Small-Scale Pattern and Processes
in Benthic and Planktonic Invertebrates
Cheryl Ann Butman and Cabell S. Davis
Cheryl Ann Butman and Cabell S. Davis
Planktonic and benthic invertebrates share the water column and its resources for at least a portion of their life cycles, and therefore some similar processes-particularly those associated with water flow-may determine their spatial distributions. The importance of flow in zooplankton ecology is obvious; these "holoplanktonic"organisms are suspended for life in moving fluid. Likewise most benthic invertebrates have a "meroplanktonic" larval stage that temporarily resides in the plankton. In addition to transporting larvae, flow processes at the sediment-water interface may affect or effect benthic invertebrate distributions by transporting sediments, food and oxygen, as well as removing their wastes.
This paper focusses largely on the organisms and regions most familiar to the authors-soft-bottom invertebrates and zooplankton in temperate coastal and shelf waters-and on scales from the individual to local population, e.g., centimeters to kilometers. The large physical and biological differences between the benthos and zooplankton necessitated a division of this paper into two separate sections. The paper represents the views of the authors and is not necessarily a consensus of their research communities.
I. Background
Benthic ecology emerged as a discipline out of fisheries science. In the early 1910s, faunal surveys to locate favorable feeding grounds for bottom fishes indicated that the dominant invertebrate species varied on different bottom types. This concept of "parallel level-bottom communities" was presented more formally in the late 1950s using quantitative information on animal distributions relative to the sediments. Research during the first half-century focussed on species distributions relative to general characteristics of the bottom, and during the second half-century on (1) quantitative relationships between faunal distributions and more specific sediment characteristics, and (2) the pre- and post-settlement processes responsible for such patterns.
Classic ecological theory and experimental methods were developed first for the terrestrial environment, then applied to the rocky intertidal (wet land), and finally to soft sediments in deeper water. Thus, it was some time before the unique character of soft-bottom systems was appreciated. Initially, research centered on post-settlement processes, such as competition and predation, that had explained pattern in terrestrial and intertidal systems. But certain time-honored experimental methods, such as caging and reciprocal transplants, were often plagued with artifacts in soft-sediment systems. Moreover, even successful experiments tended to yield site-specific results. By the mid-1970s there was growing concern that biological interactions alone were not the mechanistic panacea to explain pattern in soft-bottom systems.
A largely overlooked but potentially very important factor affecting species distributions was the near-bed flow regime. Hydrodynamics control the flux of larvae, food, oxygen and other chemicals to and from the bed. Sediment transport determines bed characteristics and stability, and flow exerts forces to which organisms must adapt or succumb. Thus, much of the research during the last two decades has focussed on processes that explicitly or implicitly involve flow, including whether larval supply and settlement initiate pattern in species distributions.
B. Significance of previous discoveries and insights
The jury apparently is out on which mechanisms are most important in structuring soft-bottom communities, as highlighted by conclusions of two 1994 reviews. One review addressed whether recruitment limitation (larval supply and early post-settlement mortality) or post-settlement processes (competition, predation, and physical disturbance) are primarily responsible for structuring soft-sediment communities. They concluded that "multiple post-settlement processes ... have been demonstrated to cause density-dependent regulation of soft-sediment invertebrates after settlement" and that these processes "have the potential to obliterate patterns set by settlement alone". Yet their tables included 105 studies on predation, 45 studies on adult-juvenile interactions, 40 studies on food limitation, but only 9 studies on recruitment-limitation. These conclusions would be more convincing if there was greater parity in the data upon which they were based. In fact, the other review, on causal relationships between animal and sediment distributions, concluded that "the complexity of soft-sediment communities may defy any simple paradigm relating to any single factor". They argued strongly for studies addressing dynamic variables integrally related to the flow regime, such as larval supply and particulate flux.
II. State of the field
In the benthos, it is not the accepted knowledge that is interesting, but the knowledge that is not. Likely points of agreement are awfully general, including the following: (1) species distributions show spatial variation in the horizontal and with depth in the bed, (2) food is generally more limiting in the deep sea than in shallow water, (3) faunal distributions correlate with sediment grain size (but the causality is unknown), (4) geochemical sediment properties and the near-bed flow regime influence species distributions and function, and (5) organisms have a first-order impact on the sedimentological and geochemical properties of the bed.
Up for grabs are the mechanisms. Predation, competition, physical disturbance, disease and anthropogenic effects have been demonstrated for some species in some environments in some cases. Understanding of the roles of food resource partitioning has been limited by the difficulty in obtaining adequate information on where a species lives, how it forages, what it forages on, and who its neighbors are. Likewise, progress on evaluating the importance of larval supply and settlement has been hindered by severe methodological issues.
In fact, the soft-sediment system is dauntingly complicated. Benthic infauna experience water above and sediment below, and their mere existence often results in significant physical bed changes (e.g., tunnels, tubes, mounds, pits, and gobs of mucus) which, in turn, can affect chemical profiles, pore-water and solids mixing. Direct sampling of the bed is always destructive, and species information cannot be obtained remotely. Moreover, planktonic larvae of some taxa (e.g., clams and snails) are not morphologically distinguishable to species using light microscopy, and thus new molecular probes are needed for species identifications.
B. Examples of exciting new findings
Among the exciting findings of the last 20 years are a variety of effects of the near-bed flow on benthic organisms, but the work most relevant to spatial structure is on larval supply, settlement and early recruitment. Experimental field studies have shown, for example, that patterns of larval recruitment can be determined by small-scale biogenic features (e.g., tubes and pits) that affect bed shear stress, sediment deposition or food supply. Likewise, flume studies have shown that both passive transport and active behavior determine larval settlement sites, and that the relative contribution of the two components is species-specific. Moreover, settlement is initiated by positive and negative cues in the seabed and water column. For example, the swimming behavior of competent larvae can be altered in the water column by a soluble chemical cue, bringing larvae closer to the bed. At a larger scale, there is growing understanding of the coupling between oceanographic phenomena, such as upwelling and internal waves, that transport larvae, and their recruitment variation on shore.
C. Current foci and rationale
Most benthic biologists of even 20 years ago had little knowledge of or appreciation for the bottom boundary-layer flow environment, but now fluid dynamics is accepted as an important factor shaping the ecology and evolution of soft-bottom organisms. In fact, flow measurements are now a routine aspect of most field programs, and experiments are designed and interpreted within the context of the flow regime. Like biological interactions, flow alone is not the mechanistic panacea for explaining pattern in benthic systems. Investigations are needed of food and space limitation, adult-larval interactions, predation, physical or chemical alterations to the bed, all under realistic flow conditions. There is a dearth of natural-history observations on the life styles, feeding strategies, food items and biological interactions of benthic organisms in the field or under simulated field conditions in the lab. Particularly valuable are experiments that test interactions between a number of processes or variables, especially when such studies are developed within the framework of a predictive model. Finally, processes occurring within local benthic systems must be integrated into a larger, regional, oceanographic framework.
III. Existing infrastructure
Studying benthic soft-sediment systems is challenging because, in the field, subsurface organisms are nearly impossible to observe directly and many experimental methods significantly disturb the sediments or the flow regime. In laboratory flume experiments, the biogeochemistry of intact sediments is significantly disturbed relative to the field and there is usually high infaunal mortality. Flumes and wave tanks have been invaluable, however, for studying phenomena affecting small numbers of individuals in small patches of sediment, for observing individual behavior, and for assessing larval sediment selectivity as a function of flow regime. In addition, state-of-the-art instrumentation for remotely measuring small-scale flows and turbulence in flumes, such as Particle Image Velocimetry, can be used to quantify, for example, effects of suspension feeders on the near-bed flow regime or larval concentration fields.
Knowledge of spatial pattern in benthic systems is both limited and archaic. The quality of shipboard-operated sampling techniques (grabs and boxcores) has steadily improved through the years. Disturbance to the sediment surface is now minimal, but vertical distributions of organisms and chemical profiles are, no doubt, distorted by the coring process. Using acoustic telemetry and GPS, the position of a boxcore can now be located in space (Earth coordinates) to Å 5 m. In SCUBA-diving depths, an acoustic array and diver-operated interrogator system can map bottom position to an accuracy of Å1 m. Submersibles could extend such spatial resolution to deep water. Moreover, acoustics show promise for remote sensing of some benthic organisms. Sorely needed is a new generation of spatial data resulting from new sampling methodologies, more statistically rigorous spatial sampling designs, and greatly improved taxonomy.
Quantifying planktonic larval concentrations over appropriate space and time scales to estimate larval supply to the bed has been problematic. Most planktonic larvae are too small to be identified to species using remote techniques such as optical or acoustical instruments. Moored direct sampling is now possible with a new time-series zooplankton pump. But, sample processing is slow, laborious and expensive, and identifications are sometimes impossible because larvae of certain taxa are not sufficiently differentiated morphologically, necessitating the development of species-specific molecular probes. An even greater challenge is obtaining field measurements of initial larval settlement. One clever new instrument automatically exposes sediments under pre-selected physical conditions (e.g., flow, light, temperature). But settlement under natural field conditions requires an autonomous, time-series, seabed sampler.
IV. Exciting future opportunities and challenges
Benthic soft-bottom ecology is, perhaps arguably, the most interdisciplinary field of marine research. A wide array of benthic organisms are food items for bottom-feeding fishes, and some species (e.g., of clams, crabs and shrimp) are commercially important. Physical, chemical and geological processes occurring within and above the bottom drive or affect biological processes within the bed, with feed-back loops between any or all of the four disciplines. Moreover, benthic biology can significantly affect the near-bed flow regime, chemical fluxes into, through, and out of the bed, sediment transport, and bed stratigraphy. Thus, it is not surprising that in this very complicated, system progress has been slow in elucidating the processes that determine spatial distributions of the organisms. Such research is critical, however, because the results can have important implications for the biology, and for near-bed flow and seafloor processes in the other disciplines.
V. General References
Butman, C.A., 1987. Larval settlement of soft-sediment invertebrates: The spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processes. Oceanogr. Mar. Biol. Ann. Rev. 25: 113-165.
Graf, G., 1992. Benthic-pelagic coupling: A benthic overview. Oceanogr. Mar. Biol. Ann. Rev. 30: 149-190.
Gray, J.S., 1974. Animal-sediment relationships. Oceanogr. Mar. Biol. Ann. Rev. 12: 223-261.
Jumars, P.A., and A.R.M. Nowell, 1984. Fluid and sediment dynamic effects on marine benthic community structure. Amer. Zool. 24: 45-55.
Nowell, A.R.M. and P.A. Jumars, 1984. Flow environments of aquatic benthos. Ann. Rev. Ecol. Syst. 15: 303-328.
Ólafsson, E.B., C.H. Peterson and W.G. 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. Oceanogr. Mar. Biol. Ann. Rev. 32: 65-109.
Rhoads, D.C., 1974. Organism-sediment relations on the muddy seafloor. Oceanogr. Mar. Biol. Ann. Rev. 12: 263-300.
Snelgrove, P.V.R., and C.A. Butman, 1994. Animal-sediment relationships revisited: Cause versus effect. Oceanogr. Mar. Biol. Ann. Rev. 32: 111-177.
I. Background
Marine zooplankton research has a rich and diverse history. Early studies (late nineteenth and early twentieth century) were largely exploratory, defining taxonomies and species distributions. Subsequent process-oriented studies were designed to explain these observed patterns, using theory from terrestrial ecology and limnology as the conceptual framework. Integrative concepts such as trophodynamic theory, involving energy and mass transfer between primary producers, herbivores, and carnivores, were used to analyze marine plankton dynamics. The patchy nature of plankton distributions was discovered early on, and it was hypothesized that patches form by upward swimming of zooplankton in regions of downwelling flow (surface convergences). In fact, defining scales of patchiness and the underlying causes of this variability have been major research thrusts in marine zooplankton ecology. Extensive process-oriented studies have focussed, for example, on explaining early observations of diel vertical migration (DVM)-zooplankton swimming to the surface at night to feed and retreating to deeper, darker waters during the day to avoid predators. In parallel with research on trophic processes and patchiness, studies of individual species' life cycles and life histories have been conducted in both the field and laboratory. Earlier work described the annual cycles of zooplankton species, including the seasonal evolution of developmental stages within populations, and laboratory culture studies examined egg production and growth rates.
B. Significance of previous discoveries and insights
Technological advancements over the past three decades have enabled major accomplishments in marine zooplankton research, especially in the areas of life-history estimation, organismal-level research, and modeling. During the 1970s and 1980s, new culturing methods were developed that greatly enhanced laboratory measurements of egg production, feeding, and growth rates as a function of food and temperature. New techniques have been used for measuring nutritional requirements in zooplankton, including the importance of dissolved organic material as a food source. Field measurements of these rates also involved development of techniques such as gut pigment analyses, fertility indices, and biochemical methodologies. Food web relationships have been elucidated with immunological probes that identify species compositions in the stomach contents of predators. Mortality rates in field populations were inferred from inverse modeling. Molecular biological methods are being developed to help distinguish morphologically similar species and life stages, thus providing better information on species population structure.
New insights into the behavior of individual organisms emerged with the use of cinematography and video microscopy. Zooplankton are not simple, passive filter feeders, but accept or reject individual food particles. Likewise, swimming and mating are multifaceted, involving highly complex behaviors. Improvements in vertically stratified sampling and carefully designed experiments have yielded important insights regarding the factors that control DVM. Field observations of reverse DVM in response to predation, together with results from enclosure experiments, clearly indicate that predation is the dominant factor controlling DVM.
Advances in computer technology and modeling techniques have resulted in considerable progress in the development of more realistic coupled biological/physical models. Concentration-based models integrate interactions among vertical migration, population growth, and physical transport in determining plankton distributions. Individual-based models are being developed to incorporate organismal processes into population dynamics and are being coupled to physical-transport models.
As the empirical database grew, theoretical formulations were developed to explain the observations. The concept that recruitment, or survival during preadult life, is a major determinant of population size has become a centerpiece of research in marine ecology. Although postulated as early as 1914, the growing body of evidence over the last three decades has substantiated the importance of recruitment variability in marine populations. Several theories explaining recruitment variability have been developed. The "match-mismatch hypothesis" implicates seasonal timing between spawning and plankton blooms as an important factor regulating recruitment. The "stable ocean hypothesis" states that vertical stability of the water column leads to development of food-rich layers that enhance early survival. The "advective transport" or "wash-out hypothesis" contends that wind-induced horizontal transport of early life stages out of favorable feeding areas causes high pre-recruit mortality. Much of the empirical and modeling research over the past decade has focussed on microscale turbulence as an important factor controlling predator/prey encounter rates in the plankton.
II. State of the field
Interactions between predation, temperature, food limitation, vertical swimming behavior and physical transport determine distributional patterns of marine zooplankton, but the relative importance of each factor remains uncertain. For many species in shelf areas, it appears that food is generally not limiting and that predation is a dominant factor controlling their population sizes. For other species, it is clear that food-limitation is important. Coupled biological/physical models are clearly needed to understand these site- or species-specific effects. As discussed above, it is now generally accepted that DVM patterns are largely controlled by predation. It is also accepted that microscale turbulence can have important impacts on individual and population growth and survival rates. The current trend is a multiple-level approach including life-history estimation, organismal-level research, and biological/physical modeling, and should continue to provide new insights in marine zooplankton ecology.
B. Examples of exciting new findings
At the organismal level, direct observations have shown that individual zooplankton can detect and follow each other's "footprints" or "trails". An individual male copepod, for example, was observed to cross the path of a female, then turn and follow her stealthily by hopping in synchrony until mating occurred. This observation sheds light on the length scales at which individuals can detect one another, information that is critical for models of zooplankton patchiness and population transport. Mechanisms of predator detection by mechanosensors on copepod antennules also have provided new insights into processes controlling predator-prey interactions and have yielded critical length scales for predator detection.
Individual zooplankton behaviors have been observed directly in the open sea and their swimming patterns were measured in relation to ambient food concentrations and turbulence. This work showed that swimming activity was higher in low-turbulence high-food layers. Such observations serve as critical input for models examining the effects of turbulence and water-column stability on recruitment success.
At the population level, molecular techniques used on field populations have shed light on the geographic origins of zooplankton populations and provide information on the spatial separation of morphologically similar species. New video sampling tools have revealed that plankton species are often separated at very fine spatial scales in association with local hydrographic conditions. Real-time automatic identification of the plankton from video has enabled rapid, interactive mapping of ephemeral plankton patches and will allow real-time data assimilation into biological/physical models. Individual-based population models coupled with ocean circulation models have allowed organismal-level processes to be incorporated into studies of population distributions.
C. Current foci and rationale The current research trend is toward organismal-level and species population dynamics and their interaction with the physical environment. Development of individual-based models coupled to physical-transport models is bridging the scale gap between the individual and population levels, but this approach is still in its infancy.
III. Existing infrastructure
Marine zooplankton research currently involves laboratory experiments, shipboard studies, and modeling. Laboratory studies typically involve culture and observation of animals in small- to medium-sized vessels. A few large tank facilities are available to address certain kinds of research questions. In general, ship availability also appears to be adequate. Existing infrastructure is inadequate, however, in the growing area of high-resolution data acquisition. A network of high bandwidth ocean observatories are required, with high-end computers for incorporation of the data into high-resolution biological/physical models.
IV. Exciting future opportunities and challenges
The single biggest challenge in zooplankton ecology (and in marine ecology in general) is development of a predictive capability. In the open ocean where species diversity is high, understanding pelagic system dynamics is presently limited to basic trophic-level interactions (e.g. N,P, Z models). In low-diversity regions, understanding population dynamics of a few species could provide insights into system-level functioning, but realistically, it is difficult to determine what regulates the population size of even a single species. Quantifying recruitment variability, a major factor affecting population size, is complicated because of the myriad of factors affecting it. Using a simple exponential model, a relative change in average mortality rate of as little as 5% during early life can lead to order-of-magnitude changes in adult population size. Moreover, factors controlling mortality, such as predator abundance, cannot be measured within 5%. Detailed studies of individual organisms are not likely to help with this problem.
A possible solution may be found if the mortality is episodic. The above model scenario assumes constant mortality during the pre-recruit phase, but episodic mortality may well be measurably large, assuming that spatial and temporal sampling is sufficiently extensive and intensive to capture the event. With low-level chronic mortality, however, determining what regulates population size may be much more difficult. Clearly the relative importance of episodic and chronic events in determining recruitment success merits further study.
Repeated annual cycles in population abundance of many temperate species (e.g., Calanus) over decadal time scales suggests a certain level of system homeostasis. An important area of future research is on the dominant compensatory mechanisms, such as multispecies interactions, that generate such stable oscillations. The continued integration of organismal- with population-level research, together with studies of multispecies interactions are needed to understand such stabilizing mechanisms and thus to develop a predictive capability.
Specific areas of future zooplankton research should include in situ sampling of behaviors and distributions, and data-assimilative model development. To adequately quantify event-scale processes, new sampling methods are required that can resolve the organisms to species in both time and space. Such sampling could be achieved, for example, using optical imaging, including holography and high-definition video, as well as range-gated laser systems for non-invasive data acquisition. High bandwidth data transfer from networks of autonomous platforms, such as profiling moorings, autonomous underwater vehicles, and possibly aircraft can provide the needed capacity for high-resolution data acquisition.
V. General References
Gallager, S. M., C. S. Davis, A. W. Epstein, A. Solow, and R. C. Beardsley, 1996. High-resolution observations of plankton spatial distributions correlated with hydrography in the Great South Channel, Georges Bank. Deep Sea Res. II 43: 1627-1664.
Haury, L.,and H. Yamazaki, 1994. The dichotomy of scales in the perception and aggregation behavior of zooplankton. J. Plankton Res. 17: 191-197.
Mackas, D. L., K. L. Denman, and M. R. Abbott, 1985. Plankton Patchiness: Biology in the physical vernacular. Bull. Mar. Sci. 37: 652-674.
Ohman, M. D., B. W. Frost, and E. B. Cohen, 1983. Reverse diel vertical migration: An escape from invertebrate predators. Science 220: 1404-1406.
Rothschild, B. J. (ed.), 1988. Toward a Theory on Biological-Physical Interactions in the World Ocean. Kluwer Academic Publishers, Boston, 650 pp.
Strickler, J. R., 1984. Calanoid copepods, feeding currents, and the role of gravity. Science 218: 158-160.
Yen, J., and J. R. Strickler, 1996. Advertisement and concealment in the plankton: what makes a copepod hydrodynamically conspicuous. Invert. Biol. 115: 191-205.
Although the soft-bottom benthos and the zooplankton live in very different physical environments, over the last 20-30 years there are some striking similarities in research focus, specifically on the roles of hydrodynamics and recruitment-limitation in determining spatial distributions. Moreover, both benthic and zooplankton biologists have recently turned to molecular techniques for the identification of morphologically indistinguishable species (larvae in the benthos and adults in the zooplankton) or to track specific populations (in the zooplankton). Strong dissimilarities between the two fields are in the areas of (1) technology development for remotely sampling organism distributions, and (2) coupled biological/physical model development. Zooplankton research has the lead in both areas. Soft-bottom research is lagging primarily because of the more complicated nature of the benthic environment, where there are two different physical media, water above sediments, and where most of the organisms undergo a planktonic larval stage. Finally, zooplankton research may be more replete in direct observations, but benthic research is more surfeit in experimental manipulations.
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