Effects of megafauna exclusion on nematode assemblages at a deep-sea site

https://doi.org/10.1016/j.dsr.2007.12.001Get rights and content

Abstract

Caging experiments were performed at the Arctic deep-sea long-term observatory HAUSGARTEN to investigate the effects of megafauna exclusion on nematode assemblages. Six experimental cages were deployed at 2500 m water depth and sampled after 4 years for meiofauna and a series of sediment parameters. With the exception of chlorophyll a and phaeopigments, which were significantly higher inside the cages, sediment parameters did not differ between inside and outside the cages. Yet multivariate analysis of the sedimentary environment showed a higher variability outside the cages, indicating higher environmental heterogeneity in the presence of megafauna. Nematode densities (aver. 1516 ind 10 cm−2) were significantly higher in sediments from inside the cages, whereas total number of species (aver. 70 sp.), Shannon–Wiener diversity (aver. 3.4) and Pielou evenness (aver. 0.8) did not differ between the two treatments. Also differences in faunal multivariate structure between cage and control samples were not significant. Nevertheless, Fisher's alpha diversity, the number of nematode genera and taxonomic distinctness showed significantly higher values outside the cages. Since univariate measures are often insensitive to changes in community structure, and interpretation of the multivariate analysis was confounded by the large number of rare species, we further analysed our data by dividing the species into three groups of frequency (frequent, intermediate and occasional) and into three groups of abundance (dominant, sub-dominant and scarce). Results from this analysis revealed that the higher nematode abundances inside the cages were mainly due to an increase in density of scarce species that were either frequent or intermediate in frequency. In contrast, occasional species were adversely affected. These results lead us to believe that it is mainly the frequent species occurring in low densities that take advantage of favourable conditions (i.e. lack of disturbance or increased phytodetritus) in the deep sea. The higher taxonomic distinctness, Fisher's diversity, and number of genera at the control sites, together with the fact that they were environmentally more heterogeneous, suggest that megafaunal organisms play an important role in creating microhabitats in the sediment and significantly influence deep-sea nematode assemblages. However, the lack of any changes in species richness inside the cages after 4 years suggests that they cannot fully account for the maintenance of the remarkable high levels of species coexistence in the deep sea. The key is more likely to be found in evolutionary history than actual ecology.

Introduction

Mechanisms of diversity maintenance in the deep sea have been the subject of speculation for decades (Snelgrove and Smith, 2002). The matter of how so many species coexist within nutrient-poor sediments is especially intriguing since the deep sea lacks the obvious spatial and temporal complexities that contribute to diversity in other high-diversity environments (Gage, 1996). On the other hand, the deep-sea environment is generally homogeneous in terms of temperature, sediment composition, physical disturbance and broad topography. At the small scale, however, there is increasing evidence of temporal and spatial variability in biogenic disturbance and biogenic microhabitats. Their importance for diversity maintenance is the focus of ongoing research (Snelgrove and Smith, 2002; Thistle, 2003).

Habitat heterogeneity and small-scale biological disturbances, although through different mechanisms, are both expected to enhance diversity. The habitat heterogeneity hypothesis assumes that structurally complex habitats may provide more diverse ways of exploiting the environmental resources, thereby increasing species diversity (Bazzaz, 1975), whereas disturbance should enhance diversity by reducing populations of dominant competitors (Connell, 1978; Huston, 1979). In the deep sea, very modest sources of disturbance are considered important because they are operating in a comparatively stable, low-energy environment. Disturbance of the surface sediment due to the feeding activities of relatively larger organisms, for example, may enhance diversity because their effects could persist long enough to be used over different successional stages by a broad spectrum of organisms (Snelgrove and Smith, 2002). In the same way, biologically generated habitat heterogeneity might persist in the sediment for years and therefore contribute to the high species coexistence in the deep sea (Thistle, 1981; Gage, 1996).

Small-scale disturbances and biogenic heterogeneity in the deep sea are created partly by the activities of epibenthic megafaunal organisms (Gray, 1974; Wheatcroft et al., 1989; Kukert and Smith, 1992), which are conspicuous elements of deep-sea communities and occur in virtually all bathyal and abyssal habitats (Gage and Tyler, 1991). These comparably large organisms are dominated by deposit feeders which rework particles at or immediately below the sediment–water interface (Gray, 1974; Thistle, 2003). The low quantities of organic matter within deep-sea sediments means that deposit feeders need to ingest and forage large amounts of sediment in order to gain a net input of energy. This requirement implies that the level of impact they have on the sediment surface can be substantial, both in terms of bioturbation and biochemical reworking (Sibuet and Lawrence, 1981; Roberts et al., 2000) and in terms of utilization and redistribution of particulate organic carbon (Lauerman et al., 1996; Kaufmann and Smith, 1997; Miller et al., 2000; Bett et al., 2001). At the same time, some larger benthic organisms may also prey on smaller organisms, potentially altering prey abundances (Iken et al., 2001; Thistle, 2003).

By documenting correlations between macro- and meiofaunal organisms and biogenic features, several studies have provided support for the importance of biological disturbance for smaller-sized organisms in the deep sea (Thistle, 1979; Levin et al., 1986; Thistle and Eckman, 1990). However, because of the inherent difficulties of conducting experiments in the deep sea, the direct effects of disturbance and habitat heterogeneity caused by megafaunal organisms on the diversity and community structure of these organisms have been difficult to assess. So far, small-scale manipulative experiments carried out in the deep sea have involved mainly colonization of defaunated sediment trays and nutrient-enriched sediment trays (Grassle, 1977; Levin and Smith, 1984; Desbruyères et al., 1985; Smith, 1985; Grassle and Morse-Porteous, 1987; Levin and Di Bacco, 1995; Snelgrove et al., 1992, Snelgrove et al., 1996). Exceptions include Smith et al. (1986) and Kukert and Smith (1992), who investigated the effects of artificial sediment mounds on macrofauna communities. All of these experiments have focused on macrofaunal groups. No equivalent experimental data are available on the impact of biological disturbance on deep-sea nematodes, the most abundant and perhaps, at the local scale, the most species-rich metazoan group in deep-sea sediments (Lambshead, 1993). Given the differences in lifestyles and dispersal potential between macrofauna and meiofauna, it is quite conceivable that processes regulating diversity differ between the groups (Warwick, 1984; Snelgrove and Smith, 2002). This paper reports on the first investigation of the effects of megafaunal exclusion on nematode assemblages at a deep-sea site (2500 m). Our hypothesis is that in the absence of megafauna disturbance and predation inside cages, nematode assemblages will be more abundant, but less species rich and diverse, than those in control sediments nearby.

Section snippets

Study site

Experiments were conducted at 2500 m water depth at the deep-sea long-term observatory HAUSGARTEN (Soltwedel et al., 2005), situated in the eastern Fram Strait west of Spitsbergen at approximately 79°N/4°E (Fig. 1). Circulation patterns in Fram Strait result in highly variable sea-ice cover, with our study site being generally ice-free during summer months. Photo/video footage from towed camera systems and remotely controlled vehicles has revealed the conspicuous presence of megafauna and

Environmental variables

Environmental variables from the first 2 cm of sediment did not differ between inside and outside the cages. The only exceptions were chl a and phaeopigments, which were both significantly higher inside the cages (Table 1). Mean chl a and phaeopigment concentrations were, respectively, 2.8 and 1.5 times higher inside the cages than in the control samples (Table 1).

Ordination by a correlation-based PCA of the environmental data showed a relatively clear distinction between cage and control

Discussion

At the genus level, nematode assemblages at our study site (regardless of treatment) were rather similar to those in other Arctic deep-sea regions. For instance, the seven most abundant genera, Thalassomonhystera, Microlaimus, Tricoma, Daptonema, Acantholaimus, Molgolaimus and Halalaimus, are in accordance with previous studies in the Arctic deep sea (Vanaverbeke et al., 1997; Vanreusel et al., 2000; Fonseca and Soltwedel, 2007; Hoste, 2006; Hasemann, 2006). The greater number of deposit

Acknowledgments

We thank the operational team of the remotely operated vehicle ‘Victor 6000’ (IFREMER/GENAVIR) and the crew of R.V. ‘Polarstern’ for their helpful support during the summer expeditions of 1999 and 2003. We are grateful to Ann Vanreusel for kindly making sediment analysis facilities at the Marine Biology Section of Ghent University available and Danielle Schram for performing the sediment analysis. Special thanks are due to Sérgio Netto, Tom Moens, Dr. Andrew Gooday and 3 anonymous reviewers for

References (103)

  • K. Iken et al.

    Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis

    Progress in Oceanography

    (2001)
  • R.S. Kaufmann et al.

    Activity patterns of mobile epibenthic megafauna at an abyssal site in the eastern North Pacific: results from a 17-month time lapse photographic study

    Deep-Sea Research I

    (1997)
  • H. Kukert et al.

    Disturbance, colonization and succession in a deep-sea sediment community: artificial-mound experiments

    Deep-Sea Research

    (1992)
  • L.A. Levin et al.

    Response of background fauna to disturbance and enrichment in the deep-sea: a sediment tray experiment

    Deep-Sea Research

    (1984)
  • S.A. Netto et al.

    Meiofauna communities of continental slope and deep-sea sites off SE Brazil

    Deep-Sea Research I

    (2005)
  • S.K. Service et al.

    Predation effect of three fish species and a shrimp on macrobenthos and meiobenthos in microcosms

    Estuarine, Coastal and Shelf Science

    (1992)
  • K.M. Sherman et al.

    The response of meiofauna to sediment disturbance

    Journal of Experimental Marine Biology and Ecology

    (1980)
  • C.R. Smith

    Food for the deep-sea: utilization dispersal and flux of nekton falls at the Santa Catalina basin floor

    Deep-Sea Research

    (1985)
  • L.D. Smith et al.

    Juvenile spot (Pisces) and grass shrimp predation on meiobenthos in muddy and sandy substrata

    Journal of Experimental Marine Biology and Ecology

    (1987)
  • D. Thistle et al.

    The effect of a biologically produced structure on the benthic copepods of a deep-sea site

    Deep-Sea Research

    (1990)
  • D. Thistle et al.

    The nematode fauna of a deep-sea site exposed to strong near-bottom currents

    Deep-Sea Research

    (1985)
  • D. Thistle et al.

    Are polychaetes sources of habitat heterogeneity for harpacticoid copepods in the deep-sea?

    Deep-Sea Research I

    (1993)
  • R. Turnewitsch et al.

    Bioturbation in the abyssal Arabian Sea: influence of fauna and food supply

    Deep-Sea Research II

    (2000)
  • W. Ulrich

    Regional species richness of families and the distribution of abundance and rarity in a local community of forest hymenoptera

    Acta Oecologica—International Journal of Ecology

    (2005)
  • A. Vanreusel et al.

    Meiobenthos of the central Arctic Ocean with special emphasis on nematode community structure

    Deep-Sea Research I

    (2000)
  • R.M. Warwick et al.

    Increased variability as a symptom of stress in marine communities

    Journal of Experimental Marine Biology and Ecology

    (1993)
  • R.M. Warwick et al.

    The effect of disturbance by soldier crabs, Mictyris platycheles H. Milne Edwards, on meiobenthic community structure

    Journal of Experimental Marine Biology and Ecology

    (1990)
  • M.C. Austen et al.

    Effects of biological disturbance on diversity and structure of meiobenthic nematode communities

    Marine Ecology Progress Series

    (1998)
  • F.A. Bazzaz

    Plant species diversity in old-field successional ecosystems in southern Illinois

    Ecology

    (1975)
  • S.S. Bell et al.

    Field evidence that shrimp predation regulates meiofauna

    Oecologia

    (1978)
  • J.M. Bland et al.

    Statistics notes: multiple significance tests: the Bonferroni method

    British Medical Journal

    (1995)
  • M.G. Chapman

    Are there adequate data to assess how well theories of rarity apply to marine invertebrates?

    Biodiversity and Conservation

    (1999)
  • K.R. Clarke et al.

    Statistical design and analysis for a “biological effects” study

    Marine Ecology Progress Series

    (1988)
  • K.R. Clarke et al.

    Changes in Marine Communities: an Approach to Statistical Analysis and Interpretation

    (2001)
  • J.H. Connell

    Diversity in tropical rain forests and coral reefs

    Science

    (1978)
  • J.H. Connell et al.

    Compensatory recruitment, growth and mortality as factors maintaining rain forest tree diversity

    Ecological Monographs

    (1984)
  • D. Desbruyères et al.

    Réactions de l’écosysteme bentique profound aux perturbations: Nouveaux résultats expérimentaux

  • K.E. Ellingsen et al.

    Taxonomic distinctness as a measure of diversity applied over a large scale: the benthos of the Norwegian continental shelf

    Journal of Animal Ecology

    (2005)
  • R.H. Findlay et al.

    Quantitative description of microbial communities using lipid analysis

  • R.H. Findlay et al.

    Efficiency of phospholipid analysis in determining microbial biomass in sediments

    Applied and Environmental Microbiology

    (1989)
  • G. Fonseca et al.

    Deep-sea meiobenthic communities underneath the marginal ice zone off Eastern Greenland

    Polar Biology

    (2007)
  • J.D. Gage

    Benthic biodiversity across and along the continental margin: patterns, ecological and historical determinants, and anthropogenic threats

  • J.D. Gage et al.

    Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor

    (1991)
  • K.H. Gaston

    Rarity

    (1994)
  • J.M. Gee

    Impact of epibenthic predation on estuarine intertidal harpacticoid copepod populations

    Marine Biology

    (1987)
  • J.M. Gee et al.

    Soft sediment meiofauna community responses to environmental pollution gradients in the German Bight and at the site of a former Dutch oil rig

    Marine Ecology Progress Series

    (1992)
  • A. Grant

    Deep-sea diversity: overlooked messages from shallow water sediments

    Marine Ecology

    (2000)
  • J.F. Grassle

    Slow recolonization of deep-sea sediment

    Nature

    (1977)
  • J.F. Grassle et al.

    Life histories and the role of disturbance

    Deep-Sea Research

    (1973)
  • J.S. Gray

    Animal–sediment relationships

    Oceanography and Marine Biology: an Annual Review

    (1974)
  • Cited by (0)

    View full text