Effects of sediment disturbance on deep-sea nematode communities: Results from an in-situ experiment at the arctic LTER observatory HAUSGARTEN

Highlights

• Experimental attempt to create small-scale disturbance at LTER observatory HAUSGARTEN.

• Impact of small-scale habitat structure on deep-sea benthic nematode communities.

• Diversity is maintained by habitat heterogeneity created by disturbances.

• Lander and ROV based in situ experiment to avoid artefacts in deep-water studies.

Abstract

The present study examines the effects of experimentally generated disturbance on bathyal nematode communities at the LTER (Long-Term Ecological Research) observatory HAUSGARTEN, situated in the Fram Strait, between Greenland and Svalbard. In order to understand the complex interactions between the biota and environmental perturbations we deployed a free-falling device (bottom lander) equipped with three rotating fork-like disturber units, able to perturbate the upper sediment layers with different disturbance frequencies at chosen time intervals. During a one-year deployment at 2493 m water depth, disturber unit DI was programmed to rotate every 14 days, DII every 28 days, and DIII every 72 days, resulting in 28, 14, and 7 perturbations, respectively. Sediment sampling following this experimental period was conducted with push-coring devices deployed by the Remotely Operated Vehicle “QUEST 4000” (MARUM, Bremen). These sediment cores were sub-sampled to determine the effect of the sediment perturbations on various sediment parameters (i.e., grain size distribution, chloroplastic pigment concentrations) as well as on benthic nematode communities.

A total of 4773 nematodes from 27 families and 81 genera were identified. Nematode densities in the disturbed areas ranged from 617 ind. / 10 cm² to 1566 ind. / 10 cm², with a mean density of 1193 ind. / 10 cm² observed overall in the disturbed sediments. Control sediments contained on average 20% more nematode specimens than were found within the disturbed sediments, with an average density of 1477 ind. / 10 cm² observed. Nematode evenness (J'), genera richness (EG₍₅₁₎) and heterogeneity (H′) were not significantly different between the treatments and controls (undisturbed vs disturbance). We found a significant effect of the interaction of disturbance frequency and sediment depth (interaction term Fr x De) on heterogeneity and genera richness, while evenness significantly differed between different sediment depths (De) and within the disturbed sediments between different disturbance frequencies (Fr). Although surface sediments in the three disturbed areas were effectively perturbated, sediment depth still has the most pronounced influence on nematode community attributes, while the experimentally induced disturbance had only a limited impact on nematode diversity and community structure. Although we found the density of some nematode genera was negatively affected by the disturbances, the deep-sea nematode community at HAUSGARTEN was generally characterized by a relatively high diversity and seemed to be largely resilient to the experimental disturbances.

Introduction

The deep sea is a far more quiescent environment when compared to shallow-water and coastal systems. Temperature, salinity, and dissolved oxygen content fluctuate within a very narrow range at abyssal depths, where food availability is generally limited (Pfannkuche, 1993) and the benthic communities appear to be particularly adapted to these stable environmental conditions. Therefore, it may be hypothesized that any kind of disturbance may play a particularly important role in shaping benthic communities in the deep sea (Dayton and Hessler, 1972; McClain and Schlacher, 2015, and citations therein), by influencing density, distribution and diversity of the communities (Snelgrove and Smith, 2002). Deep-sea assemblages respond to environmental and biological changes or habitat modification in highly complex and variable ways. Nevertheless, some general diversity and distribution patterns have been observed, with differing hypotheses having been applied to explain these patterns and elucidate the underlying processes (Moens et al., 2013). For example, the Intermediate Disturbance Hypothesis (IDH, Connell, 1978) and the Intermediate Productivity Hypothesis (IPH, Grime, 1973a, Grime, 1973b, Grime, 1979, Grime, 2001) predicts that highest diversity occurs at an intermediate level of disturbance or productivity. Maximum diversity would therefore be found at a state of non-equilibrium (Connell, 1978; Huston, 1979; Kukert and Smith, 1992; Gage, 1996). The IDH has been applied to a number of benthic communities. Dayton and Hessler (1972), Rex, 1976, Rex, 1981, and Huston (1979) used the IDH to explain high deep-sea diversity (Gallagher, 2008), with diversity and species richness of benthic fauna peaking at bathyal depths (Boucher and Lambshead, 1995).

The effects of productivity and disturbance on the general patterns of species richness among organisms that compete with one another have been illustrated using a dynamic equilibrium model (DEM) of species richness (Huston, 1979, Huston, 1994). In the context of the DEM, the IDH is a special case that occurs only under certain conditions, where productivity and population growth rates are also intermediate (Huston, 2014). The validity of the IDH has been analyzed for different compartments of the benthic fauna in several deep-sea habitats at bathyal and abyssal depths (Boucher and Lambshead, 1995; Paterson and Lambshead, 1995; Cosson-Sarradin et al., 1998; Ingole et al., 1999; Hasemann and Soltwedel, 2011; Ashford et al., 2019).

Accumulated evidence has been published indicating that disturbance is not uncommon in the deep sea and acts across multiple scales and through multiple processes. However, the exact responses consequential of the many diverse forms of disturbance which may impact on deep-sea diversity are difficult to predict at present (McClain and Schlacher, 2015).

Among the different concepts of disturbance, in the present study we primarily followed the definition given by Pickett and White (1985), focusing on patterns of change on nematode communities that follow a disturbance defined as “a discrete, unpredictable event in time that removes organisms, brings mortality to them, or otherwise disrupts the ecosystem, community or population structure by influencing the availability of resources and substrates or by changing the physical environment”. Disturbance can occur across a variety of spatial and temporal scales and includes events induced by biological (i.e., bioturbation and predation) or physical sources (i.e., turbidites, near-bottom currents, bottom trawling) (Harris, 2014; Rosli et al., 2018). On larger scales, physical disruption of the sediment by e.g., bottom trawling, deep-sea mining, strong currents, or benthic storms can have pronounced effects on deep-sea soft-sediment communities (Thrush and Dayton, 2002; Buhl-Mortensen et al., 2015). The essential aspect of large-scale physical disturbances (from whatever origin), is the movement and displacement of deep-sea sediments. At smaller scales, natural disturbance such as bioturbation and predation, but also physical disturbances mainly influence the vertical patterns in the distribution of smaller sediment-inhabiting organisms, i.e., the meiofauna (Lambshead et al., 1995; Moodley et al., 2000; Heip et al., 2001; Pusceddu et al., 2014; Rosli, 2017; Soltwedel et al., 2018).

Various studies have shown that bioturbation by macro- and megafauna enhances meiofauna abundance in subsurface sediment layers through increased downward transport of food (Lambshead et al., 1995; Moodley et al., 2000). In fact, perhaps the most important factor in the structuring of soft sediment communities is the spatio-temporal availability of organic matter (Snelgrove et al., 2000), which is the main food / energy source for benthic organisms. As the input of organic matter to the seafloor is patchy and unpredictable in space and time, the episodic nature of the input of settling organic matter can be considered as a disturbance event, especially in the low-energy and generally food-limited deep-sea environment.

To summarize, sediment-inhabiting organisms may react to physically or biologically mediated effects or a combination of both. In this sense, the interaction of physically mediated effects and resultant biological processes maintains heterogeneity in benthic environments, and thereby determining the overall structure and diversity patterns of benthic communities, including those in the deep sea.

The present study examines the effect of experimentally generated disturbance on bathyal nematode communities in the deep Fram Strait, Arctic Ocean. Nematodes are the dominating taxon in metazoan meiofauna, both in terms of abundance and biomass (Heip et al., 1982; Mazurkiewicz et al., 2016), and play an important role in the sedimentary ecosystem of the deep sea (Lambshead et al., 2000; Vanreusel et al., 2000, Vanreusel et al., 2010; Lambshead, 2004). Nematodes are therefore useful tools for understanding the processes that determine benthic diversity in the deep sea.

To study the response of sediment-inhabiting nematode communities, both in terms of community composition and density, to physical disturbance events, disturbances acting at different frequencies were artificially generated. Vertical shifts in nematode distribution patterns and changes in environmental conditions were analyzed along the different disturbance frequencies on centimeter scales. Specifically, we hypothesized that:

(1) physical disturbance has an indirect effect on nematode distribution patterns by modifying sediment characteristics and food availability along different disturbance frequencies;

(2) physical disturbance has a direct effect on nematode distribution patterns by modifying nematode densities along different disturbance frequencies;

(3) indirect and direct effects of physical disturbance mediate vertical patterns of nematode distribution, with depth-related dominance patterns shifting along different disturbance frequencies;

(4) indirect and direct effects of physical disturbance mediate diversity patterns of nematode communities along different disturbance frequencies, with diversity peaking at an intermediate level of disturbance.