Download Minireview: The importance of benthic

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. Studies on biological phenomena, such as the
role of resting stages in the population dynamics of marine
plankters, when transferred into an ecological context, will
lead to a significant increase in our understanding of the
basic mechanisms controlling the functioning of aquatic systems.
coupling
767
References
Size composition and distribution
of particles related to wind-induced resuspension in a shallow
tropical lagoon. J. Plankton Res. 17: 557-574.
BARNETT, A. M., AND A. E. JAHN. 1987. Pattern and persistence
of a nearshore planktonic ecosystem off Southern California.
Cont. Shelf Res. 7: l-25.
BHLMONTE G., AND OTHERS. 1995. Resting stages off the Italian
coast, p. 53-58. In A. Elefteriou, A. D. Ansell, and C. J. Smith
reds.], Biology and ecology of shallow coastal waters. Olsen
& Olsen.
BOBRO, E 1994. Fluctuations and variations in coastal marine environments. Publicazioni della Stazione Zoologica di Napoli I:
Mar. Ecol. 15: 3-25.
ARFI, R., AND M. BOUVY. 1995.
-,
G. BELMONTE, G. FANEIU,
S. PIRAINO, AND E RUBINO.
1996. The continuity of living matter and the discontinuities
of its constituents: Do plankton and benthos really exist?
Trends Ecol. Evol. 11: 177-180.
AND J. BOUILLON. 1993. Zoogeography and life cycle patterks of Mediterranean hydromedusae. Biol. J. Linn. Sot. 48:
--
239-266.
AND S. PIRAINO. 1992. On the origins and evolution of hidromedusan life cycles (Cnidaria, Hydrozoa), p.
59-68. In R. Dallai [ed.], Sex origin and evolution. Selected
Symposia and Mongraphs U.Z.I. 6.
BOIXH, C. J., AND G. M. HAI~LEGRAEFF. 1990. Dinoflagellate cysts
in recent marine sediments from Tasmania, Australia. Botanica
Marina 33: 173-192.
BONIS, A., J. LEPART, AND I? GRILLAS. 1995. Seed bank dynamics
and coexistence of annual macrophytes in a temporary and
variable habitat. Oikos 74: 81-92.
BROCK, M. A. 1975. Circannual rhythms. I. Free-running rhythms
in growth and development of the marine cnidarian Cumpanuluria flexuosa. Comp. Biochem. Physiol. 51: 377-383.
BURKHOLDER, J. M., E. J. NOGA, C. H. HOBBS, AND H. B. GLASGOW. 1992. New “phantom”
dinoflagellatc is the causive
agent of major estuarine fish kills. Nature 358: 407-410.
CACERES, C. 1997. Temporal variation, dormancy, and coexistence:
A field test of the storage effect. Proc. Natl. Acad. Sci. 94:
9171-9175.
CARSON, H. L. 1975. The genetics of speciation at the diploid level.
Am. Nat. 109: 83-92.
CLEGG, J. S. 1986. The physical properties and metabolic status of
Artemia cysts at low water contents: The “water replacement”
hypothesis. In A. C. Leopold red.], Membranes, metabolism,
and dry organisms. Cornell Univ. Press.
-.
1997. Embryos of Artemia franciscana survive four years
of continuous anoxia: The case for complete metabolic rate
depression. J. Exp. Biol. 200: 467-475.
COSTAS, E., V. LOPEZ RODAS, M. VALLEYO, AND M. NAVARRO.
1990. Ritmos endbgenos et aparicihn estacional de dinoflagelados. Sci. Mar. 54: 107-112.
DAC;G, M. J. 1988. Physical and biological responses to the passage
of a winter storm in the coastal and inner shelf waters of the
northern Gulf of Mexico. Cont. Shelf Res. 8: 167-178.
DAI,E, B. 1983. Dinoflagellate resting cysts: “Benthic plankton,”
p. 69-136. In G. A. Fryxell [ed.], Survival strategies of the
algae. Cambridge Univ. Press.
ELGMORK, K., G. HAI,VORSEN, J. A. EIE, AND A. LANGELAND.
1990. Coexistence with similar life cycles in two species of
freshwater copcpods (Crustacea). Hydrobiologia 208: 187199.
EPPLEY, R. W. 1986. Plankton dynamics of the Southern California
Bight. Lecture notes on coastal and estuarine studies. SpringerVerlag.
768
Marcus and Boero
FANNING, K. A., K. L. CARDER, AND I? R. BETZER. 1982. Sediment
resuspension by coastal waters: A potential mechanism for nutrient re-cycling on the ocean’s margins. Deep-Sea Res. 29:
953-965.
FIRBANK, L. G. 1993. Short-term variability of plant populations
within aregularly disturbed habitat. Oecologia 94: 35 l-355.
GAINES, S., AND J. ROUGHGARDEN. 1985. Larval settlement rate:
A leading determinant of structure in an ecological community
of the marine intertidal zone. Proc. Natl. Acad. Sci. USA 82:
3707-37 11.
GARRISON, D. L. 1984. Planktonic diatoms, p. 1-18. In K. A. Steidinger and L. M. Walker [eds.], Marine plankton life cycle
strategies. CRC.
GRAF, G. 1992. Benthic-pelagic coupling: A benthic view. Ocean.
Mar. Biol. Ann. Rev. 30: 149-190.
GROSBERG, R. K., AND D. R. LEVITAN. 1992. For adults only?
Supply-side ecology and the history of larval biology. Trends
Ecol. Evol. 7: 130-133.
HAIRSTON N. G., JR., S. ELLNER, AND C. M. KEARNS. 1996. Overlapping generations: The storage effect and the maintenance of
biotic diversity. In 0. E. Rhodes, Jr., R. K. Chesser, and M. H.
Smith [eds.], Population dynamics in ecological space and
time. Univ. Chicago Press.
AND E. G. OLDS. 1984. Population differences in the timing of diapause: adaptation in a spatially heterogeneous environment. Oecologia 61: 42-48.
AND W. R. MUNNS, JR. 1985. Bet-hedging and
c&ironmen;ally
cued diapause strategies of diaptomid copepods. Intern. Verein. Theor. Angew. Limnol. 22: 3170-3177.
R. A. VAN BRUNT, AND C. M. KEARNS. 1995. Age and
su;vivorship of diapausing eggs in a sediment egg bank. Ecology 76: 17061711.
AND W. E. WALTON. 1986. Rapid evolution of a life history trait. Proc. Natl. Acad. Sci. USA 83: 4831-4833.
HALLEGRAEFF;, G. M., AND C. J. BOLCH. 1992. Transport of diatom
and dinoflagellate resting spores in ships’ ballast water: Implications for plankton biogeography and aquaculture. J. Plankton
Res. 14: 1067-1084.
HOCMACHKA, I? W., AND G. N. SOMERO. 1984. Biochemical adaptation. Princeton Univ. Press.
KASAHARA, S., S. UY E, AND T. ONBE. 1975. Calanoid copepod eggs
in sea-bottom muds. II. Seasonal cycles of abundance in the
populations of several species of copepods and their eggs in
the Inland Sea of Japan. Mar. Biol. 31: 25-29.
LEWIN, R. 1986. Supply-side ecology. Science 234: 25-27.
MARCUS, N. H. 1980. Photoperiodic control of diapause in the
marine Calanoid copepod Labidoceru aestiva. Biol. Bull. 159:
311-318.
-.
1984. Variation in the diapause response of Lubidoceru
uestivu (Copepoda: Calanoida) from different latitudes and its
importance in the evolutionary process. Biol. Bull. 166: 127139.
-.
1995. Seasonal study of planktonic copepods and their
benthic resting eggs in northern California coastal waters. Mar.
Biol. 123: 459-465.
-.
1996. Ecological and evolutionary significance of resting
eggs in marine copepods: Past, present, and future studies. Hydrobiologia 320: 141-152.
AND C. M. FULLER. 1986. Subitaneous and diapause eggs
of ‘Lubidoceru uestivu (Copepoda: Calanoida): Differences in
fall velocity and density. J. Exp. Mar. Biol. Ecol. 99: 247-256.
R. V. LuT%, W. BuRNt:-rr, AND P. CABLE. 1994. Age, viability, and vertical distribution of zooplankton resting eggs
from an anoxic basin: Evidence of an egg bank. Limnol.
Oceanogr. 39: 154-158.
-,
AND J. SCHMIDT-GENGENBACH.
1986. Recruitment of in-
dividuals into the plankton: The importance of bioturbation.
Limnol. Oceanogr. 31: 206-210.
AND K. TAL LBEE. 1992. Potential effects of a resuspension
event on the vertical distribution of copepod eggs in the sea
bed: A laboratclry simulation. Mar. Biol. 114: 249-251.
MARGALEF, R. 19713. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1:
493-509.
MAY, L. 1986. Rotifer sampling-a
complete species list from one
visit? Hydrobic,logia 134: 117-158.
NIELSEN, T. G, AND T. KI~RBOE. 1991. Effects of a storm event on
the structure of the pelagic food web with special emphasis on
planktonic ciliates. J. Plankton Res. 13: 35-5 1.
OI~AFSSON, E. B, C. H. PETERSON, AND W. J. AMBROSE, JR. 1994.
Does recruitment limitation structure populations and communities of macro-invertebrates in marine soft sediments: The
relative significance of pre- and post-settlement processes.
Ocean. Mar. Bjol. Ann. Rev. 32: 65-109.
0~~6, T. 1991. Some aspects of the biology of resting eggs of
marine cladocerans, p, 41-55. In A. Wenner and A. Km-is
[eds.], Crustacean egg production. A. A. Balkema.
PARANJAPE, M. 1980. Occurrence and significance of resting cysts
in a hyaline tintinnid, Helicostemellu subulutu (Ehre). Jorgenson, J. Exp. Mar. Biol. Ecol. 48: 23-34.
PETERSON, W. T. 1986. The effects of seasonal variations in stratification on phnkton dynamics in Long Island Sound, p. 297320. In J. Bowman, M. Yentsch, and W. T. Peterson [eds.],
Tidal mixing and plankton dynamics. Springer-Verlag.
PIANKA, E. R. 1970. On r and K selection. Am. Nat. 104: 581588.
PITCHER, G. C. 1990. Phytoplankton sea population of the Cape
Peninsula upw elling plume, with particular reference to resting
spores of ChL,etoceros (Bacillariophyceae) and their role in
seeding upwelling waters. Estuar. Coastal Shelf Sci. 31: 283301.
-,
D. R. WALKER, B. A. MICTHELL-INNES, AND C. L. MALONEY. 1991. Short-term variability during an anchor station
study in the scathern Benguela upwelling system: Phytoplankton dynamics. Prog. Oceanogr. 28: 39-64.
SMETACEK, V. 1985. Role of sinking in diatom life-history cycles:
Ecological, evolutionary, and geological evidence. Mar. Biol.
84: 239-25 1.
-.
1988. Plankton characteristics, p. 93-130. In H. Postma
and J. J. Zijlsra [eds.], Ecosystems of the world: Continental
shelves. Elsevicr.
SNELL, T., B. BURKE, AND S. MESSUR. 1983. Size and distribution
of resting eggs in a natural population of the rotifer, Bruchionus
plicutilis. Gull! Res. Rpt. 7: 285-287.
SoMMt!R, U. 1989. Plankton ecology: Succession in plankton communities. Springer.
VAIJEI,A, I. 1995. Marine ecological processes, 2nd ed. Springer.
WAINRIGHT, S. 1987. Stimulation of heterotrophic microplankton
production by resuspended marine sediments. Science 238:
1710-1712.
WARNER, R. R, AI~D l? L. CHESSON. 1985. Coexistence mediated
by recruitment fluctuations: A field guide to the storage effect.
Am. Nat. 125: 769-787.
‘YENTSCH, C. M., I? M. HOLLIGAN, W. M. BALCII, AND A. TVIRBUTAS. 1986 Tidal stirring vs stratification: Microalgal dynamics with special reference to cyst-forming, toxin producing
dinoflagellates, p. 224-252. In 5. Bowman, C. M. Yentsch, and
W. T Peterson [eds.], Tidal mixing and plankton dynamics.
Springer-Verl lg.
Received: 23 May 1997
Accepted: 31 October 1997
Amended: 20 November 1997