Conspecific alarm cues are a potential effective barrier to regulate foraging behavior of the sea urchin Mesocentrotus nudus

Highlights

• Alarm cues are a candidate tool to prevent Mesocentrotus nudus from foraging.

• Alarm cues stopped sea urchins from feeding on the kelp.

• Alarm cues did not affect the capability of sea urchins to grasp the kelp.

• Alarm cues are an application potential in field.

Abstract

A cost-effective approach to controlling foraging and feeding behaviors of sea urchins is essential for the management of kelp beds. Laboratory experiments were designed to investigate whether alarm cues from crushed conspecific urchins can effectively prevent the foraging and feeding behaviors of the sea urchin Mesocentrotus nudus under the static seawater condition. The present study found that the number of M. nudus that foraged successfully was significantly lower when alarm cues were placed between the kelp and the sea urchins. This result indicates that alarm cues could play an important role in critical kelp-bed areas. It probably prevents sea urchins from foraging by acting as a barrier. Further, we found that alarm cues around the kelp significantly affected foraging behavior of M. nudus, indicating that the alarm cues around the kelp are a potential effective way to prevent sea urchins from foraging for the kelp. In addition, the number of sea urchins that stopped feeding was significantly higher in the group in the presence of alarm cues than that in the control group. This indicates that alarm cues may have an application in stopping sea urchins from feeding. However, there was no significant difference of Aristotle's lantern reflex between the groups with and without alarm cues. These results indicate that alarm cues greatly affect foraging behavior, but not Aristotle's lantern reflex of M. nudus. All together, the present study suggests that alarm cues have an application potential in the management of the kelp beds as green engineering. Future studies are essential to further investigate the chemical basis of the alarm cues of sea urchins for the application in large-scale.

Introduction

Kelp beds not only provide food and shelter for many marine invertebrates, but purify the pollutants in seawater and thus play an important role in marine ecosystems (Steneck et al., 2002; Ling, 2008). Kelp beds are greatly threatened by storm activity (Filbee-Dexter and Scheibling, 2014; Glasby and Gibson, 2020), environmental changes (Ling et al., 2008; Byrne and Hernández, 2020) and grazed by herbivores (Valentine and Johnson, 2005; Gabara et al., 2020). Overgrazing by sea urchins is the most important reason for a phase shift from productive kelp beds to barrens with a great decline in primary productivity and habitat structural complexity (Filbee-Dexter and Scheibling, 2014; Ling et al., 2019). Exclusion of sea urchins would be an effective approach to managing kelp beds that overgrazed by sea urchins (Poore et al., 2012). Techniques for excluding sea urchins include physical removal by divers (Ling et al., 2010; Sanderson et al., 2016) and the use of quicklime (Leighton et al., 1966). Recently, Ling et al. (2020) established an effective method to suppress the overgrazing of kelp by sea urchins using the octocoral Erythropodium hicksoni as a natural biological barrier. It is, however, not generally available in the ocean. Thus, an effective approach to suppressing the overgrazing of sea urchins is essential for the management of kelp beds.

Foraging behavior is the process by which sea urchins use their tube feet to detect chemicals released from the kelp and move towards the kelp (Pisut, 2004). Feeding is the behavioral response of sea urchins to use their teeth in the Aristotle's lantern to grasp and ingest the kelp (Brothers and McClintock, 2015). Consumption of kelp using the teeth transforms kelp beds into urchin barrens (Pearse, 2006; Ling et al., 2015; Agatsuma et al., 2019). Thus, suppressing foraging and feeding behaviors is critical to managing the kelp beds that endangered by sea urchins. Sea urchins sense alarm cues from the extracts of crushed individuals, although the chemical basis remains unknown (Parker and Shulman, 1986). The emergence of alarm cues causes various behavioral reactions of sea urchins, for example, cryptic behavior (Spyksma et al., 2017) and aggregative behavior (Kintzing and Butler, 2014). Interestingly, obvious escape behavior was observed in the sea urchin Mesocentrotus nudus exposed to the crushed individuals in field (Zhadan and Vaschenko, 2019). It is reasonable to hypothesize that alarm cues have an application potential in suppressing the foraging and subsequent feeding responses of M. nudus.

Mesocentrotus nudus of test diameter ˃20 mm graze the attached kelp destructively, resulting in the transition of kelp beds to barrens (Agatsuma et al., 2019). It is thus of interest to investigate whether alarm cues can exclude M. nudus from kelp beds by acting as a barrier. Whether alarm cues appearing around the kelp prevent sea urchins from foraging is unknown. Further, it is unknown whether alarm cues cause emigration of sea urchins that are feeding on the kelp, although it is reasonable to hypothesize any foraging responses. A full understanding of foraging and feeding responses to alarm cues would help establish an effective approach for the management of kelp beds.

The main purposes of the present study are to investigate: 1) whether alarm cues placed in areas to the kelp are an effective barrier that prevents M. nudus from foraging; 2) whether alarm cues placed around kelp prevent foraging behavior of M. nudus; 3) whether M. nudus stop foraging on kelp or continue escaping; 4) whether alarm cues cause emigration of M. nudus that are feeding on the kelp; 5) whether alarm cues have significant effects on the Aristotle's lantern reflex of M. nudus.