Prey naiveté to invasive lionfish Pterois volitans on Caribbean coral reefs

Abstract

Native prey can be particularly vulnerable to consumption by exotic predators. Prey naiveté, the failure to recognize a novel predator due to lack of recent co-evolutionary history, likely facilitates the disproportionate impact that some exotic predators exert on prey populations. Lionfish Pterois volitans, exotic predators from the Pacific, have invaded coral reefs and other coastal habitats along the western Atlantic. Prey naiveté towards novel lionfish was tested in field experiments and with observations using closest approach distance as the anti-predator response. We quantified the distance of prey fishes to exotic lionfish in both the Atlantic and Pacific (invasive and native ranges of lionfish) as well as to native predators in the Atlantic. In the Atlantic, experiments indicated that Haemulon plumierii, prey of lionfish, generally display a closer approach distance to exotic than to native predators, and field observations of free-ranging fish revealed that at least 5 other species of small fishes (Halichoeres bivitattus, Halichoeres garnoti, Scarus taeniopterus, Stegastes leucostictus and Thalassoma bifasciatum) also might exhibit limited predatoravoidance behaviour towards invasive lionfish. We also found that 3 families of small fish (Labridae, Pomacentridae and Scaridae) maintained greater distances from lionfish in the Pacific compared with the Atlantic in both experimental and field observations. These results suggest prey naiveté to exotic lionfish by at least 8 species of fish (Abudefduf saxatilis, H. plumierii, H. bivitattus, H. garnoti, S. taeniopterus, Sparisoma aurofrenatum, S. leucostictus and T. bifasciatum) in the Atlantic, which could be contributing to the rapid expansion of this invasive species by enhancing its fitness and reproductive output through high predation efficiency.

Trait‐mediated foraging drives patterns of selective predation by native and invasive coral‐reef fishes

“…In particular, many authors have surmised that the na€ ıve prey hypothesis-in which native species do not recognize the threat posed by the lionfish's unique appearance and stalking behavior and fail to evade approaches by themexplains the high rates of native prey consumption by lionfish in the invaded range (Albins and Hixon 2013, Côt e and Maljkovi c 2010, Cure et al 2012, Côt e et al 2013a, Marsh-Hunkin et al 2013, Black et al 2014, Kindinger 2015, Anton et al 2016, Eaton et al 2016, Benkwitt 2017. In particular, many authors have surmised that the na€ ıve prey hypothesis-in which native species do not recognize the threat posed by the lionfish's unique appearance and stalking behavior and fail to evade approaches by themexplains the high rates of native prey consumption by lionfish in the invaded range (Albins and Hixon 2013, Côt e and Maljkovi c 2010, Cure et al 2012, Côt e et al 2013a, Marsh-Hunkin et al 2013, Black et al 2014, Kindinger 2015, Anton et al 2016, Eaton et al 2016, Benkwitt 2017.…”

“…Our observations also allowed us to evaluate assumptions about behavioral mechanisms that may have facilitated the success of invasive Indo-Pacific lionfish in the broader Caribbean region. In particular, many authors have surmised that the na€ ıve prey hypothesis-in which native species do not recognize the threat posed by the lionfish's unique appearance and stalking behavior and fail to evade approaches by themexplains the high rates of native prey consumption by lionfish in the invaded range (Albins and Hixon 2013, Côt e and Maljkovi c 2010, Cure et al 2012, Côt e et al 2013a, Marsh-Hunkin et al 2013, Black et al 2014, Kindinger 2015, Anton et al 2016, Eaton et al 2016, Benkwitt 2017. However, our observations suggest that prey respond as appropriately to this non-native predator as they do to native piscivores, given that encounter rates (i.e., prey within a distance at which a successful strike could be made) with lionfish across prey types were quite ordinary in comparison with the two native predators we observed (All prey species we studied have been identified in lionfish's diet in the invaded range; Albins and Hixon 2013, Morris and Akins 2009, Muñoz et al 2011, Layman and Allgeier 2012, Côt e et al 2013a, b, Dahl and Patterson 2014, Eddy et al 2016, Harms-Tuohy et al 2016.…”

Invasive predator tips the balance of symmetrical competition between native coral‐reef fishes

“…A lack of evolutionary history with invasive predators can also result in suboptimal antipredator response by native prey (i.e., prey naivete; Diamond and Case 1986, Cox and Lima 2006, Freeman and Byers 2006. Lionfish is an invasive species that also uses a unique hunting strategy (Albins and Lyons 2012), and the extent of naivete appears to vary among native prey fishes in the presence of this novel predator (Marsh-Hunkin et al 2013, Black et al 2014, Kindinger 2015, Anton et al 2016, Eaton et al 2016. Naivete could vary between native basslet species, however, a lack of evolutionary history between predator and prey per se cannot independently explain differential predation within prey species (i.e., among size classes).…”

The lionfish Pterois sp. invasion: Has the worst‐case scenario come to pass?

“…the lack of adaptive responses by prey exposed to a novel predator (Sih et al, 2010). A number of methods have been used to assess the naïveté of Atlantic prey fishes to lionfish, from observations of fish on natural and artificial reefs (Albins & Hixon, 2008;Côté & Maljković, 2010;Anton et al, 2016;Benkwitt, 2017), to field presentations to prey of predators and non-predators in cages and bottles (Black et al, 2014;Kindinger, 2015;Anton et al, 2016) and various laboratory experiments that confront prey with visual or chemical cues of predators and non-predators (Marsh-Hunkin et al, 2013;Eaton et al, 2016). The prey responses measured are equally varied and range from behaviours expected to change under risk of predation (e.g.…”