Faunal response to different sources of heterogeneity on the Chilean margin
Meiofauna assemblages became more diverse (in terms of higher taxa) with increasing DO and decreasing organic carbon, due to increased abundances of fauna other than nematodes. The highest taxon diversity was observed at an upper slope site, with relatively high sand content off Chiloé, beyond the OMZ influence. This is also supported by the lower nematode/copepod ratio at this site. The reduction or absence of forms unable to tolerate low oxygen concentration in the OMZ, such as harpacticoid copepods, is well documented (Hicks & Coull 1983; Murrell & Fleeger 1989; Neira et al. 2001a). For this indicator of alpha diversity (taxon number), there is a positive effect of either sand content or release of negative effects of oxygen deficiency. However, no species data are available, and we still do not know how OMZ habitats add to beta or even gamma diversity for this group (i.e. are those OMZ-endemic species? if so, then they must be added to the regional species pool). Examples of OMZ endemics are Glochinema bathyperuviensis and Glochinema spinithorni, species apparently endemic to the OMZ bathyal sediments off Peru and Baja California, respectively (Neira et al. 2001b, 2005).
Studies off Peru indicate that beyond the OMZ habitat, sediment heterogeneity has more relevance in shaping meiofaunal higher taxa diversity compared to the OMZ core, where oxygen is the limiting factor. Different oxygen requirements of some species may explain vertical partitioning in the sediment by nematodes (Neira et al. 2001b; Neira & Decraemer 2009). In the deep sea, small-scale, biogenic relief generates heterogeneity that persists longer and contributes more to niche diversification than in shallow water, where water turbulence and rapid obliteration by sedimentation occur (Jumars 1975, 1976). Regarding the larger size classes, there were no correlations between the diversity attributes of macrofauna (S, N, H′, J′ and ES) and those of megafauna (e.g. S of macrofauna versus S of megafauna for the same stations), suggesting different response patterns to habitat characteristics. Megafaunal abundances were usually lowest at shallower stations; megafauna are almost excluded within the OMZ, in contrast with the abundant macrofauna dominated by a few species.
However, for both macro- and megafauna, the highest diversity was observed in general at the OMZ/AIW boundary or at deepest sites. A depth-related grouping of assemblages was reported by Palma et al. (2005) for the macrofauna. This in turn was explained by the different environments generated by the water masses involved, including dissolved oxygen as a main variable. The boundaries of the three important deep water masses in the region, the ESSW (down to about 400 m), the AAIW (500–1200 m depth), and the PDW (>1200 m depth), coincided quite well with the depth ranges of station groups and with specific species inventories in the study area (Palma et al. 2005). However, the causes for the change in species composition with depth are complex and several factors might act to produce the observed pattern. Indeed, zonation patterns in the deep sea have been attributed to physical and/or biological factors such as temperature (Rowe & Menzies 1969), pressure (Young et al. 1996), hydrographic conditions and topography (Lampitt et al. 1986; Rice et al. 1990), nutrient input (Rex 1981; Rice et al. 1990), larval dispersal (Rowe & Menzies 1969; Billett 1991), competition, predation and trophic level (Rex 1981; Cartes & Sardà 1992). Although many of these factors, if not all, could be acting off Chile to generate the observed patterns, the effect of the OMZ on macrobenthic communities is evident, with a community characterized by a low number of taxa, low species richness and diversity, and high dominance of a few species (Table 2). This was also reported by Levin et al. (2002) and Gallardo et al. (2004) for OMZ communities off Peru and central Chile, respectively, and during the onset of dysoxic conditions (i.e. bottom water dissolved oxygen <1 ml·l−1) at the shelf off Concepción (Sellanes et al. 2007). Indeed, only a few polychaete species were in general responsible for total biomass within the OMZ; among them, the polychaetes Aricidea pigmentata and Mediomastus branchiferus were the dominant ones (Quiroga et al. 2005). These species have been previously described as highly abundant in habitats associated with low-oxygen environments and high concentrations of organic matter (Gallardo et al. 1995; Carrasco et al. 1999). In terms of abundance, off northern Chile, the OMZ stations were dominated by polychaetes and oligochaetes, constituting about 90–100% of the macrofauna. The polychaete Magelona phyllisae and Oligochaeta sp. A (probably Olavius sp.) were the most abundant organisms in this area, followed by Cirratulus cirratus and Levensenia gracilis, although the latter also occurred outside the OMZ (Palma et al. 2005). In central Chile, the OMZ stations were dominated by the small-bodied polychaetes Cossura chilensis and Paraprionospio pinnata (Palma et al. 2005). Studies indicate that most of the more abundant polychaete species in this area are well adapted to cope with oxygen-deficient conditions by having enzymatic mechanisms associated with anaerobic pathways (González & Quiñones, 2000); P. pinnata is among the best adapted, displaying high activities of four pyruvate oxidoreductases, suggesting a high metabolic plasticity conferring the ability to thrive even in anoxic conditions. At stations beneath the OMZ, the larger polychaetes Paramphinome australis, Fauvelopsidae sp. A and Maldane sarsi, and the amphipod Ampeliscidae sp. A, showed higher densities (Palma et al. 2005; Quiroga et al. 2005).
Although indicators of alpha diversity are lower within the OMZ when compared with more oxygenated downslope habitats, the number of OMZ endemic species probably increases the regional inventory, thus adding to beta diversity. A review of beta diversity patterns (cumulative species turnover with depth) within different OMZs, including the same three transects off Chile discussed in this article, is presented by Gooday et al. (this volume). In general, on margins with an OMZ, species turnover is marked above the OMZ, is depressed within it and then increases again as DO levels begin to rise across the lower boundary. Off Chile, this depressed turnover within the OMZ is often caused by species that have been only reported for the OMZ core, and could thus be considered OMZ-endemics (an exception is P. pinnata, which is an opportunistic species that often proliferates in dysoxic conditions but is not an OMZ-endemic). An example of some of OMZ-endemic species is provided in Table 4. The relatively low number of these species reported so far for this margin does not necessarily mean that there are few OMZ-endemics, but is probably an effect of the paucity of taxonomic studies on deep-water benthic assemblages in the SE Pacific.
Table 4. Metazoan benthic species that have been collected only within the OMZ core along the SE Pacific margin.
|Size group||Class: Family||Species||Locality||Depth (m)||DO (ml·l−1)||References|
|Meiofauna||Nematoda: Epsilonematidae||Glochinema bathyperuvensis||off Callao, Peru (∼12°S)||305||0.017||Neira et al. (2001a,b)|
|Nematoda: Selachinematidae||Desmotersia levinae|| || || ||Neira & Decraemer (2009)|
|Macrofauna||Oligochaeta: Tubificidae||Olavius crassitunicatus||off Callao, Peru (∼12°S)||305||0.017||Levin (2003)|
|Polychaeta: Cirratulidae||Aphelochaeta multiflis||off Concepcion, Chile (∼36°S)||124||0.45||Palma et al. (2005)|
|Polychaeta: Dorvilleidae||Diaphorosoma sp.||off Quique, Chile (∼20°S)||313||<0.5||Levin (2003)|
|Polychaeta: Sabellidae||Chone chilensis||off Antofagasta, Chile (∼22°S)||98||0.02||Palma et al. (2005)|
|Polychaeta: Syllidae||Sphaerosyllis sp.||off Antofagasta, Chile (-22°S)||98||0.02||Palma et al. (2005)|
|Megafauna||Mollusca: Columbellidae||Astyris sp.||Callao, Peru to Antofagasta, Chile (12°–22°S)||305–319||0.017–0.06||Levin et al. (2002); Quiroga et al. (2009)|
|Mollusca: Ischnochitonidae||Tripoplax balaenophila||off Concepcion, Chile (∼36°S)||240||<0.5||Schwabe & Sellanes (2004)|
|Mollusca: Leptochitonidae||Leptochiton sp.||off Antofagasta, Chile (∼22°S)||319||0.06||Schwabe and Sellanes (in press)|
Enhanced species richness and diversity of macrofauna and megafauna was observed at the sites just beneath the OMZ (e.g. >500 m off Antofagasta and >365 m off Concepción, Table 2). Consistent with this, another characteristic reported for the benthic assemblages within and beyond the OMZ at many sites, is a sharp zonation within the lower OMZ transition zone (e.g. Volcano 7 off Mexico –Levin et al. 1991; Wishner et al. 1995; Oman –Levin et al. 2000; Chile –Gallardo et al. 2004; Pakistan margin –Levin et al. 2009). This feature has been explained by the different tolerance thresholds to low oxygen concentrations by different groups (Gooday et al. 2009). In general, annelids are more tolerant than mollusks, followed by crustaceans and the echinoderms, with the last being the least tolerant (Díaz & Rosenberg 1995; Vaquer-Sunyer & Duarte 2008). All these observations strongly suggest that the OMZ boundaries constitute highly heterogeneous sub-zones in terms of environmental conditions with, in general, abrupt shifts in animal communities, sometimes at vertical scales of tens of meters (e.g. at the Pakistan margin –Levin et al. 2009).
Local heterogeneity influence on regional-scale diversity
The macrofauna of the Chile margin seeps have yet to be studied, but may include additional species not characteristic of the other habitats. Levin et al. (this volume) found that nearly half of the seep macrofauna present on the Oregon and California margin (500–800 m depth) were seep endemics, not present in OMZ or other slope settings.
The maximum megafaunal species number and rarefied species richness were always observed below the OMZ, but a little bit deeper than the maximum observed for the macrofauna, at mid slope depths (e.g. below 1347 m off Antofagasta and at 1294 m off Concepción). However, for the megafauna, the maximum number of species (considering all sites) was observed at the seep site (CMSA), although local diversity (H′) and rarefied species richness was moderate. At the CMSA the overall increase in abundance, biomass, and diversity of the heterotrophic megafaunal communities, including top predatory fishes, is not a function of increased local primary production, because stable isotope analysis indicates that there is no reliance on in situ (chemosynthetic) production (Sellanes et al. 2008). However, methane-derived authigenic carbonates provide a suitable habitat for sessile organisms and associated fauna, and this hard substratum may in turn provide a rich feeding ground for other mobile species. This has been also suggested for the Gorda Escarpment off northern California, where multispecies aggregations of octopus (Benthoctopus sp. and Graneledone sp.) and blob sculpins (Psychrolutes phrictus) brood at seep sites. This preference has been ascribed to the interaction of local topography, physical, and geological settings (Drazen et al. 2003).
As indicated by rarefaction analysis (Fig. 5), in general, species number and diversity increase toward higher latitudes, with the diversity peak tending to be found at shallower depths in the same direction. Off Chiloé, where the OMZ was absent, a high diversity and number of species were recorded at 480 m. This coincided with the presence of hardgrounds, evidenced by underwater images and trawled rocks at this site (Fig. 4I, Hebbeln 2001). Megafauna is the only group that has been studied off Chile for regular slope, OMZ and seep habitats. In spite of the low diversity, megafaunal assemblages within the OMZ have some endemic species (Table 4), such as the columbellid gastropod Astyris sp. (Quiroga et al. 2009) and a new species of polyplacophoran, Leptochiton sp., with an enhanced number of branchial structures (Schwabe & Sellanes submitted). On the other hand, seep sites with a high local diversity also contribute to regional diversity, with many endemic species. For instance, at the CMSA off Concepción, 112 megafaunal species have been reported by Sellanes et al. (2008); 11 of them are seep endemics (chemosymbiotic clams and polychaetes, and their commensal fauna) and at least 10 other species are new to science, i.e. so far only known from this site. Thus, both habitats, seeps and OMZ sediments, increase the regional pool of species, although to different degrees. It has been postulated that at a regional scale, OMZs can act as a barrier to gene-flow between allopatric populations, creating strong vertical gradients in physical and biological parameters (White 1987; Rogers 2000). Along with a limited utilization of sinking organic matter in the OMZ water column, which results in an abundant supply of food for organisms immediately below it, this may lead to strong vertical gradients in selective pressure for optimal rates of growth, modes of reproduction and development, interaction with other species. These selective agents, combined with increased habitat specialization in the lower boundaries of OMZs, may translate into enhanced regional biodiversity.
The results suggest that the bathymetric distribution of sublittoral benthic organisms of the Chilean margin are controlled largely by the water masses occurring in the region, which modulate bottom-water oxygen conditions and sediment organic loading, whereas hardgrounds, when present, constitute faunal attractors primarily for larger organisms. However, as indicated in the previous section, different taxa, and even different size groups, have a distinct response to these environmental factors, including the still poorly studied small fauna associated to carbonates. Physiological adaptations to oxygen deficiency and constraints related to body size of each group would be responsible for the large-scale patterns (e.g. zonation and latitudinal trends), whereas habitat heterogeneity (e.g. at water mass boundaries, heterogeneous sediments, seeps) would explain the local fauna diversity patterns and the occurrence of many endemic species.