To see and not be seen: Carangids hide behind sharks to prey on fish

Concealment strategies in predators include morphological adaptations or colorations/patterns aiming to increase hunting success by hiding disguise from prey or blending in with the environment (Pembury Smith & Ruxton, 2020; Stevens & Merilaita, 2009). In fish, these strategies may also involve specific behavioral patterns such as the shadowing behavior, consisting of a predator (i.e., the shadowing species) swimming closely to a larger moving individual (i.e., the shadowed species) to hide from its prey (Matchette et al., 2023). In this interspecific association, documented by only a few examples in coral reef ecosystems, the shadowing individual receives benefits (e.g., facilitated access to food), and the shadowed individual, which is often a nonpredatory species, is assumed to experience neither advantage nor disadvantage, although the cost/benefit may be context-specific (Aronson, 1983; Matchette et al., 2022, 2023; Ormond, 1980; Sazima et al., 2007). This study provides multiyear direct observations of a previously undocumented shadowing hunting strategy adopted by the blue runner Caranx crysos (Mitchill, 1815) associating with adults of the sandbar shark, Carcharhinus plumbeus (Nardo, 1827), to conceal themselves and approach prey undetected. Teleosts may associate with sharks for various purposes, including increased protection from other predators, enhanced access to food, or to remove parasites from their skin through exfoliation (Andrades et al., 2012; Brunnschweiler, 2006; Fuller & Parsons, 2019; Knochel et al., 2023; Ovegård et al., 2022; Papastamatiou et al., 2007; Williams et al., 2022). However, to our knowledge, shadowing behavior displayed by teleosts associated with sharks for hunting purposes has not been reported. Our observations were made through benthic baited remote underwater video (BRUV) and dive-operated video (DOV) surveys during the monitoring of a sandbar shark aggregation occurring every summer around Lampione island (Cattano et al., 2021, 2023; see Appendix S1 for further details). During the study, we recorded 26 predation events (10 from BRUV and 16 from DOV) performed by C. crysos, consisting of high-speed attacks on shoals of small gregarious fish: the common damselfish (Chromis chromis) and the picarels (Spicara spp.). BRUV (n = 11 out of 54) and DOV (n = 23 out of 49) footage also recorded C. crysos closely associated with a C. plumbeus individual, matching its swimming speed and direction (Figure 1). These interactions lasted on average 27 s (±21 SD) for DOV and 15 s (±5 SD) for BRUV, though their durations are likely underestimated as events always started and ended outside the field of view. In nine out of 34 blue runner-shark association events (i.e., two events recorded by BRUV and seven by DOV, 26% occurrence), shadowing C. crysos left the shark to attack prey groups and then returned to its former position to restore the association (Videos S2–S6). This behavior might provide an advantage to the shadowing species by keeping it concealed until just before the attack, when it is close enough to prey groups to achieve hunting success. This strategy differs from the most common hunting behavior displayed by C. crysos, which in most of the cases involved groups of two or more individuals swimming midwater or near to the seabed and pursuing prey located in the water column or just above the seafloor (Appendix S1: Figure S1; Video S1). Prey fish responded to the approaching blue runners by forming schools (i.e., a polarized and coordinated aggregation used as an antipredator strategy; Pitcher & Parrish, 1993) and reducing interindividual distance before darting toward the seafloor to shelter (Video S1). To estimate the potential benefit of displaying shadowing behavior, we measured the occurrence of prey response (i.e., the number of observations where prey formed schools in response to an approaching predator) from BRUVs (n = 54) under three different circumstances: (1) when single or multiple individuals of C. crysos approached the prey (n = 23); (2) when C. crysos approached the prey by swimming close to a shark (i.e., shadowing behavior; n = 8: prey groups were not present in three out of the 11 videos recording shadowing events); (3) when a shark was recorded swimming close to a prey shoal (n = 20). Furthermore, we used DOV observations (n = 49) to measure the occurrence of prey school formation per time of observation in the presence of C. crysos hunting, as well as the average time between the predator approach (identified as the start of predator acceleration toward prey groups) and the prey school formation (i.e., when individuals within the prey group started reducing their interindividual distance, orienting in the same direction and showing synchronized and polarized movements; Pavlov & Kasumyan, 2000). This latter measurement was used as a proxy of prey reaction distance exhibited in response to shadowing and non-shadowing predator strategies. BRUV's results show that in 96% of the cases (22 out of 23 events) prey groups were able to perceive the hunting risk in advance displaying an antipredator response (i.e., schooling formation) when unassociated C. crysos approached them (Figure 2). On the contrary, events of prey school formation were significantly lower (1 out of 8 events, 12.5% occurrence; G = 30.304, df = 2, p < 0.0001) when shadowing C. crysos approached, and this response was similar when a shark approached alone (3 out of 20 events, 15% occurrence; Figure 2). DOV results showed a similar response pattern by prey, in which the number of schooling events was significantly lower (t = −5.2235, p < 0.001) and the timing of school formation was delayed (t = −6.9586, p < 0.001) when shadowing C. crysos approached than when they were not associated to C. plumbeus (Appendix S1: Figure S2). Although the outcome of the recorded attacks could not be assessed because the events took place too far from the video systems, these results indicate that risk detection by prey was lower and delayed when C. crysos displayed shadowing behavior than when they did not, thus suggesting that blue runners might choose shadowing behavior to potentially enhance their hunting success. Our observations also revealed that most of the time shadowing behavior was displayed by a single individual (100% and 87% of the associations recorded by BRUV and DOV, respectively), while only in three out of 23 shadowing events two or more individuals were recorded swimming in association with a single shark (Appendix S1: Figure S1). When this occurred, we documented that C. crysos individuals competed to maintain the association, with usually one of the associating individuals attempting to chase away the others (Video S4). This evidence suggests that C. crysos might face a trade-off between hunting within a group and risking an unsuccessful predation due to increased threat detection by prey or hunting alone and take advantage by a shadowing strategy. Investigating species interactions in the field is particularly challenging due to the difficulty in tracking individual fish in open environments. Through a combination of remote and DOV sampling techniques, this study contributed to a better understanding of species interactions by documenting these in their natural habitats. Previous studies have reported fish associated with sharks to remove parasites by chafing their bodies against the skin (Papastamatiou et al., 2007; Williams et al., 2022), to reduce the risk of being predated (Sheaves et al., 2023), or to enhance access to food through opportunistic feeding strategies, where following species feed on other associated species or on feces released and matter regurgitated by the followed shark (i.e., scavenging behavior; Andrades et al., 2012; Barry et al., 2023; Dove & Robinson, 2021; Norman et al., 2021; Ovegård et al., 2022). Concealment in carangids has been previously documented with juvenile individuals using floating objects or pelagic animals, such as Fish Aggregating Devices (FADs) and jellyfish, for antipredator purposes (Bonaldo et al., 2004; Sinopoli et al., 2015). Other studies have reported associations between carangids and larger heterospecific, but the predatory purpose of the association was only hypothesized (Baird, 1993; Mendonça et al., 2011; Ormond, 1980; Sorgon et al., 2021). By reporting a rare evidence of shadowing behavior displayed by teleosts with large-body sharks, our records add on previous evidence suggesting that the size of the shadowed species is likely an important factor in triggering shadowing behavior in other fish species. However, intense target and accidental fishing has dramatically reduced pelagic shark populations (e.g., Ferretti et al., 2008), whilst a reduction of up to 42% has been recorded for the reef-associated sandbar sharks over a decade (Saidi et al., 2020) in the Mediterranean Sea. Therefore, by removing large-bodied species such as sharks, intense fishing may have decreased the availability of shadowed individuals in the region, with this potentially affecting the hunting success of non-target, following species such as C. crysos, along with making this shadowing strategy a rare event. This likely restricts the probability of observing shadowing events only to the few seasonal shark aggregations present in Mediterranean waters such as the one occurring around Lampione island (Cattano et al., 2021, 2023), offering the predators present in those waters unique opportunities to find a host individual that can fulfill the shadowed role. While our observations seem to suggest that sandbar sharks neither gain nor suffer from the association, the shadowing behavior—beside lowering threat detection ability of prey—may provide at least two additional benefits to the blue runner: (1) to gain protection and/or concealment by the shadowed species and (2) to reduce its swimming costs by enhancing hydrodynamic efficiency. Such potential benefits have been suggested by other studies reporting interspecific associations elsewhere (e.g., Sheaves et al., 2023; Sumikawa & Miyoshi, 2022), although further evidence supporting these mechanisms is needed. Shadowing species may display a high level of behavioral plasticity, choosing predatory strategy depending on the context they face (e.g., Matchette et al., 2022). Accordingly, the reef-associated blue runner C. crysos is an active predator able to display pursuit strategy, consisting of a sudden acceleration toward prey followed by a return to normal cruising speed upon leaving the area (Peterson et al., 2021; Sancho, 2000; this study), and the ambush strategy, involving either attacks on fish schools from hidden positions near the seafloor (Cermak, 2002; Sancho, 2000) or associating with a shark (this study). This behavioral plasticity in blue runners is reflected in their highly differentiated diet, which not only mostly consists of small teleosts, but also includes crustaceans (Sley et al., 2009) and zooplankton (Keenan & Benfield, 2003). Notably, also C. plumbeus is considered an opportunistic feeder whose diet changes ontogenetically shifting from small fish, crustaceans, and cephalopods in juveniles to larger prey in adults (Saidi et al., 2007), suggesting no overlaps for prey preference in the association between blue runners and sandbar sharks. Previous work also suggests that the choice of a predatory strategy could be linked to the structural complexity of the habitats or to the size of targeted prey shoals, with decreasing hunting success (i.e., increased prey vigilance) occurring in less complex habitats and with larger prey group size (Major, 1978; Polyakov et al., 2022). Shadowing behavior could allow C. crysos to avoid such increased vigilance ability of large prey groups, minimize detection, and decrease the reaction (or flight) distance of the prey. Future studies should describe how associating with large-sized sharks benefit C. crysos in terms of predation success and energy expenditure, and whether such association may affect the shadowed species. Evaluating cost/benefits of this behavior for the shadowing and the shadowed species can contribute to understanding the evolution of alternative predatory strategies and the ecological context in which they occur. In summary, remote and DOVs revealed that hunting C. crysos may display an alternative predatory strategy by associating with sharks to conceal themselves and potentially increase their attack success toward prey shoals. Our findings highlight the importance of shark aggregations for studying how the presence of large high-level predators may foster new species interactions and increase different biodiversity facets, thus potentially influencing community structure and function. The sandbar shark aggregation around Lampione island is a transient phenomenon that may introduce or modify species associations. In this regard, studying communities and species interactions in this location and in other high-level predator aggregation sites may shed light on the ecological importance of species showing spatial and temporal transience, such as many sharks. Carlo Cattano, Desiree Grancagnolo, Giorgio Aglieri, Gabriele Turco and Marco Milazzo collected data. Carlo Cattano, Fabio Badalamenti, Marco Milazzo provided expert insight into data interpretation. Desiree Grancagnolo analyzed data and created figures. Carlo Cattano conceived the study and composed the manuscript. All coauthors contributed to the final version of the manuscript. We thank Rocco Canella of the diving center Pelagos 2.0 and the staff of the Pelagie Island Marine Protected Area for the support in field surveys. This study was supported by the National Geographic Society through a grant to Carlo Cattano (grant number: EC-85788C-21) and by the Blue Marine Foundation through two projects funded to Carlo Cattano (projects Shark Noise: C75F22000030007 and PRESTO: C73C23000300007). Gabriele Turco was funded by the National Recovery and Resilience Plan, Mission 4 Component 2 Investment 1.4 – Call for tender no. 3138 (16/12/2021) rectified by decree no. 3175 (18/12/2021) of the Italian Ministry of University and Research funded by the NextGenerationEU; project CN_00000033, concession decree no. 1034 (17/6/2022) adopted by the Italian Ministry of University and Research, CUP B73C22000790001, project “National Biodiversity Future Center-NBFC. The authors declare no conflicts of interest. Data (Cattano et al., 2025) are available in Zenodo at https://doi.org/10.5281/zenodo.14713984. Appendix S1. Video S1. Video S1 Metadata. Video S2. Video S2 Metadata. Video S3. Video S3 Metadata. Video S4. Video S4 Metadata. Video S5. Video S5 Metadata. Video S6. Video S6 Metadata. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.