Prey-specific encounter rates and handling efficiencies as causes of prey selectivity in ambush-feeding hydromedusae

We examined the foraging process in the jellyfish Sarsia tubulosa feeding on three types of prey: cirripede nauplii, cypris larvae, and Acartia tonsa copepodites. Clearance rate was used as measure of prey selectivity. To estimate maximal clearance rate (Fmax), we used a predictive encounter model with input parameters quantified from video observations. Both encounter rate and handling efficiency were important in determining Fmax. Encounter volume rate was three times higher for cirripede nauplii than for copepodites, but sequential handling was 10 times more efficient for copepodites than for cirripede larvae. Two critical steps in the postcapture feeding process—capture of encountered prey with the tentacle, and mouth attachment to the captured prey—created a clear selectivity for copepods over barnacle larvae. Predicted values were close to laboratory measurements of Fmax, and for cirripede nauplii also to field-estimated Fmax. We suggest that species-specific handling efficiency is the main factor creating trophic niche separation in the large functional group of ambush-feeding hydromedusae. Highly specific behavior, physiology, and morphology have evolved in many predators to allow predation on specifically targeted prey. Specialization on certain target prey results in prey selectivity, i.e., the preferential uptake of some prey types over others from a mixed composition of potential prey. Comparisons of prey composition in the water and of composition of ingested prey have revealed that jellyfish of the classes Scyphozoa and Hydrozoa are selective feeders (Larson 1987; Purcell 1997; Purcell and Sturdevant 2001). Because jellyfish populations can bloom and locally have increased in density in recent years (Mills 2001), there is a need to acquire a quantitative understanding of their selectivity for different prey in order to predict their impact on different prey populations. A mechanistic understanding of the encounter and handling processes leading to prey selectivity in jellyfish is largely lacking. On the basis of morphological and behavioral generalizations, jellyfish are sometimes classified into one of two functional groups: (1) cruising predators that actively create feeding currents that bring prey organisms in contact with the tentacles or other nematocyst-bearing capture organs, and (2) ambush predators that deploy their tentacles and rely on prey to swim into contact with the tentacles for capture. Hydrozoa is the class with highest jellyfish species diversity, and jellyfish from this class can form blooms of several hundred individuals m23 (Fulton and Wear 1985; Pagès et al. 1996). Costello and Colin (2002) found that cruising hydromedusa species overlapped their diets of softbodied prey whereas ambush-feeding hydromedusae displayed a predator-specific selectivity for certain crustaceans or ciliated prey. In ambush-feeding jellyfish, prey selectivity is not related to prey behaviors vis-à-vis entrainment currents generated by the predator, but may arise from prey-specific differences in probability of encounter generated by the prey and from prey-specific differences in postencounter prey handling efficiency. However, the relative effects of the different processes involved in the capture and ingestion of different prey are presently not known for this large functional group of pelagic predators. Sarsia tubulosa is an ambush-feeding hydromedusa that has been reported from northern Atlantic and northern Pacific coastal waters in spring and early summer (Russell 1953). This jellyfish feeds primarily on crustacean plankton such as copepods and barnacle larvae (Lebour 1922; Costello and Colin 2002). The general feeding behavior of Sarsia tubulosa is typical of an ambush-feeding jellyfish, and has been extensively described by Hernande and Passano (1967) and Passano (1973). With the exception of intermittent swimming this medusa fishes motionless with its four tentacles extended. A motile prey that swims into contact with one of the fishing tentacles triggers nematocyst discharge and contraction of the fishing tentacle. The nematocysts of Sarsia tubulosa are believed to be specialized toward capture and retention of crustacean prey. The tentacles of this jellyfish contain a battery of desmoneme and stenotele nematocysts that adhere to the exoskeleton of the prey, and thus anchor prey to the tentacle (Purcell and Mills 1988). After capture, the catcher tentacle bends inward toward the center, and contact between the mouth on the distal end of the long manubrium and the captured prey is established. As prey is engulfed by the mouth it is also released from the tentacle that moves back into fishing posture. Prey is digested within the gut. In this study, we use Sarsia tubulosa as a model organism to examine to what extent prey encounter rates and handling efficiency affect predation rate in an ambushfeeding medusa. For different prey, we compare predicted 1 Corresponding author ([email protected]). Acknowledgments We thank Limfjordsamterne for their valuable help in collecting experimental animals. This work formed part of the EUROGEL project (EVK3-CT-2002-00074) supported by the European Commission. Funding for the project was also provided by grant 9801391 from the Danish Natural Science Council to T.K. Limnol. Oceanogr., 51(4), 2006, 1849–1858 E 2006, by the American Society of Limnology and Oceanography, Inc.