Chemical cues and energy cost associated with the induction of anti-predatory responses in the green-lipped mussel perna viridis

Abstract

Aquatic animals are known to perceive and assess the risk of predation by means of chemical cues which are either released from predators, or from prey that have either been captured or injured. The ability to develop adaptive responses to increase resistance against predators is crucial; failure to avoid a predator can be lethal. The green-lipped mussel Perna viridis is a tropical and subtropical species distributed widely in Asia and plays a crucial role in structuring intertidal communities. It is susceptible to predators such as crabs and muricid gastropods. The present study investigated the inducible anti-predator responses of P. viridis, upon exposure to different types of chemical cues and the energy cost associated with these responses. Byssal threads are strong proteinaceous fibres which are secreted by the byssal gland of the mussel. They are essential to a mussel’s defence against predation; an increase in the attachment strength can effectively reduce dislodgement by predators. A laboratory experiment was conducted to investigate the byssal thread production by juvenile P. viridis in response to waterborne cues from damaged conspecifics or damaged heterospecifics from the black mussel Brachidontes variabilis. The byssal thread production and the mobility of the mussels were studied for 96 hours. P. viridis which was exposed to damaged conspecifics produced the thickest (27.3% thicker than control) and longest (21.7% longer than control) byssal threads and were followed by those exposed to damaged heterospecifics with values being 23.1% and 15.5% higher, as compared to the control. The byssus volume increased by 133.6% and 60.0% in the damaged conspecific and damaged heterospecific treatments, respectively. P. viridis exposed to the damaged conspecifc cues also had higher mobility. Results showed that P. viridis is able to differentiate different damage-released chemical cues and respond according to its associated risk level. The finding that damaged heterospecific cues can trigger anti-predator response in mussels by adjusting its byssus production is novel. Most of the studies on anti-predator responses in mussels and other aquatic animals were laboratory experiments; rarely have such experiments been performed in the field, despite the fact that the results achieved there would be more ecologically relevant. P. viridis was exposed to the predatory crab Thalamita sima, in the field for 48 hours and byssal thread production was examined and compared with those exposed to either deposit-feeding gastropods or the control, without any cues. It was the first time a field study on this topic was undertaken in subtropical waters. Although considerably lower magnitude of responses was found in the field, this study has verified that P. viridis, in both laboratory and field conditions, produced longer and thicker byssal threads when they were exposed to predators as compared with other treatment groups. Caution should be exercised when making predictions based on laboratory experiments. More ecologically relevant, field-manipulated experiments are recommended for the future. Forming clumps is one of the behavioural features of mussels. Early studies have shown that mussels at the centre of a clump suffer lower predation than those at the edge. However, their growth and reproduction are also reduced when compared with mussels either located at the edge of a clump or that are solitary. The location of the mussels may determine the extent of the anti-predator responses, which is induced upon exposure to predation-related chemical cues. The hypothesis was tested in a laboratory experiment with clumping behaviour and byssal thread production of juvenile P. viridis being investigated in response to waterborne cues from damaged conspecifics or damaged heterospecifics, B. variabilis. The formation of clumps was monitored for 48 hours, and the byssal thread production of mussels located at various positions on and in the clumps was determined at the end of the experiment. The results did not reveal any evidence of the induction of clumping behaviour by damaged alarm signals. Instead, solitary mussels and those found at the edges of the clumps in the damaged conspecific treatment produced significantly more byssal threads, which were twice and 39.8%, respectively more than those located within the clumps. A similar trend was observed in the length of byssal threads in which solitary mussels and edge mussels produced 22.7% and 16.0% longer, respectively, threads than the mussels located within the clumps. In addition, the results showed that mussels exposed to broken green mussels produced the greatest volume, the highest number and longest byssal threads, over mussels in other treatments, irrespective of their spatial positions. The results coincided with the hypothesis that the level of anti-predator response elicited by mussels is determined by the spatial position of the mussels in the clump. Scope for growth (SFG), which represents the energy available for growth and reproduction after maintenance requirements are met, was employed to determine and quantify the cost of anti-predator responses to P. viridis. Physiological responses, including absorption efficiency, clearance rate, excretion rate and respiration rate were measured for mussels exposed to chemical cues from damaged conspecifics or predators feeding on different prey over a two-week period. Lower clearance rate and absorption efficiency were observed in P. viridis exposed to unfed crabs or crabs feeding on conspecific mussels. A decrease in the clearance rate and an increase in the respiration rate were also observed for P. viridis exposed to damaged conspecifics. Subsequently, a 62.8% and 58.6% reduction in the SFG was found for treatments with unfed crabs or crabs feeding on conspecific mussels, respectively, as compared to the control. The results suggest that there is an apparent fitnesss cost involved in the induction of anti-predator responses. Growth potential of P. viridis may be severly reduced under predation risk in view of the trade-offs between investments in inducible defences and energy acquisition. This sub-lethal effect not only affects the growth rate and population dynamics of P. viridis but may cascade through the phytoplankton abundance, altering the food web structure.