avoiding predation vs. foraging. When we averaged the effect of both predators across space and time, they suppressed herbivory similarly. Yet, they altered feeding differently depending on time of day and distance from the model. Although feeding increased strongly with increasing distance from the predators particularly during dawn, we found that the barracuda model suppressed herbivory more strongly than the grouper model during mid-day. We suggest that prey hunger level and differences in predator hunting modes could influence these patterns. Understanding how context mediates NCEs provides insight into the emergent effects of predator-prey interactions on food webs. These insights have broad implications for understanding how anthropogenic alterations to predator abundances can affect the spatial and temporal dynamics of important ecosystem processes.

Active acoustic surveys reveal coastal fish community resistance to an environmental perturbation in South Florida.

Coastal fish communities are under increasing levels of stress associated with climate variation and anthropogenic activities. However, the high degree of behavioral plasticity of many species within these communities allow them to cope with altered environmental conditions to some extent. Here, we combine meteorological information, data from hydroacoustic surveys, and recordings of goliath grouper sound production to examine the response of coastal fish communities to heavy rainfall events in South Florida, USA, that resulted in the release of excess storm water into surrounding estuaries and coastal waters. We observed a nearly 12,000% increase in water column acoustic backscatter following a heavy rainfall event of September 16th, 2015. Interestingly, estimates of school backscatter, a proxy for biomass, increased by 172% with the onset of the perturbation. Schooling fish density also increased by 182%, as did acoustically derived estimates of mean schooling fish length (21%). Following the perturbed period, school backscatter decreased by 406%, along with schooling density (272%), and mean schooling fish length (35%). Hydrophone and hydroacoustic data also revealed that goliath grouper (Epinephelus itajara) spawning aggregations were persistent in the region throughout the duration of the study and continued to exhibit courtship behavior during the perturbed period. Our observations demonstrate the high level of resistance common in coastal species but raises new questions regarding the threshold at which fish communities and reproductive activities are disrupted. As coastal land use continues to increase, and the effects of global climate change become more pronounced, more Before-After Control Impact (BACI) studies will provide improved insight into the overall response of nearshore communities to future perturbations and the cumulative effect of repeated perturbations over extended periods.

Capture stress and post-release mortality of blacktip sharks in recreational charter fisheries of the Gulf of Mexico.

Understanding the stress responses of sharks to recreational catch and release fishing has important management and conservation implications. The blacktip shark Carcharhinus limbatus is a popular recreational species targeted throughout the western, central and eastern Gulf of Mexico (Gulf) yet it is unclear what levels of physiological stress result from catch-release fishing practices with hook and line gear and if the stress levels result in post-release mortality. This study correlates physiological response to stress through blood chemistry analysis and examines post-release behaviour of adult blacktip sharks caught to determine post-release mortality rates. Release behaviour was determined by pop-up satellite archival transmitting (PSAT) tags that record temperature, depth and light level data. To quantify physiological stress levels, blood samples were collected from 52 blacktip sharks and a suite of metabolic and osmotic markers were measured. Thirty-six of those blacktip sharks were also outfitted with a PSAT tag yielding time-at-large from 3 to 180 days. Of the 36 tags, 22 (61%) provided sufficient data to confirm post-release fate and 11 (31%) were recovered providing high-resolution data. Tag data suggests a post-release morality rate of 22.7% (95% confidence interval 7.8-45.4%), with mortality occurring within minutes (immediate mortality) to over 12 h post-release (delayed mortality). Compared to survivors, immediate mortalities exhibited significantly higher lactate (median 2.8 mmol/Lsurvivor vs 5.9 mmol/Limmediate mortality) and significantly lower hematocrit (median 24.4% survivor vs 14% immediate mortality) levels, but no difference was detected between survivors and delayed mortalities. Higher mortality in the western (30%) compared to the central (20%) Gulf may be due to shark handling. All PSATs from mortalities (N = 5) were recovered, and archived data revealed evidence of tag ingestion by predators. Results suggest reduced fight time, decreased handling time and limited air exposure provide blacktip sharks the best survival chances after release by recreational anglers.

The Evolution of Lateralization in Group Hunting Sailfish.

Lateralization is widespread throughout the animal kingdom [1-7] and can increase task efficiency via shortening reaction times and saving on neural tissue [8-16]. However, lateralization might be costly because it increases predictability [17-21]. In predator-prey interactions, for example, predators might increase capture success because of specialization in a lateralized attack, but at the cost of increased predictability to their prey, constraining the evolution of lateralization. One unexplored mechanism for evading such costs is group hunting: this would allow individual-level specialization, while still allowing for group-level unpredictability. We investigated this mechanism in group hunting sailfish, Istiophorus platypterus, attacking schooling sardines, Sardinella aurita. During these attacks, sailfish alternate in attacking the prey using their elongated bills to slash or tap the prey [22-24]. This rapid bill movement is either leftward or rightward. Using behavioral observations of identifiable individual sailfish hunting in groups, we provide evidence for individual-level attack lateralization in sailfish. More strongly lateralized individuals had a higher capture success. Further evidence of lateralization comes from morphological analyses of sailfish bills that show strong evidence of one-sided micro-teeth abrasions. Finally, we show that attacks by single sailfish are indeed highly predictable, but predictability rapidly declines with increasing group size because of a lack of population-level lateralization. Our results present a novel benefit of group hunting: by alternating attacks, individual-level attack lateralization can evolve, without the negative consequences of individual-level predictability. More generally, our results suggest that group hunting in predators might provide more suitable conditions for the evolution of strategy diversity compared to solitary life.

Maximum swimming speeds of sailfish and three other large marine predatory fish species based on muscle contraction time and stride length: a myth revisited.

Billfishes are considered to be among the fastest swimmers in the oceans. Previous studies have estimated maximum speed of sailfish and black marlin at around 35 m s-1 but theoretical work on cavitation predicts that such extreme speed is unlikely. Here we investigated maximum speed of sailfish, and three other large marine pelagic predatory fish species, by measuring the twitch contraction time of anaerobic swimming muscle. The highest estimated maximum swimming speeds were found in sailfish (8.3±1.4 m s-1), followed by barracuda (6.2±1.0 m s-1), little tunny (5.6±0.2 m s-1) and dorado (4.0±0.9 m s-1); although size-corrected performance was highest in little tunny and lowest in sailfish. Contrary to previously reported estimates, our results suggest that sailfish are incapable of exceeding swimming speeds of 10-15 m s-1, which corresponds to the speed at which cavitation is predicted to occur, with destructive consequences for fin tissues.

Not So Fast: Swimming Behavior of Sailfish during Predator-Prey Interactions using High-Speed Video and Accelerometry.

Billfishes are considered among the fastest swimmers in the oceans. Despite early estimates of extremely high speeds, more recent work showed that these predators (e.g., blue marlin) spend most of their time swimming slowly, rarely exceeding 2 m s(-1). Predator-prey interactions provide a context within which one may expect maximal speeds both by predators and prey. Beyond speed, however, an important component determining the outcome of predator-prey encounters is unsteady swimming (i.e., turning and accelerating). Although large predators are faster than their small prey, the latter show higher performance in unsteady swimming. To contrast the evading behaviors of their highly maneuverable prey, sailfish and other large aquatic predators possess morphological adaptations, such as elongated bills, which can be moved more rapidly than the whole body itself, facilitating capture of the prey. Therefore, it is an open question whether such supposedly very fast swimmers do use high-speed bursts when feeding on evasive prey, in addition to using their bill for slashing prey. Here, we measured the swimming behavior of sailfish by using high-frequency accelerometry and high-speed video observations during predator-prey interactions. These measurements allowed analyses of tail beat frequencies to estimate swimming speeds. Our results suggest that sailfish burst at speeds of about 7 m s(-1) and do not exceed swimming speeds of 10 m s(-1) during predator-prey interactions. These speeds are much lower than previous estimates. In addition, the oscillations of the bill during swimming with, and without, extension of the dorsal fin (i.e., the sail) were measured. We suggest that extension of the dorsal fin may allow sailfish to improve the control of the bill and minimize its yaw, hence preventing disturbance of the prey. Therefore, sailfish, like other large predators, may rely mainly on accuracy of movement and the use of the extensions of their bodies, rather than resorting to top speeds when hunting evasive prey.

Experimental evidence of threat-sensitive collective avoidance responses in a large wild-caught herring school.

Aggregation is commonly thought to improve animals' security. Within aquatic ecosystems, group-living prey can learn about immediate threats using cues perceived directly from predators, or from collective behaviours, for example, by reacting to the escape behaviours of companions. Combining cues from different modalities may improve the accuracy of prey antipredatory decisions. In this study, we explored the sensory modalities that mediate collective antipredatory responses of herring (Clupea harengus) when in a large school (approximately 60,000 individuals). By conducting a simulated predator encounter experiment in a semi-controlled environment (a sea cage), we tested the hypothesis that the collective responses of herring are threat-sensitive. We investigated whether cues from potential threats obtained visually or from the perception of water displacement, used independently or in an additive way, affected the strength of the collective avoidance reactions. We modified the sensory nature of the simulated threat by exposing the herring to 4 predator models differing in shape and transparency. The collective vertical avoidance response was observed and quantified using active acoustics. The combination of sensory cues elicited the strongest avoidance reactions, suggesting that collective antipredator responses in herring are mediated by the sensory modalities involved during threat detection in an additive fashion. Thus, this study provides evidence for magnitude-graded threat responses in a large school of wild-caught herring which is consistent with the "threat-sensitive hypothesis".

Regional variation in mercury and stable isotopes of red snapper (Lutjanus campechanus) in the northern Gulf of Mexico, USA.

The presence of total mercury (Hg) in fish tissue and the potential associated health risks has become a global concern in marine ecosystems. Few studies have examined basin-scale variation in Hg accumulation in marine ecosystems, and determining if Hg concentrations in fish tissue vary across marine ecosystems is a key monitoring question. The present study evaluated Hg concentrations in red snapper (Lutjanus campechanus) tissue across three regions of the northern Gulf of Mexico (Alabama, Louisiana, and Texas, USA) and between two habitat types (oil and gas platforms and nonplatforms) within each region. Nitrogen (δ(15)N), carbon (δ(13)C), and sulfur (δ(34)S) stable isotopes were used to investigate ecological differences that may affect Hg concentrations among regions and between habitats. Mercury concentrations in red snapper tissue were positively correlated with fish total length. Regional differences in Hg concentrations were significant, with fish collected from Alabama having the highest concentrations and fish collected from Louisiana having the lowest. No significant difference existed in Hg concentrations between habitats, suggesting that association with platforms may not be a significant factor contributing to red snapper Hg concentrations. While δ(15)N did not differ significantly among the three regions, Texas red snapper were more enriched in δ(34)S and depleted in δ(13)C compared with Alabama and Louisiana red snapper. Although the majority of red snapper collected in the present study had Hg concentrations below safe consumption guidelines, regional differences suggest that spatially explicit monitoring programs may be important for basin-wide assessments.

Characterization of Atlantic cod spawning habitat and behavior in Icelandic coastal waters.

The physical habitat used during spawning may potentially be an important factor affecting reproductive output of broadcast spawning marine fishes, particularly for species with complex, substrate-oriented mating systems and behaviors, such as Atlantic cod Gadus morhua. We characterized the habitat use and behavior of spawning Atlantic cod at two locations off the coast of southwestern Iceland during a 2-d research cruise (15-16 April 2009). We simultaneously operated two different active hydroacoustic gear types, a split beam echosounder and a dual frequency imaging sonar (DIDSON), as well as a remotely operated underwater vehicle (ROV). A total of five fish species were identified through ROV surveys: including cusk Brosme brosme, Atlantic cod, haddock Melanogrammus aeglefinus, lemon sole Microstomus kitt, and Atlantic redfish Sebastes spp. Of the three habitats identified in the acoustic surveys, the transitional habitat between boulder/lava field and sand habitats was characterized by greater fish density and acoustic target strength compared to that of sand or boulder/lava field habitats independently. Atlantic cod were observed behaving in a manner consistent with published descriptions of spawning. Individuals were observed ascending 1-5 m into the water column from the bottom at an average vertical swimming speed of 0.20-0.25 m s(-1) and maintained an average spacing of 1.0-1.4 m between individuals. Our results suggest that cod do not choose spawning locations indiscriminately despite the fact that it is a broadcast spawning fish with planktonic eggs that are released well above the seafloor.

The dynamics of coordinated group hunting and collective information transfer among schooling prey.

Predator-prey interactions are vital to the stability of many ecosystems. Yet, few studies have considered how they are mediated due to substantial challenges in quantifying behavior over appropriate temporal and spatial scales. Here, we employ high-resolution sonar imaging to track the motion and interactions among predatory fish and their schooling prey in a natural environment. In particular, we address the relationship between predator attack behavior and the capacity for prey to respond both directly and through collective propagation of changes in velocity by group members. To do so, we investigated a large number of attacks and estimated per capita risk during attack and its relation to the size, shape, and internal structure of prey groups. Predators were found to frequently form coordinated hunting groups, with up to five individuals attacking in line formation. Attacks were associated with increased fragmentation and irregularities in the spatial structure of prey groups, features that inhibit collective information transfer among prey. Prey group fragmentation, likely facilitated by predator line formation, increased (estimated) per capita risk of prey, provided prey schools were maintained below a threshold size of approximately 2 m(2). Our results highlight the importance of collective behavior to the strategies employed by both predators and prey under conditions of considerable informational constraints.