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.

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.

Prior exposure to weathered oil influences foraging of an ecologically important saltmarsh resident fish.

Estuarine ecosystem balance typically relies on strong food web interconnectedness dependent on a relatively low number of resident taxa, presenting a potential ecological vulnerability to extreme ecosystem disturbances. Following the Deepwater Horizon (DwH) oil spill disaster of the northern Gulf of Mexico (USA), numerous ecotoxicological studies showed severe species-level impacts of oil exposure on estuarine fish and invertebrates, yet post-spill surveys found little evidence for severe impacts to coastal populations, communities, or food webs. The acknowledgement that several confounding factors may have limited researchers' abilities to detect negative ecosystem-level impacts following the DwH spill drives the need for direct testing of weathered oil exposure effects on estuarine residents with high trophic connectivity. Here, we describe an experiment that examined the influence of previous exposure to four weathered oil concentrations (control: 0.0 L oil m-2; low: 0.1 L oil m-2; moderate: 0.5-1 L oil m-2; high: 3.0 L oil m-2) on foraging rates of the ecologically important Gulf killifish (Fundulus grandis). Following exposure in oiled saltmarsh mesocosms, killifish were allowed to forage on grass shrimp (Palaeomonetes pugio) for up to 21 h. We found that previous exposure to the high oil treatment reduced killifish foraging rate by ~37% on average, compared with no oil control treatment. Previous exposure to the moderate oil treatment showed highly variable foraging rate responses, while low exposure treatment was similar to unexposed responses. Declining foraging rate responses to previous high weathered oil exposure suggests potential oil spill influence on energy transfer between saltmarsh and off-marsh systems. Additionally, foraging rate variability at the moderate level highlights the large degree of intraspecific variability for this sublethal response and indicates this concentration represents a potential threshold of oil exposure influence on killifish foraging. We also found that consumption of gravid vs non-gravid shrimp was not independent of prior oil exposure concentration, as high oil exposure treatment killifish consumed ~3× more gravid shrimp than expected. Our study findings highlight the sublethal effects of prior oil exposure on foraging abilities of ecologically valuable Gulf killifish at realistic oil exposure levels, suggesting that important trophic transfers of energy to off-marsh systems may have been impacted, at least in the short-term, by shoreline oiling at highly localized scales. This study provides support for further experimental testing of oil exposure effects on sublethal behavioral impacts of ecologically important estuarine species, due to the likelihood that some ecological ramifications of DwH on saltmarshes likely went undetected.

Effects of short-duration oil exposure on bay anchovy (Anchoa mitchilli) embryos and larvae: mortality, malformation, and foraging.

The Deepwater Horizon oil spill highlighted the need to understand the effects of oil exposure on marine eggs and larvae. To determine how short-duration exposure impacts the survivability of early life stages of the bay anchovy, Anchoa mitchilli, embryos and larvae ≤ 3-days-post-hatch (dph) were exposed to high-energy water accommodated fractions of weathered crude oil for 2 or 6 h. Lethal and sublethal effects of short-duration oil exposure were observed, including crippling malformations and altered optimal swimming and foraging behavior of larvae without malformation. The probability of mortality for larvae exposed as embryos (37.37 and 77.31 µg L-1 total polycyclic aromatic hydrocarbons or 'TPAH'), assessed 48 h after exposure, increased from 0.06 to 0.15 (2 h) and 0.10-0.23 (6 h) relative to unoiled controls. When exposed as 1-dph larvae (8.80-37.37 µg L-1 TPAH) and assessed 24 h after exposure, the probabilities increased from 0.20 to 0.76 (2 h) and 0.28-0.99 (6 h). Among surviving larvae, probabilities of yolk-sac, finfold, notochord, and cranio-facial malformations increased with exposure concentration, duration, and time after exposure by up to 0.07 immediately following exposure of 1-dph larvae and 0.55 24 h after exposure. When assessed 48 h after exposure as embryos, the probability of larval malformation reached 0.43. First-feeding (3-dph) foraging behavior was altered immediately and 24 h after 2 h exposures (8.80-77.31 µg L-1 TPAH). Time spent in motion and swim speed increased with exposure concentration by up to 331% and 189%, respectively. The number of bursts min-1 increased by 293% immediately and 152% 24 h after exposure. Burst distance decreased by 201%. Pause duration and burst speed decreased by 391% and 250% immediately and 124% and 109% 24 h after exposure. No effects were found for burst duration or tortuosity. Our results suggest potential cascading effects on fitness and trophic interactions.

Habitat-specific inter and intraspecific behavioral interactions among reef sharks.

Behavioral interactions such as dominance are critical components of animal social lives, competitive abilities, and resulting distribution patterns with coexisting species. Strong interference competition can drive habitat separation, but less is known of the role of interference if agonistic interactions are weak. While most theoretical models assume interference abilities to be constant in an environment, few consider that the extent of interference can vary by habitat and change model predictions. Using baited underwater cameras, we show a consistent dominance status between two sympatric reef sharks at an uninhabited Pacific atoll. Blacktip reef shark (Carcharhinus melanopterus) and gray reef shark (Carcharhinus amblyrhyncos) relative abundance showed an inverse relationship to each other but the strength of this relationship varied by habitat. Reef shark relative abundance declined more rapidly in the presence of heterospecifics on forereef habitats as opposed to backreefs. In all habitats, gray reef sharks were more likely to bite bait cages than blacktips when both species were present, and appeared to be the dominant species. Intraspecific interactions were also apparent, with individual willingness to bite bait decreasing as the number of conspecifics increased. Gray reef sharks may exert differential control over blacktip foraging success in different habitats. Habitat-specific behavioral interactions may partially explain patterns of spatial separation between competing species where interference is weak.

Previous oil exposure alters Gulf Killifish Fundulus grandis oil avoidance behavior.

Oil spills threaten the structure and function of ecological communities. The Deepwater Horizon spill was predicted to have catastrophic consequences for nearshore fishes, but field studies indicate resilience in populations and communities. Previous research indicates many marsh fishes exhibit avoidance of oil contaminated areas, representing one potential mechanism for this resilience. Here, we test whether prior oil exposure of Gulf killifish Fundulus grandis alters this avoidance response. Using choice tests between unoiled and oiled sediments at one of three randomized concentrations (low: 0.1 L oil m-2, medium: 0.5 L oil m-2, or high: 3.0 L oil m-2), we found that, even at low prior exposure levels, killifish lose recognition of oiled sediments compared to control, unexposed fish. Preference for unoiled sediments was absent across all oil concentrations after oil exposure, and some evidence for preference of oiled sediments at high exposure was demonstrated. These results highlight the lack of response to toxic environments in exposed individuals, indicating altered behavior despite organism survival. Future research should document additional sublethal consequences that affect ecosystem and food web functioning.

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.

Effects on schooling function in mackerel of sub-lethal capture related stressors: Crowding and hypoxia.

The selectivity of fishing gears with respect to fish species and size is important, both for fisheries management and fishing operations. Purse seining is an efficient, environmentally friendly fish capture methodology generally targeting single species aggregations, but once a fish school has been selected and surrounded by the seine, there is no selections for individual size, species or catch quantity. A common practice for evaluating the catch is to haul the seine to a point where physical samples or inspections of catch composition can be made. The release process is called slipping and may lead to mortality in the released fish. The objective of this study was to simulate a crowding situation and investigate how the behaviour was affected in response to increased fish density, decreased oxygen levels, or a combination of the two, and to see if there is a behavioural measure that can be used to set safe crowding limits. The experiment was conducted on Mackerel (Scomber scombrus) held in net pens. The volume of the net pen was reduced to increase fish density, and a tarpaulin bag was wrapped around the pen to reduce the oxygen levels. Oxygen, fish density and space occupancy was monitored during the experiment, and the behavioural reactions was assessed using an imaging sonar. The main result was that the schooling function, i.e. the response to a predator model, was significantly reduced during crowding but not in response to hypoxia. There were some indications of a slow recovery of the function post-treatment. We conclude that crowding causes behavioural responses that occur before densities that induce fish mortality. Consequently, there is a behavioural response that could be used as a proxy for setting safe crowding limits.

Technical and conceptual considerations for using animated stimuli in studies of animal behavior.

Rapid technical advances in the field of computer animation (CA) and virtual reality (VR) have opened new avenues in animal behavior research. Animated stimuli are powerful tools as they offer standardization, repeatability, and complete control over the stimulus presented, thereby "reducing" and "replacing" the animals used, and "refining" the experimental design in line with the 3Rs. However, appropriate use of these technologies raises conceptual and technical questions. In this review, we offer guidelines for common technical and conceptual considerations related to the use of animated stimuli in animal behavior research. Following the steps required to create an animated stimulus, we discuss (I) the creation, (II) the presentation, and (III) the validation of CAs and VRs. Although our review is geared toward computer-graphically designed stimuli, considerations on presentation and validation also apply to video playbacks. CA and VR allow both new behavioral questions to be addressed and existing questions to be addressed in new ways, thus we expect a rich future for these methods in both ultimate and proximate studies of animal behavior.

Computer-animated stimuli to measure motion sensitivity: constraints on signal design in the Jacky dragon.

Identifying perceptual thresholds is critical for understanding the mechanisms that underlie signal evolution. Using computer-animated stimuli, we examined visual speed sensitivity in the Jacky dragon Amphibolurus muricatus, a species that makes extensive use of rapid motor patterns in social communication. First, focal lizards were tested in discrimination trials using random-dot kinematograms displaying combinations of speed, coherence, and direction. Second, we measured subject lizards' ability to predict the appearance of a secondary reinforcer (1 of 3 different computer-generated animations of invertebrates: cricket, spider, and mite) based on the direction of movement of a field of drifting dots by following a set of behavioural responses (e.g., orienting response, latency to respond) to our virtual stimuli. We found an effect of both speed and coherence, as well as an interaction between these 2 factors on the perception of moving stimuli. Overall, our results showed that Jacky dragons have acute sensitivity to high speeds. We then employed an optic flow analysis to match the performance to ecologically relevant motion. Our results suggest that the Jacky dragon visual system may have been shaped to detect fast motion. This pre-existing sensitivity may have constrained the evolution of conspecific displays. In contrast, Jacky dragons may have difficulty in detecting the movement of ambush predators, such as snakes and of some invertebrate prey. Our study also demonstrates the potential of the computer-animated stimuli technique for conducting nonintrusive tests to explore motion range and sensitivity in a visually mediated species.

Collective responses of a large mackerel school depend on the size and speed of a robotic fish but not on tail motion.

So far, actuated fish models have been used to study animal interactions in small-scale controlled experiments. This study, conducted in a semi-controlled setting, investigates robot5 interactions with a large wild-caught marine fish school (∼3000 individuals) in their natural social environment. Two towed fish robots were used to decouple size, tail motion and speed in a series of sea-cage experiments. Using high-resolution imaging sonar and sonar-video blind scoring, we monitored and classified the school's collective reaction towards the fish robots as attraction or avoidance. We found that two key releasers-the size and the speed of the robotic fish-were responsible for triggering either evasive reactions or following responses. At the same time, we found fish reactions to the tail motion to be insignificant. The fish evaded a fast-moving robot even if it was small. However, mackerels following propensity was greater towards a slow small robot. When moving slowly, the larger robot triggered significantly more avoidance responses than a small robot. Our results suggest that the collective responses of a large school exposed to a robotic fish could be manipulated by tuning two principal releasers-size and speed. These results can help to design experimental methods for in situ observations of wild fish schools or to develop underwater robots for guiding and interacting with free-ranging aggregated aquatic organisms.

Investigating the Effect of Tones and Frequency Sweeps on the Collective Behavior of Penned Herring (Clupea harengus).

We experimentally played back tones and sweeps to captive herring (Clupea harengus) in a net pen and measured the collective response of a large and a small group of fish using a camera, echo sounder, and multibeam sonar. The playbacks ranged in frequency from 160 to 500 Hz and 131 to 147 dB re 1 µPa in received sound pressure level. Herring behavior was scored by a team that blindly evaluated the observations. Overall, the responses were modest. Stronger reactions were observed at higher source levels, lower frequencies, and smaller school sizes, but there was no effect on signal rise time.

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".

Investigating differences in vigilance tactic use within and between the sexes in eastern grey kangaroos.

Aggregation is thought to enhance an animal's security through effective predator detection and the dilution of risk. A decline in individual vigilance as group size increases is commonly reported in the literature and called the group size effect. However, to date, most of the research has only been directed toward examining whether this effect occurs at the population level. Few studies have explored the specific contributions of predator detection and risk dilution and the basis of individual differences in the use of vigilance tactics. We tested whether male and female (non-reproductive or with young) eastern grey kangaroos (Macropus giganteus) adopted different vigilance tactics when in mixed-sex groups and varied in their reliance on predator detection and/or risk dilution as group size changed. This species exhibits pronounced sexual dimorphism with females being much smaller than males, making them differentially vulnerable toward predators. We combined field observations with vigilance models describing the effects of detection and dilution on scanning rates as group size increased. We found that females with and without juveniles relied on predator detection and risk dilution, but the latter adjusted their vigilance to the proportion of females with juveniles within their group. Two models appeared to equally support the data for males suggesting that males, similarly to females, relied on predator detection and risk dilution but may also have adjusted their vigilance according to the proportion of mothers within their group. Differential vulnerability may cause sex differences in vigilance tactic use in this species. The presence of males within a group that do not, or only partially, contribute to predator detection and are less at risk may cause additional security costs to females. Our results call for reexamination of the classical view of the safety advantages of grouping to provide a more detailed functional interpretation of gregariousness.

Exploring the costs and benefits of social information use: an appraisal of current experimental evidence.

Research on social learning has focused traditionally on whether animals possess the cognitive ability to learn novel motor patterns from tutors. More recently, social learning has included the use of others as sources of inadvertent social information. This type of social learning seems more taxonomically widespread and its use can more readily be approached as an economic decision. Social sampling information, however, can be tricky to use and calls for a more lucid appraisal of its costs. In this four-part review, we address these costs. Firstly, we address the possibility that only a fraction of group members are actually providing social information at any one time. Secondly, we review experimental research which shows that animals are circumspect about social information use. Thirdly, we consider the cases where social information can lead to incorrect decisions and finally, we review studies investigating the effect of social information quality. We address the possibility that using social information or not is not a binary decision and present results of a study showing that nutmeg mannikins combine both sources of information, a condition that can lead to the establishment of informational cascades. We discuss the importance of empirically investigating the economics of social information use.

Considerations in video playback design: using optic flow analysis to examine motion characteristics of live and computer-generated animation sequences.

The increasing use of the video playback technique in behavioural ecology reveals a growing need to ensure better control of the visual stimuli that focal animals experience. Technological advances now allow researchers to develop computer-generated animations instead of using video sequences of live-acting demonstrators. However, care must be taken to match the motion characteristics (speed and velocity) of the animation to the original video source. Here, we presented a tool based on the use of an optic flow analysis program to measure the resemblance of motion characteristics of computer-generated animations compared to videos of live-acting animals. We examined three distinct displays (tail-flick (TF), push-up body rock (PUBR), and slow arm wave (SAW)) exhibited by animations of Jacky dragons (Amphibolurus muricatus) that were compared to the original video sequences of live lizards. We found no significant differences between the motion characteristics of videos and animations across all three displays. Our results showed that our animations are similar the speed and velocity features of each display. Researchers need to ensure that similar motion characteristics in animation and video stimuli are represented, and this feature is a critical component in the future success of the video playback technique.