Acoustic and visual stimuli combined promote stronger responses to aerial predation in fish

Abstract

Bird predation poses a strong selection pressure on fish. Since birds must enter the water to catch fish, a combination of visual and mechano-acoustic cues (multimodal) characterize an immediate attack, while single cues (unimodal) may represent less dangerous disturbances. We investigated whether fish could use this information to distinguish between non-threatening and dangerous events and adjust their antipredator response to the perceived level of risk. To do so, we investigated the antipredator behavior of the sulphur molly (Poecilia sulphuraria), a small freshwater fish which is almost exclusively preyed on by piscivorous birds in its endemic sulfide spring habitat. In a field survey, we confirmed that these fish frequently have to distinguish between disturbances stemming from attacking birds (multimodal) and those which pose no (immediate) threat such as bird overflights (unimodal). In a laboratory experiment, we then exposed fish to artificial visual and/or acoustic stimuli presented separately or combined. Sensitivity was high regardless of stimulus type and number (more than 96% of fish initiated diving), but fish dove deeper, faster, and for longer when both stimuli were available simultaneously. Based on the system’s high rates of bird activity, we argue that such an unselective dive initiation with subsequent fine-tuning of diving parameters in accordance to cue modality represents an optimal strategy for these fish to save energy necessary to respond to future attacks. Ultimately, our study shows that fish anticipate the imminent risk posed by disturbances linked to bird predation through integrating information from both visual and acoustic cues.

Fish waves as emergent collective antipredator behavior

“…Shooting into the water had no noticeable effects on the birds presumably because they are used to objects from overhanging trees frequently dropping into the river. 16 We verified that the spatial extension of the two-dimensional fish schools and thus number of fish that a predator was faced with was similar across all treatments (shots and controls as well as natural bird attacks, see Figure S2).…”

“…Usually, kiskadees did not elicit post-attack waves, presumably because the stimulus of just putting the tip of their beak into the water (Video S3) was not a strong enough trigger. 16 In kingfishers, waiting times significantly increased with the number of post-attack waves, but were not affected by whether the kingfisher caught a fish or not (SI_stats_5; LMM (Gaussian-lognormal) , number of waves: F 1,103 = 14.48, p < 0.001; success: F 1,100 = 0.39, p = 0.535; year: F 1,58 = 0.02, p = 0.881; Figure 3E). The probability to launch a successful attack for kingfishers was not affected by the number of waves observed or the time a bird waited before the attack (SI_stats_6; GLMM (binomial; cloglog link) , number of waves: c 2 (1) = 0.56, p = 0.456; waiting time: c 2 (1) = 0.04, p = 0.833; year: c 2 (1) = 5.17, p = 0.023; Figure 3F).…”

“…It remains unclear how much of the original escape function of the diving during the waves is still present because the fish dive only a few centimeters deep (Video S2), which is unlikely to provide much protection from herons with long beaks and kingfishers that enter the water. Also, wave dives in response to predator stimuli typically last 3-5 s (see Lukas et al 16 ) and are much shorter than foraging dives (35-135 s), which fish perform individually and not in groups. 15 This shows that fish are capable of much longer dive times but decide not to maximize the underwater time in the presence of predators.…”

Subcritical escape waves in schooling fish

“…Next, we explore whether an additional change of individuals' responsiveness (quantified by the average response threshold) can move the school to or across a critical manifold. Although (28) found no significant change in individual responsiveness resulting from a higher perceived environmental risk, these findings may not extend to multisensory cues or noisy environments (51,52). In Fig.…”

Are you scared yet? Variations to cue indices elicit differential prey behavioral responses even when gape-limited predators are relatively small

“…These modalities can include vision, audition, olfaction, taste, and pressure (Bouwma and Hazlett 2001;Smolka et al 2011). In addition to these singular modes, organisms use sensory information gathered from multiple modes for a more accurate description of the surrounding environment (Lukas et al 2021). Within the landscape of fear concept, these sensory mechanisms have evolved to detect the degree of threat or risk associated with the presence of predators.…”