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Ihnol. Oceanogr., 43(5), 1998, 763-768 0 1998, by the American Society of Limnology and Oceanography, Inc. Minireview: The importance of benthic-pelagic life cycles in coastal aquatic systems coupling and the forgotten role of Nancy H. Marcus Department of Oceanography, Florida State University, Tallahassee, Florida 32306 Ferdinand0 Boer-o Dipartimento di Biologia e Stazione di Biologia Marina, CoNISMa, Universita di Lecce, 73100 Lecce, Italy Abstract The classical models of production and plankton community dynamics in coastal waters include an important role for benthic-pelagic coupling in the form of biogcochemical cycling (the turnover of nutrients in the form of either living matter or its decomposed constituents). We think, however, that biogeochemical explanations of ecosystem functioning underrepresent the actual complexity of the studied phenomena. We suggest that models will be more complete if they incorporate life-cycle patterns of planktonic and benthic organisms. The inclusion of such biological information into an ecological context will enhance the understanding of ecological patterns of global importance. What we presently know provides compelling evidence that new research directions, ranging from sedimentology to systematics and from physiology to molecular biology, are needed. Coastal regions are among the most productive ecosystems in the world. Benthic-pelagic coupling, which refers to the linkages between benthic and pelagic environments in aquatic systems, plays a major role (along with terrigenous input and upwelling) in determining the production and biological structure of these aquatic systems (e.g. Sommer 1989; Valiela 1995). Most studies of benthic-pelagic coupling, however, have only focused on how energy flow and fluxes of organic matter and nutrients affect production and community structure (e.g. reviewed by Graf 1992). The classical scenario begins with the resuspension of nutrients from the seabed into the photic zone, perhaps owing to a storm event (e.g. Dagg 1988; Nielsen and Kiorboe 1991). The nutrients stimulate bacterial and phytoplankton production, which in turn stimulates zooplankton production, and so on up the food chain (e.g. Fanning et al. 1982; Wainright 1987). Large resuspended particles provide food for planktonic (e.g. Arfi and Bouvy 1995) as well as benthic grazers. Organisms that are not consumed in the water column eventually die and sink to the seafloor to fuel the benthic community. Resuspension events also affect plankton community structure because higher nutrient levels enable larger cells (e.g. diatoms) to dominate, whereas smaller phytoplankton dominate under low-nutrient stratified conditions. These size differences may lead to differences in the zooplankton community because of differences in the feeding capabilities of grazers. The concept of benthic-pelagic coupling is also applicable to the many marine organisms that have both benthic and pelagic life stages. Most benthic macrofauna living in coastal systems have planktonic larvae. Depending on the species, these stages may last hours to months in the water column, during which time such species may be transported great distances. Conversely, many planktonic organisms enter a benthic resting phase and spend weeks to years in the seabed. Although grazing, physical mixing processes, and associated changes in the nutrient regime have been invoked to account for the existence of planktonic assemblages in nearshore waters that are distinct from shelf waters and open-ocean regions (e.g. Peterson 1986; Barnett and Jahn 1987), Margalef (1978) suggested that the actual distribution of phytoplankton populations reflects life-cycle limitations and the selective properties of the environment. A similar point of view was expressed by Smetacek (1985, 1988). Moreover, Eppley (1986) suggested that dormant life-cycle stages may provide the key to understanding fluctuations in the abundance of planktonic species. Benthic resting stages Benthic resting stages of phytoplankton have been known for quite some time. Dale (1983) described more than 60 dinoflagellate species having a resting cyst as part of their life cycle, and benthic cyst assemblages have since been described throughout the coastal oceans of the world (e.g. Belch and Hallegraeff 1990). Considerable interest has been focused on the cysts of dinoflagellates, in particular those species responsible for red tides and other noxious blooms (e.g. Burkholder et al. 1992), because cysts may provide the seed stock for bloom formation (Yentsch et al. 1986). Diatoms form resting cells and spores (reviewed by Garrison 1984), and the latter have been implicated as seeding agents of bloom formation in the Cape Peninsula upwelling plume (Pitcher 1990; Pitcher et al. 1991). Benthic resting stages have been reported in a variety of zooplankton taxa, including rotifers (Snell et al. 1983), tintinnids (Paranjape 1980), and cnidaria (Boer0 et al. 1992), although most research has focused on cladocerans (OnbC 1991) and copepods (see Marcus 1996). Many studies have Acknowledgments Support for this work was provided to N.M. from NSF grant OCE 93-13672 and to EB. from MURST, MIRAE and CNR. This review was conceived during a stay of both authors at the Bodega Marinc Laboratory. J. Clegg greatly encouraged the preparation of this paper. 763 764 Marcus and Boero reported on the distribution and abundance of resting stages in coastal regions. Although the benthic resting stage of most marine copepods is the egg phase, some freshwater species are dormant as benthic copepodites (e.g. Elgmork et al. 1990). Entering into a benthic dormant state has been associated with adverse environmental conditions (e.g. Marcus 1980, 1984; Elgmork et al. 1990) as well as with predation (Hairston and Olds 1984; Hairston et al. 1985). Previous studies have made it clear that individuals of many taxa previously thought to spend their entire life cycle in the water column actually rest in the seabed for periods ranging from a single adverse season to decades (Marcus et al. 1994) and longer (Hairston et al. 1996). These benthic resting stages enable the persistence of species in the system, and they appear to be important agents of local recolonization. They may also be important agents of dispersal since they survive under a wide range of conditions. Some have been identified in the ballast tanks of ocean-going ships (Hallegraeff and Belch 1992). Resting stages also afford species a temporal refugium from adverse conditions. Despite these potentially important roles, the influence of benthic resting stages on plankton production and community dynamics has yet to be fully elucidated. The primary outcome of most studies of benthic resting stages conducted to date has been clarification of biological mechanism(s) by which seasonal species disappear and return to the plankton year after year. A more synthetic and ecological approach is now needed for understanding how life-cycle dynamics, as well as carbon and nutrient fluxes, grazing, and other factors, affect the production and plankton community dynamics of coastal waters. This means that research on plankton must include the study of environments where “classical” plankters are not supposed to thrive, i.e. the sea bottom. Life cycles and ecology The value of a holistic approach to studies on plankton is certainly evident in the concept of supply-side ecology (Gaines and Roughgarden 1985; Lewin 1986) that was developed to explain the destiny of benthic communities. The maintenance of populations and species requires that organisms are replaced when they die. Life cycles and histories play a fundamental role in the replacement process. The concept of supply-side ecology focused attention on the importance of propagules for maintaining the long-term continuity of benthic communities. The source of the propagules can be the local community or distant communities. Each community, in its turn, supplies other communities with propagules. The novelty of this concept was disputed by several authors, but, as remarked by Grosberg and Levitan (1992), it enforced a concept that was not generally acknowledged by the scientific community. The example of benthic-pelagic coupling is valid not only for benthic communities, which have to be supplied with planktonic propagules, but also for planktonic communities, which have to be supplied with what were formerly benthic propagules. Many planktonic organisms are in fact present in the water column for restricted periods, disappearing during one season and reappearing at the onset of the following favorable season. If the planktonic community is viewed as a whole, the biomass shrinks and expands, but living forms are present continuously. If the biomass is split in10 species, however, discontinuities are evident. The explanation for these discontinuities is being found for an increasingly great number of species, and this body of information is now sufficient to propose a novel approach to understanding the functioning of marine systems. Supply-side ecology has been used to explain the persistence of benthic communities that depend on the flux of biomass from the benthos to the plankton and then to the benthos again. We suggest the use of an analagous concept, supply-vertical ecology, to explain the persistence of planktonic communities that depend on the supply of biomass from the plankton to the benthos and then to the plankton again. By merging supply-side ecology with supply-vertical ecology, a complete mixing of traditionally separated domains of the marine environment is achieved (Fig. 1). Such division is already bridged by the concept of meroplankton, which refers to the stages of organisms that spend only a portion of their life-cycle in the plankton. The meroplankton includes a variety of taxa and life-cycle stages (e.g. larvae of benthic organisms, planktonic eggs and larvae of nekton, adult medusae) that have benthic larval (polyp) stages, and planktonic copeplods that have benthic resting eggs. Belmonte et al. (1995) proposed the term merobenthos to describe the benthic stages of organisms that spend their juvenile and adult stages in the plankton. However, all organisms that spend part of their life cycle in the plankton and part in the benthos should be considered members of both the meroplankton and the merobenthos. In coastal systems many supposed holoplankters have benthic resting stages and should therefore be classified as meroplankton. Thus, for organisms with complex life cycles it is more accurate to refer to the pelagic stages as larval or adult meroplankton, and tc the benthic stages as embryonic/larval or adult merobenthos. The terms holoplankton and holobenthos should be reserved for those species that spend their entire life cycle in either the pelagic or benthic realms. Dale (1983) proposed a different (and contradictory) term for dinoflagellate benthic cysts-benthic plankton! The value of terms describing as a u,hole what is just a part of a life cycle was considered by Boero (1994) and Boero et al. (1996) in proposing an integrated model of plankton dynamics that incorporated life cycles. Do plankton and benthos really exist? Clearly the boundaries between these two domains are not as sharp as previously thought. New perspectives The examples described above provide compelling evidence that our understanding of production and plankton community dynamics in coastal waters will be improved by extending the predominant elemental-based view of benthicpelagic coupling to include life-cycle linkages. Life-cycle linkages are beginning to be appreciated, and the new findings suggest that research efforts are needed that explore fine-scale processes that have global-scale implications. Elucidating these processes will require a variety of approaches. Life cycles and benthic-pelag,ic 765 coupling Pelagic The first products of sexual reproduction go to the plankton ____._ ---~ Biogeochemical Coupling go to the benthos Growth into 8 --- belong to Temporary Eggs and cysts belong to Meiobenthos The small Fig. 1. The integration of biogeochemical and biological phenomena in benthic-pelagic cou- pling. Information on the physiology of resting stages of aquatic organisms is needed because physiological and biochemical processes influence longevity and thus the potential for future recruitment from the sea bed. Dehydrated stages (e.g. Artemia cysts) are ametabolic (Clegg 1986), which greatly extends their longevity. Hydrated systems are typically metabolically active because energy is needed to maintain the integrity of cells. In marine systems, resting stages are typically exposed to anoxia while buried in the sediments. If they are not ametabolic they must respire anaerobically. Anaerobic respiration requires suitable storage substrates, and organisms must be able to regulate their usage. They also must be able to deal with the waste products generated by metabolism and they must be able to recover when exposed to suitable conditions. Anaerobic fermentation of glucose releases far fewer ATP molecules than does aerobic respiration. Hochachka and Somero (1984) suggested that the most effective means of extending survival under anoxia is to reduce metabolism. Longevity during exposure to anoxia has been related to the amount of stored glycogen. Those organisms with more glycogen survive longer. In addition, some invertebrates depend on alternative metabolic pathways to generate a greater number of ATP molecules than through classic anaerobic fermentation. The reports of viable 40- and 300-year-old copepod resting eggs from marine and freshwater systems, respectively (Marcus et al. 1994; Hairston et al. 1995), are difficult to explain from a biological perspective because it is hard to understand how internal energy reserves could sustain the eggs for so long. On the other hand, these eggs may be ametabolic, as was recently reported for hydrated Artemia cysts exposed to anoxia (Clegg 1997). Knowing how resting stages manage to survive from physiological and biochemical perspectives will enable better predictions of their longevity. The resting eggs of copepods can be quiescent or diapausing. Quiescent eggs hatch when conditions become favorable, as do diapausing eggs that have completed the refractory period (see Marcus 1996). Alternatively, some diapausing stages may have internal mechanisms that regulate activation independent of external conditions. Circannual clocks that affect germination have been reported in some plankters (e.g. dinoflagellates, Costas et al. 1990; hydromedusae, Brock 1975), but this field is largely unexplored. Resting stages are subject to predation in the water column and in the sea bed. However, some copepod resting eggs have tough outer coverings and spines that protect them from being consumed and destroyed by some predators (Marcus and Schmidt-Gengenbach 1986). Predation in the water column may actually enhance the deposition of copepod resting eggs onto the seabed since eggs contained in fecal pellets probably have a greater settling velocity than do the eggs alone. In addition, eggs may be transported to other locations depending on how long it takes to pass through the digestive system of predators and the mobility of the predators. Copepod resting eggs contain organic matter in a compacted form, possibly with a rich energetic value, such as the seeds of angiosperms. Since copepod resting eggs are present in the millions in coastal sediments (see Marcus 1996), they could also be an important food source for some benthic organisms. Many meiobenthic organisms belong to groups that, in other environments, puncture cells 766 Marcus and Boero to extract their contents (e.g. tardigrades and nematodes). Differential predation on resting propagules by these organisms could affect plankton community dynamics. To our knowledge this problem has never been tackled. Studies of copepods have shown that the concentration of resting eggs is typically high ( lo6 mh2) in shallow protected environments that trap fine particles (e.g. estuaries and lagoons; Kasahara et al. 1975). These patterns likely reflect physical attributes of the eggs, which in turn affect their settling velocity (Marcus and Fuller 1986; Marcus and Taulbee 1992). Although most work has focused on inshore areas, eggs have been found in deep waters, for example, off Georges Bank at 165 m (Marcus unpubl. obs.) and off northern California (Marcus 1995). Marine canyons at the edges of continental shelves are sites where fine sediments from inshore areas are often deposited. Benthic resting stages may accumulate in these locations as well. If material from these canyons can be reintroduced onto continental shelves via upwelling, then canyons may provide an additional refuge and source of recruits for coastal planktonic communities. Complete extinction can be avoided by attaining a refuge from predation at low densities, as suggested by the classical Lotka-Volterra model. If the cause of reduced population size, however, is linked to adverse environmental conditions (e.g. temperature, nutrients, salinity), then low density may not afford sufficient (or any) protection. Environmental fluctuation is more typical of coastal or freshwater systems, but despite short-term variability in population densities and species composition, these communities are remarkably stable on a long-term basis. This is most likely due to a storage effect (Warner and Chesson 1985) resulting from the existence of benthic banks of eggs, spores, or cysts. Drawing from many single-species- and single-taxon-oriented studies, Boero (1994) and Boero et al. (1996) outlined a model for the functioning of coastal plankton communities by proposing the central importance of benthic resting stage banks, as did Hairston et al. (1996) for freshwater systems. With the exception of a few studies, research on benthic storage banks has primarily focused on the level of individual species. Belmonte et al. (1995) examined multitaxon benthic resting stage banks in a coastal marine system. Caceres (1997) examined the importance of a storage bank in the maintenance of species diversity in a freshwater lake. In the same way that recruitment limitation may affect the population and community structure of benthic macroinvertebrates in some marine habitats (Olafsson et al. 1994), the successful hatching or germination of benthic propagules may be a major determining factor of plankton community dynamics. Studies of seed-bank dynamics and plant communities have revealed relationships between seed longevity and above-ground population variability (e.g. Firbank 1993; Bonis et al. 1995). Although persistent seed banks ensure the reappearance of annual species year after year, the aboveground populations may display considerable short-term variability due to environmental variation acting on recruitment and subsequent survival. Where environmental fluctuations are so great that a species may not successfully reproduce in a given year, persistent seed banks guarantee their long-term survival. For aquatic systems, small freshwater ponds are the most variable environments whereas the coast- al ocean is the least variable, with large lakes being intermediate. We suggest that persistent storage banks should occur in small ponds whereas annual storage banks should be more characteristic of coastal systems. Divergence from this scheme could reflect the evolutionary history of species. The existence of storage banks may have evolutionary implications. As Hairston proposed in a series of papers on freshwater environments (e.g. Hairston and Walton 1986), organisms derived from propagules of different ages allow for genetic flow among different cohorts. Marcus et al. (1994) and Hairston et al. (1995) reported that copepod resting stages can remain dormant for decades to centuries, thus providing a mechanism to connect cohorts many generations apart. The fact that some zooplankton populations typically reach a peak when phytoplankton is plentiful could reflect coevolution, leading predators to evolve complex life cycles that are tuned to resource availability (Boer0 1994). It is also a common phenomenon that some plankters are very abundant in some perilBds (even leading to blooms, as in the case of jellyfish or dinoflagellates), only to disappear for many years. These sudden flushes, followed by sudden crashes, might express ai-1 evolutionary potential, as suggested by Boero (1994). A flourishing species represented by numerous individuals is subjected to the most widespread type of selection-stabili:cing selection enhanced by a high genetic flux among merging populations. Sudden decreases in abundance might subject the species to bottleneck and founder effects, prerequisites for speciation patterns of the flush-andcrash type (Carson 1975). However, resting stages constitute a deposit of specimens that allow stability in species that normally pass through population crashes (seasonal species). Their presence can be considered insurance against extinction (Boer0 1994). In this framework, the presence of species in a given zone cannot be judged only by considering active stages. A species can in fact be completely absent as perceivable individuals and be nonetheless present as a resting stage (e.g. May 1986). The species pool of a given area can thus be divided into two compon,=nts, referred to by Boero et al. (1996) as the realized biodiversity (species represented by some active specimens) and the potential biodiversity (species represented by resting specimens only). Species considered extinct because they have not been recorded for several years may persist out of sight as resting stages. Their sudden reappearance would be inexplicable were it not for resting stages. The application of r/K theory (Pianka 1970) to seasonal species that go through massive mortalities requires a thorough understanding of the life cycle. If the decrease in number of active stages is counterbalanced by an increase in resting stage production, thus leading to a more or less stable number of (different) representatives of the population, then consideration of just the active stages might lead to the misclassification of species according to this framework. Boero and Bouillon (1993) have shown for the Mediterranean hydroidomedusan fauna that the presence of a longlived pelagic sta,ge (the medusa) is not linked to a wider biogeographical distribution than that of species with no medusa. The hydroidomedusae with restricted biogeographical distributions (in .:his case, those endemic to the Mediterranean Sea) are evenly divided among species with and with- L&e cycles and benthic-pelagic out a medusa stage and, furthermore, the cosmopolitan species are composed mainly of species without a medusa. This situation suggests that, besides classical planktonic propagules such as medusae or larvae, species might be distributed by other means, such as rafting on floating objects or drift of fragments. Species with resting stages can be dispersed as such by currents or even by human activities. Ballast waters, for instance, have been shown to be an effective means of transport for resting stages (Hallegraeff and Belch 1992). Noxious blooms are an increasingly important problem for the management of coastal systems. They can lead to mass mortalities of both plankton, benthos and nekton, and some species can produce toxins that are dangerous for humans who eat fish and shellfish (e.g. ciguatera poisoning). Dinoflagellates and diatoms are *the main groups responsible for most harmful algal blooms, and some of these blooms appear to originate from resting stages in the sea bed (e.g. recent outbreaks of Pfeisteria piscida; Burkholder et al. 1992). The management of cyst banks could be attempted if we could answer some basic questions. For instance, the identification of accumulation sites, if these are present, and the determination of necessary germination and hatching requirements could lead to the establishment of regulations that limit activities during particularly crucial periods. The introduction of predator meiofaunal species to regulate the abundance of propagules of potentially dangerous species could prove effective as a means of biologically controlling the cyst banks of potentially dangerous bloomers. Conclusion The development of advanced technologies (from computerized on-board sensors to satellites) has greatly contributed to the growth of oceanography. There has been a tremendous improvement in our ability to study and understand the basic patterns and processes taking place in the marine environment. This progress has allowed oceanographers to tackle biological problems at regional and global scales (e.g. the determination of phytoplankton activity by the remote sensing of chlorophyll distributions). While important, these advances must not divert all of our attention from the more traditional ways of studying how the ocean works because mathematical models can often obscure the importance of diversity. The mechanisms leading to many global-scale phenomena (such as pelagic-benthic coupling) depend on finely scaled life-cycle and life-history patterns, requiring appreciation of how the species forming a community are able to cope with highly variable conditions. The study of these phenomena requires a diversity of expertise in disciplines ranging from taxonomy to population ecology. Progress in these disciplines is typically slower compared to fields where technology can collect atid process large amounts of data relatively quickly. The evidence provided here, however, suggests that such long-term investments will be very productive. 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