Zonation patterns of intertidal meiofauna/nematodes

Intertidal meiobenthic species inhabit specific zones according to their ecological requirements, life cycle, feeding habits and interactions with other organisms (Giere, 2009). Generally, the zonation pattern of meiofauna is a reflection of their responses to both physical and biological factors. More specifically, distribution patterns of meiofauna in sandy beach habitats can be divided into vertical and horizontal zonation (McLachlan and Turner 1994; McLachlan and Jaramillo 1995; Giere 2009; Moens et al. 2013; Urban-Malinga 2014). Below we briefly describe horizontal and vertical patterns of meiofauna distribution.

3.4.1

Horizontal zonation patterns

McLachlan and Jaramillo (1995) have described four different types of horizontal zonation of fauna on sandy beaches, namely: 1) no clear zonation; 2) two zones delimited by the driftline; 3) three zones of supralittoral, littoral and sublittoral, according to Dahl’s (1952) classification; and 4) four physical zones, a dry zone, a zone of water retention, a zone of resurgence, and a zone of saturation based on sediment moisture. These horizontal zonations are reflected in the distribution patterns of both macrofauna and meiofauna and can be important in planning of biodiversity surveys.

It has been reported that in sandy beaches, benthic zonation is predominantly controlled by

physical forces related to wave exposure, which in turn influence other habitat parameters,

including granulometry (sediment grain size and sediment structure) (McLachlan and Brown 2006; Schlacher et al. 2008). They also influence the fluctuations of other environmental variables such as water table level, temperature and salinity (Hinton 2000; Li et al. 2000; Urish and McKenna 2004).

As part of the physical forces mentioned above, the tidal level has been identified as one of the major factors influencing the horizontal patterns of meiofauna. Indeed, the concept that meiofauna assemblages change along a gradient perpendicular to the waterline has been well

37 recognized (Warwick 1971; Hodda and Nicholas 1985). Several reports have found significant differences in meiofaunal densities among intertidal positions, showing that

densities increase from the upper towards the lower littoral zone (Hodda and Nicholas 1985;

Ólafsson 1991; Gheskiere et al. 2002; Kotwicki et al. 2005). In fact, nematode assemblages at the lower intertidal are often considered an extension of, and not fundamentally different from, subtidal nematode assemblages (Gheskiere et al. 2004; Maria et al. 2013b). However, some exceptions with highest densities in the upper beach zone exist (Rodriguez et al. 2001). The density pattern of marine nematodes resembles the usual pattern for macrofauna, but the diversity pattern does not: in macrofauna, density and diversity both tend to increase towards the lower intertidal, whereas in meiofauna diversity more commonly peaks at the mid-tidal level (see below) (Fig. 1-12).

Regarding the beach type, McLachlan and Turner (1994) have stated that optimum conditions

for the existence of a diverse and abundant meiofauna occur in intermediate beaches. Their

prediction was based upon the fact that beaches with intermediate morphodynamic characteristics represent an equilibrium state between organic inputs (which increase towards the dissipative beach state) and oxygenation conditions (which increase towards the reflective beach state) (McIntyre 1969; Ott 1972). On the scale of a single beach, essentially the same equilibria may explain the occurrence of diversity peaks of meiofauna around the mid- intertidal (Armonies and Reise 2000; Gheskiere et al. 2004; Gingold et al. 2010; Maria et al. 2013b) (see below for more info).

38 Fig. 1-12. Conceptual diagram of typical across shore gradient in meiofauna and macrofauna abundance and diversity.

Regarding the effect of tidal level on the horizontal diversity pattern of marine nematodes, it has been demonstrated that nematode species diversity often increases from lowest values at the upper littoral to a maximum around the mid-tidal level and then again decreasing – albeit not drastically – towards the low-water line (Armonies and Reise 2000; Gheskiere et al. 2004; Gingold et al. 2010). This is in contrast with macrobenthos diversity, which generally increases almost linearly from the upper to the lower intertidal. This trend may be explained by a direct dependence of feeding activity in many macrofaunal species on tidal submergence (Armonies and Reise 2000). The unimodal diversity pattern of meiofauna is why in the present study, we sampled from this mid-intertidal zone. Higher diversity at the middle beach can be attributed to the fact that an optimal balance among desiccation/temperature/salinity stress, hydrodynamic disturbance and sediment stability, food availability and oxygen concentration is usually reached somewhere in the mid-intertidal. As such, nematode diversity gradients across beaches may provide a good illustration of both the intermediate disturbance

hypothesis (IDH) (Connell 1978) and the dynamic equilibrium hypothesis (DEM) (Huston

1979). The IDH predicts that species diversity will be highest at intermediate levels of disturbance (here the combination of hydrodynamic disturbance and physiological stress following from low-tide exposure), whereas the DEM predicts that the effect of disturbance or

39 stress on diversity depends on productivity (here the availability of organic matter). Another point is that the middle beach is a transitional area, with a mixture of swash and surf zone processes, which allows the co-occurrence of species from both the upper beach and the subtidal (McLachlan and Brown 2006; Maria et al. 2013b). In the study of Maria et al. (2013b), 63 % of the nematode species occurring in the middle beach were also found in the upper beach and/or in the subtidal. Furthermore, biological factors, such as predation and competition for food, are also known to play a key role for the establishment and maintenance of meiofauna zonation on sandy beaches (Snelgrove and Butman 1995; Giere 2009; Maria et al. 2011b; Maria et al. 2012).

In addition, the presence of particular ‘microhabitats’ on beach can interfere with the above- discussed horizontal diversity and density patterns of nematodes on sandy beaches. Gingold et al. (2010) demonstrated that beach microhabitats (runnels and sandbars) differed in environmental conditions and possessed significantly distinct nematofaunal assemblages. Runnels featured higher levels of taxonomic and functional diversity, while sandbars possessed a more homogeneous nematode community. In contrast with sandbars, in which food (organic matter and microbenthic algae) is scarcer, runnels remain submerged over a longer period of time and accumulate organic matter. Consequently, the runnel community with relatively calm conditions exhibited a higher degree of patchiness around food sources resulting in small-scale aggregations and clumped distributions, presumably owing to a predominance of active displacement under calmer conditions and sediment cohesion by algal films (Gingold et al. 2011). Maria et al. (2013b) also reported that nematode communities from runnel and sandbar habitats are significantly different at macrotidal ridge-and-runnels beaches in the North Sea.

3.4.2

Vertical patterns

Vertical zonation of the meiobenthos is generally controlled by oxygen and the position of the redox discontinuity layer, RPD (McLachlan and Jaramillo 1996; Steyaert and Vincx 1996; Steyaert et al. 2003). The RPD is a distinct redox-cline which marks the transition between oxidized and reduced conditions in the sediment (Gray 1981). The position of this layer is controlled by hydrodynamic forces, sediment properties (such as grain size) and organic content of the sediment. These abiotic factors are in fact variable in the different habitats and

40 this is reflected in different vertical distribution patterns of meiofauna, which in turn exhibit "taxon" (e.g. Nematoda tend to be more tolerant to hypoxia than harpacticoid copepods (Modig and Ólafsson 1998; Moodley et al. 2000) and species-specific (see e.g. Steyaert et al., 2007) tolerances to reduced oxygen concentrations.

Both long and short-term effects of oxygen on vertical distribution of meiofauna can be important. Reports have indicated that long oxygen stress (longer than 2 months) can cause changes in meiofaunal community structure and vertical distribution patterns (Moodley et al. 1997; Wetzel et al. 2002). Yet, short-term exposure to hypoxia and/or anoxia can also profoundly affect nematode abundances and decimate populations of common species, including some which are generally considered fairly tolerant to reduced oxygen conditions (Steyaert et al., 2007). It is not always clear whether such impacts are the direct consequence of hypoxia or rather an indirect result through increased concentrations of toxic sulfides under low-oxygen concentrations (Wetzel et al. 2001; Wetzel et al. 2002; Steyaert et al. 2007).

Coarser (permeable) sediments are generally more oxygenated with a deeper RPD, whereas in finer sediments or in non-permeable sediments, meiofauna can be largely restricted to the upper first cms or mms of the sediment (Coull, 1988). Numerous studies (McLachlan 1978; Ólafsson and Elmgren 1997; de Jesús-Navarrete and Herrera-Gómez 2002; Kotwicki et al. 2005) have reported highest meiofauna densities in the top 10 cm of beach sediments, while Martins et al. (2015) reported the highest meiofauna densities in the 10-30 cm strata in southeast/southern Brazilian reflective beaches. In the latter study, the higher abundance of meiofauna in intermediate strata (10-30 cm) was potentially caused by the migration of organisms in an attempt to escape the physical stress caused by the wave impact and the desiccation characteristic of the intertidal zone (Urban-Malinga et al. 2004). In addition, it has been reported that in well-oxygenated sandy beaches, meiofauna occasionally can be distributed to depths of 50 cm or deeper (McLachlan and Brown 2006). For example, Munro et al. (1978) recorded nematodes down to 105 cm at such well-oxygenated beaches. Such distances are too large to be explained by active downward migration alone. They could, however, partly relate to passive up- and downward migration of nematodes with the sediment water table during incoming and outgoing tides, a phenomenon which can be very pronounced particularly in coarser sediments near the upper littoral (McLachlan et al. 1977; Urish and McKenna 2004). Another factor which also affects the depth of the RPD zone is seasonal temperature variations. With increasing summer temperatures, the RPD layer will

41 move upwards, resulting in change in meiofaunal assemblages. This factor can be particularly important on exposed sandy beaches, where seasonal temperature fluctuations can be considerable (Harris 1972b).