Predation on Pelagic Coelenterates: a Review

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Predation on Pelagic Coelenterates: a Review J. Mar. Biol. Ass. U.K. (2005), 85, 523–536 Printed in the United Kingdom REVIEW Predation on pelagic coelenterates: a review Mary Needler Arai Pacific Biological Station, 3190 Hammond Bay Road, Nanaimo, British Columbia, Canada, V9T 6N7; and Department of Biological Sciences, University of Calgary, 2500 University Drive N.W., Calgary, Alberta, Canada, T2N 1N4. E-mail: [email protected] Coelenterates (cnidaria and ctenophores) are well recognized as predators in food webs of marine ecosystems but are less often considered as prey. This is partly because they are digested very rapid- ly. In studies based on predator stomach contents the measured masses of different prey organisms are rarely scaled by their relative rates of digestion. Predators that are frozen and thawed, or for which whole stomachs are placed in preservatives, may have already lost much of their coelenterate content when they are examined. There is also a tendency to assume that gelatinous organisms, with their high water and salt content relative to organic content, are poor food. However, given the high rates of digestion (and presumably of assimilation) coelenterates may provide sources of energy com- parable to better recognized prey such as arthropods. It is already becoming well documented that a number of cnidaria and ctenophores as well as fish utilize gelatinous organisms as prey. Data is accumulating more slowly on predation by a wide range of other carnivores such as molluscs, arthro- pods, reptiles and birds. INTRODUCTION feeding on macroscopic animals, although some uti- lize microzooplankton, near surface forms may pos- The ecology of pelagic coelenterates (Cnidaria and sess symbionts, and a few have been shown to take up Ctenophora) has been more extensively investigated in dissolved organic material (DOM) directly (Arai, recent years. In spite of their fragility they are now 1997b). They are not, however, generally recognized well recognized by marine zoologists as including a as prey. A typical comment is that by Sommer et al. significant biomass especially under bloom conditions. Abundant forms in the neuston of the tropics and tem- (2002); ‘Gelatinous zooplankton are usually consid- perate zones are the hydrozoan chondrophores such ered a dead end in the pelagic food web because their as Velella and siphonophores. These may project part- low nutritional value makes them a minor food item ly into the air and form pleustonic rafts that are pas- for vertebrates, although there are some minor excep- sively transported by winds. The oceanic water col- tions (e.g. the moon fish Mola mola and sea turtles).’ umn includes holoplanktonic Hydrozoa (tra- Coelenterates are indeed depicted incorrectly as dead chymedusae, narcomedusae, and siphonophores) as ends in their paper on pelagic food web configura- well as coronate Scyphozoa and Ctenophora. To these tions. In fact there is already information in the litera- in neritic areas are added species with benthic stages ture showing that coelenterates are not dead ends and in the life cycle such as anthomedusan and leptome- are preyed on by a number of types of animals as will dusan Hydrozoa and semaeostome and rhizostome be described below. Scyphozoa. The pelagic larvae of Anthozoa such as The most extensive data on predators to date are for corals and Ceriantharia may contribute significant other coelenterates and fish. The former was reviewed biomass locally. Most ctenophores are holoplanktonic by Purcell (1991a) and the latter by Ates (1988) and and may be abundant both inshore and offshore. In Arai (1988) and by Purcell & Arai (2001). The present spite of their abundance the recognized involvement review updates the data on coelenterates and fish and of these coelenterates in pelagic food webs is not well also presents evidence for other groups such as mol- balanced. Their role as important predators on luscs, arthropods, reptiles and birds. marine animals such as other coelenterates, arthro- Although there may be visual observations such as pods and larval fish has been extensively investigated those of Mola mola (Linnaeus, 1758) and turtles referred and reviewed (Arai, 1988, 1997a,b; Purcell, 1991, to by Sommer et al. (2002), most quantitative data 1997). Most are primarily documented as carnivores comes from investigations of stomach contents of the Journal of the Marine Biological Association of the United Kingdom (2005) 524 M.N. Arai Predation on pelagic coelenterates predator. These stomach contents are seldom scaled for coelenterates at the bottom of the water column (Fautin comparative digestion rates as they logically should be. & Fitt, 1991). Larvae of sea anemones such as Edwardsia Even if stomachs are examined immediately the diet lineata (Verrill, 1874) and Peachia quinquecapitata proportions of animals without resistant structures are McMurrich, 1913 which infest ctenophores and underestimated. In addition predators are often stored medusae may feed only on the ingested food of the host by methods such as freeezing or fixation of whole fish or directly on the host tissue (Mills, 1993; Bumann & which allow loss of soft tissues before observations are Puls, 1996). Finally the beroid ctenophores prey prima- made. In a few cases relatively resistant structures of rily on other ctenophores and the cydippid ctenophore coelenterates such as the ctenes of Ctenophora, the Haeckelia feeds on narcomedusae (Purcell, 1997). cnidae of Cnidaria or the sails of the Chondrophora Semaeostome scyphomedusae eat a broad range of may be examined. plankton including fish and arthropods but also gelati- Also, as in the quote, it is often considered that gelat- nous prey such as other scyphomedusae, hydrome- inous animals can be ignored since they might consti- dusae and ctenophores (Purcell, 1997). They may have tute poor diets because of the low ratio of organic major effects on the populations of some common coe- material to salt and water. The energy contents of coe- lenterate prey even when the prey has responses that lenterates with large amounts of mesogloea have been allow a portion of them to escape. Chrysaora quinquecirrha difficult to measure accurately due to the high amount (Desor, 1848) can eliminate the ctenophore Mnemiopsis of salt and hence of bound water (Arai, 1997a). leidyi A. Agassiz, 1865 from tributaries of Chesapeake Typically they are reported with calorimetric values Bay even though adult M. leidyi can often increase per unit of wet weight which are less than 20% of swimming speed and escape with some loss of tissue those of arthropods (Arai, 1988; Davis et al., 1998). (Purcell & Cowan, 1995; Kreps et al., 1997). Some On the other hand if two prey items of the same wet semaeostomes are able to prey on other semaeostomes weight are compared this low energy content of the even though they may have developed escape respons- coelenterates may be compensated for by higher rates es. Cyanea capillata (Linnaeus, 1758) can capture Aurelia of digestion (and presumably assimilation) of gelati- aurita (Linnaeus, 1758) of the same or smaller size even nous animals. This has been shown for chum salmon, when the prey changes direction and swims faster Oncorhynchus keta (Walbaum, 1792), feeding on the (Bamstedt et al., 1994; Hansson, 1997). Similarly ctenophore Pleurobrachia or on the same wet weight of Phacellophora camtschatica Brandt, 1835 can only catch shrimp, where rate of ctenophore digestion exceeded Aurelia of smaller size than the predator (Strand & shrimp by over 20 times (Arai et al., 2003). Provided Hamner, 1988). the fish has a good supply of prey to process at this Some coelenterates are dependent on other coelen- high rate, the Pleurobrachia provide a good diet. Similar terate prey for particular compounds or structures. measurements need to be repeated on a number of Aurelia aurita ephyrae can be raised on diets of Artemia predator–coelenterate prey combinations. nauplii or mixed zooplankton. Cyanea capillata ephyrae, however, require gelatinous prey such as the ctenophore Bolinopsis infundibulum (O.F. Muller, 1776), PREDATORS OF PELAGIC Aurelia, or the hydromedusa Phialella even though the COELENTERATES adults have a much broader diet (Bamstedt et al., 1997). Aequorea victoria (Murbach & Shearer, 1902) requires a Cnidaria and Ctenophora diet including coelenterazine from other luminescent One important group of predators on pelagic coelen- medusae or ctenophores in order to produce biolumi- terates which has been reviewed by other authors is that nescence (Haddock et al., 2001). The ctenophore of other coelenterates (Purcell, 1991a, 1997). Included Haeckelia rubra (Kolliker, 1853) incorporates cnidae from among the hydromedusan predators are such pandeid narcomedusan prey into their own tentacles (Carre et anthomedusae as Stomotoca, leptomedusae such as al., 1989). Aequorea, and narcomedusae such as Solmissus (Arai & There may be fairly complex food webs even within Jacobs, 1980; Larson et al., 1989; Purcell, 1991b; the coelenterate community of a single bay such as Raskoff, 2002). Apolemia uvaria (Leseuer, 1815) is an Departure Bay, British Columbia (Arai & Jacobs, unusual siphonophore in that it consumes a significant 1980). Predation may be size dependent so that the amount of gelatinous prey including hydromedusae roles of predator and prey may interchange and add to and ctenophores (Purcell, 1981). As discussed below the complexity. For example, adults of the hydrome- many Scyphozoa prey on other scyphomedusae and on dusa Aequorea victoria eat adult Clytia gregaria (L. Agassiz,
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