March 20-22, 1998

NCEAS, Santa Barbara

Participants: Michael A. Rex (Convener), Ron J. Etter, Paul V.R. Snelgrove, Hal Caswell, J. Frederick Grassle, Carol T. Stuart, Craig R. Smith, Robert R. Hessler, and Eugene D. Gallagher



The purpose of this session was to synthesize patterns of local diversity on ecological time scales in the deep-sea benthos, and review potential explanations of species coexistence to evaluate whether current theory could plausibly account for the known patterns. Deep-sea species diversity is very high, possibly rivaling that of tropical rain forests and coral reefs. How can so many ecologically similar deep-sea species coexist in what appears to be a relatively unstructured soft-sediment environment?


We defined "local" scales as 0.25m2box-core samples and their replicates at individual sampling stations. There were up to 20 replicates per sampling station in the studies that we considered, and ship-board navigation allows placement of replicates to within distances of 10's to 100's of meters apart. We also considered manipulative experiments and observations carried out on similar spatial dimensions, decimeters to meters. The temporal scale available to study was very limited because precision quantitative sampling has been restricted to the last 20 years, and the longest time series of samples taken at the same locality spans only three years.

As very general conceptual context for our discussions, we took the approach that species diversity is a dependent variable that can potentially be explained as a function of independent biological and physical variables. The features of species diversity addressed were: 1. species density (the number of species per 0.25m2), 2. rarefaction diversity [the Hurlbert-Sanders expected number of species E(Sn)], 3. the proportion of singletons (species represented by single individuals), 4. the relative abundance of the most dominant species in samples, and 5. estimates of the regional species pool. We were primarily concerned with the macrofauna, but comparisons were also made with the meiofauna whenever possible.

Diversity was compared between "shallow" (<200m) and "deep-sea" (>200m) ecosystems, and along a bathymetric gradient in the western North Atlantic from Georges Bank on the continental shelf (1296 VanVeen Grabs, 38-168m) to lower bathyal (558 box cores, 250-3500m) depths in the deep sea. This is the largest regional database available for precision samples. (Many thanks to Fred Grassle and his colleagues for making this database available to the Working Group, and to Ron Etter for analyzing the data before and during the session to help direct our discussions). Patterns of diversity in this extensive database were also compared to the level of diversity measured in other ocean basins where comparable quantitative sampling methods had been used (Table 1). We reviewed all known case studies of small-scale observations and experiments on community structure (44 studies altogether, Tables 2-4) primarily to assess the effects of localized disturbance, organic enrichment and environmental heterogeneity on species coexistence. (Special thanks to Craig Smith who originally developed Table 1-4 for our earlier NCEAS Workshop, and to Paul Snelgrove who updated them for our Working Group meeting).

We evaluated variation in diversity in the context of seven models of local coexistence adapted largely from Tilman and Pacala (1993) and Holt (1993) [in Ricklefs, R.E. and Schulter, D. eds., 1993, Species Diversity in Ecological Communities, Chicago Univ. Press] and expanded and modified somewhat to fit marine benthic systems. These models were: 1. spatial heterogeneity in two or more limiting factors combined with interspecific tradeoffs in abilities to deal with these factors, 2. temporal variability in resource supply combined with nonlinearities in the responses of species to resource levels, 3. spatio-temporal variability in disturbance combined with tradeoffs between competitive and colonization abilities, 4. disproportionate predation on competitive dominants, 5. competitive similarity, 6. source-sink effects in heterogeneous environments, and 7. recruitment limitation models (noninteractive).

We applied the Ewens-Caswell (Caswell, H., 1976, Ecol. Monogr. 46:327-352) neutral model to sample data in order to test whether species diversity departed from neutral (unstructured) expectations in terms of V statistics and the proportion of singletons. (Kudos to Hal Caswell for revising and reprogramming the neutral model for our Working Group meeting, and for performing a variety of tests of the model as part of our work in Santa Barbara).

Findings, conclusions and recommendations for future research

  1. Geographic patterns of local diversity. The overall patterns of diversity with depth (including the continental shelf) is unimodal with a peak at about 2000m. Deep-sea diversity, between 500 and 3500m in the western North Atlantic, is higher than on the continental shelf. This confirms, using controlled intra-regional comparisons and a large database of quantitative samples, the long-standing assertion that the deep sea supports elevated diversity, as well as earlier studies using non-quantitative samples, which suggested that the diversity-depth trend is unimodal with maximum diversity at mid-bathyal depths. Standing stock (biomass and abundance) declines exponentially with depth. If standing stock can be taken to reflect the rate of nutrient input, the depth-diversity pattern generally supports the productivity-diversity trend which tends to be unimodal over a broad range of productivity in aquatic, marine and terrestrial environments (Rosenzweig and Abramsky, 1993). As with similar unimodal relationships in other environments, diversity was most depressed at the highest densities which occur on the continental shelf. A variety of other deep-sea environments with elevated animal abundance resulting from unusually high trophic input (proximity to high surface production or oxygen minimum zones, food concentrated by bottom topography, reducing habitats) also show depressed species diversity. Interestingly, tests of the neutral model showed that diversity across most of the depth range within the deep sea (including the diversity peak at 2000m) did not depart from neutral expectations (V statistics were well within two standard deviations of zero). Strongly significant negative deviations occurred on the continental shelf and uppermost slope. There were also significant negative deviations at the greatest depth sampled (3000-3500m). The proportion of singletons in deep-sea samples, long thought to be uniquely high for marine communities, do not depart from neutral samples of their size (number of species and individuals).
  2. The consensus among deep-sea ecologists, and ecologists in general, is that the positive relationship between animal density and diversity at low densities probably reflects higher local extinction rates associated with small population size. The negative relationship between abundance and diversity at higher densities is much more problematical. This may be where some combination of the causes mentioned above may come into play most strongly in structuring deep-sea communities. We found it difficult to evaluate the contending theories which collectively include resource supply, physical disturbance, biological interactions (competition and predation), sources of environmental heterogeneity and dispersal operating on a variety of spatial and temporal scales, as well as the adaptive properties and flexibilities of individual species. As others have pointed out (e.g. Tilman and Pacala 1993), all of the models would permit a high level of species coexistence to develop as long as there exists variation in individual fitness and some kind of tradeoff in response to environmental factors. Perhaps the real question is "Why do near-shore marine communities have depressed diversity compared to the deep sea?"

    It became clear from our analyses, simulations and weighing of potential explanations that several new or additional kinds of sampling are necessary to test alternative hypotheses. 1. More precision sampling is needed on longer time scales to assess the population dynamics phenomena implicit in nearly all potentially relevant theories. 2. It would also be very helpful to expand the spatial scale of quantitative sampling beyond 0.25m2 to meters or tens of meters either with contiguous box cores or precise local random sampling design to capture a more complete picture of neighborhood environmental heterogeneity and population structure. 3. The huge database of quantitative samples in the western North Atlantic should be extended below 3500m to include the vast abyssal environment. 4. The quantitative sampling that has dominated deep-sea ecology for the past two decades should be complemented with larger qualitative (e.g. epibenthic sled) samples, to acquire more information on life histories of individual species and to better assess the species pool. Overall, this part of our meeting was very productive and successful in clearly establishing the pattern of diversity with depth using the largest and most geographically comprehensive database available, comparing the observed diversity patterns to expectations from a neutral model, determining where in the deep sea manipulative experiments are most likely to yield measurable and interpretable results, and determining what new sampling protocols are required to effectively test theories of community structure.

  3. Levels of Species Coexistence. When controlled, within-habitat comparisons are made in the North American Basin, levels of species coexistence in the deep-sea benthos are higher than in adjacent shallow-water areas. The prevailing contemporary explanation for high local species diversity in the deep sea has been environmental heterogeneity in the form of "patchiness" on scales of <m2 that results from the activities of megafaunal animals, deadfalls, sinking plant material and phytodetritus. However, an exhaustive review of published experiments and direct observations (Tables 2-4), suggested that organic and physical sources of heterogeneity typical for the deep seabed are associated with only modest changes in community structure - generally a shift in abundance of one or a few species, or the temporary appearance of an opportunist not normally present in the background community. Since deep-sea samples on scales of 0.09m2 contain 50-150 species, and 0.25m2 box cores can collect hundreds of species, it is difficult to see how the effects of observed or experimentally induced heterogeneity and disturbance can account for this very high level of local coexistence. Fewer than one percent of macrofaunal species seem to respond. Species coexistence in deep-sea sediments remains a major challenge to ecological theory.
  4. Numerical vs. Functional Response. Gene Gallagher provided an important new insight from our wide-ranging discussion of data and theory. Deep-sea and coastal faunas appear to respond to disturbance and heterogeneity in fundamentally different ways. Coastal communities exhibit very marked numerical responses to seasonal variation in food and disturbance. This response is characterized by conspicuous shifts in dominance and the number of coexisting species. Changes in relative abundance are often experienced throughout the community. This large inclusive kind of response is not evident in deep-sea communities. Here, the numerical response to temporal and spatial environmental change seem restricted to a small minority of species, usually expressed as a temporary change in abundance. Deep-sea species may have evolved adaptations to "even out" environmental variation through a more functional kind of response, such as caching food resources (physically or metabolically), or modulating the allocation of energy to reproduction and growth over long period of time.



We plan to write at least three papers based on our work so far:

  1. A review of analytical methods to assess diversity, the importance of standardization and control in sampling designs, and the potential relevance of functional and numerical community responses. Gene Gallagher is the principal organizer.
  2. Application of neutral models to estimates of deep-sea diversity. Hal Caswell, Ron Etter and Mike Rex are principal organizers.
  3. A review of the effects of disturbance and spatial heterogeneity on deep-sea species diversity. Craig Smith and Paul Snelgrove are the principal organizers.