Paper: Black, A.N., S.R. Weimann, V.E. Imhoff, M.L. Richter, and M. Itzkowitz. 2014. A differential prey response to invasive lionfish, Pterois volitans: Prey naiveté and risk-sensitive courtship. Journal of Experimental Marine Biology and Ecology 460: 1-7. DOI:10.1016/j.jembe.2014.06.002
This story sounds a lot like a bad high school romance. You see your crush across the hall! Do you make a move? You have to scope out the scene first! If she’s alone, go for it! What if there’s another guy nearby? He’s not even her type, but you know from rumors that he likes to pick fights and you know you’d lose. You should just hang back and wait until tomorrow. But come tomorrow, the new guy is hanging around her. You don’t know much about him and know you’d never win a fight against him. But, he may not be a that big a threat and you’re convinced that this girl is the one for you… Do you take that risk for love? If you were a Beaugregory Damselfish, you would!
Many of you have probably heard of the lionfish invasion in the Northern Atlantic Ocean and the Caribbean. These predatory fish are beautiful but deadly. In their invaded range, their populations are increasing rapidly, while native coral reef fish populations are declining. Lionfish (and other invasive predators) are so effective at capturing and consuming prey and reproducing for a number of reasons, including lack of predators, competitors, parasites, and prey naiveté. Prey naiveté refers to a state in which prey species do not recognize the new predator on the block as a threat, making them easy targets. Lionfish are novel in Caribbean reef habitats due to their unique coloration and movement, their elongated fins which they use to corral prey, and the way they focus jets of water to confuse their prey (https://www.youtube.com/watch?v=zVglFQBej60). They are such a foreign concept that the locals just don’t know what to make of them. Unfortunately, the inability to recognize lionfish as a danger makes some coral reef fish highly vulnerable to predation.
Organisms evolved to behave in ways that maximize their fitness—their ability to survive and reproduce. Predation removes the chance of reproducing in future, so many species have evolved to minimize risky behaviors in the face of predation. They may increase their use of refuges, group together, or minimize movement. During reproduction, animals are especially at risk of predation due to increased coloration or conspicuous courtship displays, for example. When organisms reduce their risk by halting any reproductive behaviors, they exhibit what is known as risk-sensitive courtship. But reducing reproductive behaviors has a fitness cost too as it may lead to missed opportunities to create progeny. To know whether they should avoid courtship behavior, they must first be able to recognize whether a predator is present or not. In the case of invasive predators, the prey may not know that they should stay safe at home rather than going on a date. Or, they may believe that love is worth the risk.
The Study and Findings
Researchers decided to examine what role prey naiveté and risk-sensitive courtship play in the interactions between lionfish (Pterois volitans) and the beaugregory damselfish (Stegastes leucostictus), a common prey item for lionfish.
The research team conducted their studies in Discovery Bay, Jamaica, where lionfish have been present since 2008. They created standardized artificial nest sites that males quickly claimed and began defending as their territories. Males at these artificial breeding sites were exposed to various combinations of stimuli and their behaviors recorded to determine 1) normal anti-predator behavior, 2) whether they recognize lionfish as a predator, and 3) whether they exhibit risk-sensitive courtship in the presence of native predators or lionfish.
Among the native predators damselfish face is one called the sand diver (Synodus intermedius)—a sit-and-wait predator. Since damselfish recognize sand divers as predators, their behavior when shown one was recorded. For comparison, they were also shown a herbivorous fish, the parrotfish Scarus taeniopterus. Stimuli fish were placed in clear containers with holes in the end so that chemical cues could be detected by the prey. The tube was 0.3 m from the damselfish’s territory. Researchers recorded the amount of time spent in refuges and how much time they spent within a body length of the stimulus fish, referred to as intruder proximity and indicative of active territorial defense. Since time spent in refuge was always greater than close to an intruder, they subtracted intruder proximity time from time spent in refuge to generate a “mean difference score”. Higher mean difference scores indicate more time spent hiding and less defending their territory. They found that the male damselfish spent much more time hiding when a sand diver was nearby than when a parrotfish was (Fig. 1).
For this part of the study, the male damselfish were exposed to four different types of stimuli: small sand diver, large sand diver, small lionfish, or large lionfish. Different size classes represent varying degrees of threat. Bigger fish are more threatening! The same behaviors were recorded and the same mean difference score was used to indicate time spent hiding versus defending the territory. The damselfish must recognize lionfish as predators since they behave similarly in their presence as they do when facing native sand divers. As predicted, they hide more from larger predators, regardless of species (Fig. 2). Prey species can learn that lionfish are predators and respond to the threat.
To determine how the males behave when love is on the line, the team added a female beaugregory damselfish in a separate clear container to the stimulus groups, now 1) a female with a sand diver (small and large), 2) a female with a lionfish (small and large), 3) a female only—which will show the response of males to a female presence when there is no predation risk. The researchers still examined time spent in a refuge and intruder proximity to calculate a mean difference score, but they added female proximity (time spent within one body length of the female), number of “dips” (a display behavior) performed, number of calls and time spent calling to females.
What they found is very interesting. Males exhibit risk sensitive courtship by hiding more and minimizing reproductive behaviors when facing a sand diver, regardless of its size. They protect themselves and their ability to have offspring in the future. However, even recognizing lionfish as a danger, the males do not spend nearly as much time hiding as when faced with sand divers (Fig 3). They even still engage in similar levels of courtship activity—similar time near females (Fig 4), number of dips, chirps, and time spent chirping—when courting a female without any predators around as they do when lionfish are present. Therefore, male damselfish do diminish their reproductive activities in response to the native predator, but strangely, not in response to the invasive one.
Damselfish are not naïve prey. They do recognize lionfish as a potential predator and behave accordingly. They spend more time in refuge to protect themselves and secure their survival… unless of course, there’s a female involved. When faced with a known predator, the sand diver, they exhibit that risk-sensitive courtship behavior as predicted. Rather than spending time near the female or displaying and vocalizing to impress her, they protect themselves by hiding from the sand diver. By engaging in this risk-sensitive behavior, these males not only reduce their risk of predation (good for them) but also their reproductive success (not so good). That pattern is reversed when faced with the invasive lionfish. Male damselfish expose themselves to greater predation risk to better their chances of reproductive success. The “why” is a question for future studies. Maybe it takes a different degree of knowing a threat exists to override the drive to reproduce than it does if you don’t really have anywhere to go? What this study does show is important. It identifies another possible reason for the success of the lionfish invasion: vulnerability during reproductive behavior. (My input: that vulnerability applies to both the males and females and without containers may have dire consequences for both.) However, it also provides hope that prey fish may learn to recognize an invasive predator as a threat.