RICERCA ITALIANA     

Contribution of meiofauna to marine biodiversity of the Italian coasts

Università degli Studi di Sassari

Abstract

Meiofauna is one of the potentially more promising fields in marine research. Among other aspects, it constitutes a veritable 'new frontier' of systematic studies (it only needs to mention that all the newly described phyla belong to the meiofauna!), and its contribution to marine biodiversity is particularly significant. This notwithstanding, the number of researchers in the field is dwindling worldwide. Such 'taxonomic bottleneck' appears particularly stigmatizable, considering the widespread phenomena of global change, which are affecting our planet. In fact, the synergism of temperature rise, range shift and other stresses, in particular habitat destruction, introduction of exotic species, and spreading of pathogens, could disrupt the connectedness among species and lead to a reformulation of species communities, reflecting differential changes in species, and to numerous extirpations and possibly extinctions. Meiofauna taxa, characterized by short life cycles, fast metabolic rates, limited distribution (at least in the cases in which the application of techniques of molecular taxonomy has contributed to the resolution of sibling species complexes) and lack of dispersal larval stages, appear as ideal candidates to follow the evolution of the process in the sea. A paradox is thus evident, with the faunistic group, which could represent a useful indicator of the effects of global change on marine communities, which is in reality the most poorly known fraction of the whole marine fauna.
Present project represents a significant contribution towards a change of attitude towards meiofaunal studies, by means of the mobilization of most Italian researchers active in the field of taxonomy of meiofaunal groups. Synergism among different expertises will allow a broad-range taxonomic research, at a level never attempted before, on the biodiversity of meiofauna at different levels:
1) Species level, with the production of checklists of meiofaunal species present in three areas, chosen as biogeographically paradigmatic for the Italian coasts. Particular attention will be devoted to the resolution of sibling species complexes, whose presence appears pervasive among meiofaunal taxa, by means of molecular, morphological, and karyological analysis, as well with the contribution of studies on reproductive biology. In addition, habitats never or only rarely sampled so far (such as marine caves and dysoxic environments) will be explored.
2) Community level, through the analysis of community structure and seasonal dynamics in sites representative of the same biotic communities.
3) Population level, through the analysis of population genetic structure of selected taxa. Comparisons among taxa, pertaining to different phyla, will allow inferences about dispersal strategies as well as phylogeographical reconstructions.
The data set obtained for the Italian coasts as well as for biogeographically strategic areas of the Mediterranean, where sampling campaigns are planned, will allow to identify areas of faunistic homogeneity, and to analyze the consistency of biogeographical patterns across meiofaunal taxa.
Present programme is furthermore aimed to the formation of mainly post-doc students in the challenging field of the taxonomy of meiofaunal groups, whose study has been particularly affected by the taxonomy crisis of latest decades. <<<

Principal Investigator

Marco CURINI GALLETTI Università degli Studi di SASSARI

Research Objectives

The recent Symposium on Marine Biogeography of the Mediterranean (XXXIV Congresso SIB, Ischia, October 21-24, 2002) evidenced that i) present state of knowledge of systematics and biogeography of meiofauna groups is among the poorest of the whole Italian fauna, and that ii) this lack of knowledge is particularly regrettable, considering the overwhelming contribution of meiofauna to marine biodiversity (Bianchi & Morri, 2002). Furthermore, such 'taxonomic bottleneck' raises particular concern, at the light of recent phenomena of global change that are affecting our planet. As a consequence of present climatic changes, in fact, we can expect future latitudinal shifts in the marine biota of 300-600 km in the next 50 years (Southward et al., 1995; Warwick & Turk, 2002). The synergism of rapid temperature rise, range shift, and other types of stress, such as habitat destruction and introduction of exotic species, could lead to a reformulation of species communities and to numerous extirpations, and possibly extinctions (Root et al., 2003). Documentation of the process in the sea is however mostly based on vagile species (often particularly conspicuous, such as fishes) or with planctonic larval stages, where it might be difficult to discriminate between long-term range shift from accidental reports outside the normal range of the species. On the contrary, range shifts in more sedentary species follow from slow processes of population extinctions and colonizations, factors that made such species particularly suitable to follow the evolution of the phenomenon in land (Walther et al., 2002). Meiofauna, characterised by short life cycles and lack of dispersal stages, appears thus as an ideal candidate for monitoring the effect of global warming in the sea - yet, it is among the least known fractions of the marine fauna. Furthermore, present paucity of data on composition and distribution of meiofauna groups hinders our capability to recognize exotic species, and the problem of cryptogenicity (Carlton, 1996) is expected to assume more and more relevance in meiofaunal groups.
Present project aims to contribute significantly to the resolution of the problem, through the active involvement of the italian researchers active in the field of systematics of meiofaunal organisms. Synergism of different expertises will allow a broad-range taxonomic research, aimed to:
1) inventory of meiofauna biodiversity of the italian coasts.
Due to the constraints of a biennial project, research will be performed in three areas, located in the geographic sectors acknowledged for the Italian coastline by the 'Checklist of species of the Italian Fauna'. For each area, a comprehensive checklist of the meiofauna species present, will be produced. A collaboration with external taxonomic authorities is envisaged, for groups whose specific competence is not present in our team. Such survey, produced by the interaction of different expertises in meiofaunal groups, has been scarcely attempted previously, and will make Italian coasts among the best known areas in the world, as far as meiofauna is concerned. Particular attention will be devoted to the resolution of sibling species complexes, pervasive in meiofauna, mainly by means of molecular techniques. Furthermore, habitats never or scarcely studied hitherto will be sampled - such as submarine caves and carbonatic sediments, which preliminary surveys have suggested to harbour high species diversity. The data set obtained for the Italian coasts, as well as for biogeographically strategic areas of the Mediterranean, where further sampling campaigns are planned, will allow to identify areas of faunistic homogeneity, and to analyse the consistency of biogeographical patterns among meiofaunal taxa.
2) analysis of meiofauna biodiversity at the community level.
As a result of their high abundance, rapid generation times, and fast metabolic rates, meiofaunal organisms play an important role in ecosystem function. Thus, the state of meiofaunal assemblages may reflect the overall health of the marine benthos (Kennedy & Jacoby, 1999). The vast majority of research in the field of meiofaunal communities has been so far limited to the study of the Copepoda/Nematoda fraction (the only organisms easily retrievable from fixed samples), with identifications of organisms, with few notable exceptions (e.g. Ceccherelli & Mistri, 1990), at higher taxonomic levels (from genus to phylum!). Our project is aimed to analyse meiobenthic communities, for the majority of taxa, at the species level. Such investigation, which, for the first time, implies a synergism among numerous expertises, will yield information on the actual contribution of 'soft-bodied meiofauna' to the overall meiofauna diversity, as well as data, such as structure of community and seasonal dynamics, integrative of the checklists obtained by qualitative studies. These data will further enable comparisons of species composition and community structure in the same habitats among different areas.
3) analysis of meiofauna biodiversity at the population level.
Population genetic structure of paradigmatic taxa will be investigated. Comparisons among taxa, pertaining to different phyla, will allow inferences about dispersal strategies, as well as phylogeographical reconstructions, aimed to add information about the so-called 'meiofauna paradox' (see Giere, 1993).
Curricula of senior researchers of the four Units partecipating to the project present high level publications in systematics of their own groups, thus showing that basic facilities in their laboratories are adequate to support research as planned in present project - although some upgrading might be desiderable (as indicated by a few Research Units). Furthermore, the fundings requested appear to be the minimum realistically possible for the fulfillment of the project. Part of the limitation of the budget is basically due to the strong synergism among groups, which includes joint sampling campaigns and facilitations such as free use of laboratories and lodging in one of the sites chosen for research. A significant share of the budget will be allocated to financing scholarships and research grants. In fact, an exigency much felt by all the Units partecipating to the project is the need to contribute to the recruitment of a new generation of taxonomists in groups of the meiofauna, whose study has been severely affected worldwide by the taxonomy crisis of the latest decads. Furthermore, a relevant novelty of the project is the fact that all information gathered (checklists of species, identification keys, reports of possible endemisms of the geographical sectors) will be also made available on the web, in already chosen sites.
In summary, the project, which stems out from the co-operation of the research teams active in Italy in the field of systematics of meiofaunal taxa, aims to contribute significantly, in a two year period, to the knowledge of biodiversity (at population, species and community level) of biogeographically paradigmatic areas of the italian coasts and of the Mediterranean, and places special emphasis on synergism among groups and on the formation of new taxonomists. Researchers partecipating to the project are particularly motivated to document the present status of biodiversity of the meiofauna as a basis for the appreciation of future environmental modifications - and have been so far limited in their purpose by lack of fundings, that, already scarce in general in systematic research, have particularly penalized research on 'inconspicuous' organisms. <<<

First Results

Expected results of Phase 1 are as follows:
- Accomplishment of qualitative and quantitative sampling campaigns in the three areas chosen;
- Identifications of sites in marine caves, dysoxic environments and carbonatic sediments suitable for research; accomplishment of a preliminary series of samplings;
- Samplings in selected extra-italian areas;
- Accomplishment of the analyses possible on fresh samples; fixation of material for further analyses;
- Identification of target species for phylogenetical studies, population genetic structure, and reproductive biology experiments;
- Standardization of experimental protocols for genetic markers;
- Production of preliminary faunistic inventories of meiofauna groups for the areas studied; in particular, the first inventories of marine Rotifera for the whole Mediterranean will be produced.At the end of Phase 2, the main expected results will be:
- Contribution to the faunistic knowledge of protected areas of major naturalistic interest, by means of the elaboration of checklists and catalogues of lesser-known invertebrate groups, which are generally neglected in faunistic surveys;
- New and pre-existing faunistic and distributional data will allow a better estimate of the global biodiversity of the Italian seas. Moreover, data acquired during the research will provide information for assessment and monitoring of the effects caused by climatic and ecological changes acting in the Mediterranean Sea.
In particular, at the end of Phase 2, the following results will be achieved:
- Production of checklists of meiofaunal taxa for the areas chosen, and of the first checklist of Rotifera for the Mediterranean. For such group, furthermore, the first comparisons among marine populations of different substrata and environments will be performed, the spatio-temporal community dynamics analyzed, and the actual presence of clonal structure and resistance stages in marine species investigated;
- Analysis of the presence of sibling species in meiofauna, by means of molecular, karyological, morphological and biological-reproductive approaches;
- Contribution to the phylogenetical knowledge of taxa of meiobenthos, by means of molecular and morphological studies of species of particular phylogenetical relevance found during the research;
- Analysis of composition and distribution of taxa of the meiofauna, resulting in a significative improvement of present state of knowledge of the biogeography of mediterranean meiofauna;
- Analysis of genetic population structure, as a tool for the understanding of dispersal capability of selected taxa and as bases for phylogeographical reconstructions;
- Analysis of meiofaunal community structure, and assessment of the actual contribution of the 'soft bodied meiofauna' to diversity of meiofauna;
- Formation of specialistic expertise on meiofauna taxonomy;
- Divulgation of results by means of publication on the web, presentations to scientific meetings, and production of scientific publications. <<<

Timescale

24 months

National and international background

The overwhelming value of biodiversity as an indication of environmental health and for the functioning of ecosystems is now largely documented (cf Culotta, 1996; Johnson et al., 1996). However, while numerous studies have addressed the issue of conservation of biodiversity on land, marine habitats have so far received much less attention (Cognetti & Curini Galletti, 1993; Ormond, 1996; Carlton et al., 1999; Bianchi & Morri, 2000). It is now clear that marine ecosystems are equally at risk, and that those marine ecosystems that receive the most sustained and unrelenting pressure from human activities are particularly vulnerable (Roberts et al., 2002). The few documented cases of extinction of marine animals, which concern vertebrates (mainly mammals and birds) and very few macroinvertebrates, restricted to brackish habitats or excessively exploited commercially (Roberts & Hawkins, 1999), are among the factors responsible of the delayed awareness of the urgency to protect marine biodiversity. This may reflect intrinsic differences of the marine environment compared to terrestrial habitats, namely the high connectivity of the marine system, and a generally much higher population size. A growing awareness is however rising, that present perception of marine biodiversity is woefully inadequate, which makes assessment of its modifications during time, impossible (Sala, 2002). Recent, intensive taxonomic research has revealed that even the contribution to marine biodiversity of relatively well known taxa such as Mollusca, is severely underestimated, and that, at least in some of the families, the fraction of described species is less than 20 % of the total number of species sampled (Bouchet et al., 2002). Furthermore, the recent discovery of a new, large species of cetacean in an area extensively studied as southern California (Heyning, 2002), throws indeed a dishearthening light on our knowledge of even the most 'conspicuous' marine groups. On the basis of extrapolations, it has been suggested that marine benthic communities may harbour more than 10 million species of macrofaunal organisms, largely still awaiting description (Grassle & Maciolek, 1992). Our knowledge of the taxonomy of most of the invertebrate groups is so scant that they cannot be used for detailed systematic evaluations. For this reason, relatively well known groups, both taxonomically and geographically, are chosen as surrogates for the whole biodiversity (Vane-Wright et al., 1994). Latest years, furthermore, have testified a revolution in our approach to the systematics of marine organisms, due to the recognition (by molecular and biochemical methods) that many of the marine and brackish water cosmopolitan or wide-ranging 'species' are often a taxonomic blanket for multiple evolutionary partitions, from genetically divergent populations to sibling species (Knowlton, 1993; 2000). Furthermore, crucial for the appreciation of the actual levels of biodiversity in the sea is the recent knowledge that, in land as in fresh-water, the highest species diversity peaks in the size range around 1-2 mm (Siemann et al., 1996), which, in the sea, is mostly represented by meiofaunal organisms, whose taxonomic knowledge is at present very poor, and which still constitutes a veritable 'new frontier' of systematic studies. Furthermore, the suggestion of the existence of a simple relation between the number of individuals in a given size class and the number of species present in that class (May, 1975), implies that the number of species of meiofauna, which may be phenomenally abundant (up to 23 million specimens of nematods alone per square meter have been documented!)(Warwick & Price, 1979), may be equally very high (Blaxter, 2003; Siemann et al., 1996). There are indeed suggestions that marine Nematoda alone may number up to 100 million species (Lambshead, 1993, Malakoff, 2003). Evidences of the very high diversity of meiofauna, at any taxonomic level considered, are summing up. In fact, all of the most recently described phyla belong to meiofauna: Gnathostomulida (1956), Loricifera (1983) and Cycliophora (1995) (Ax, 1956; Kristensen, 1983; Funch & Kristensen, 1995) as well as new classes, such as Micrognathozoa (Kristensen & Funch, 2000). Application of molecular techniques has shattered present understanding of the Platyhelminthes, resulting in the removal of Acoela and Nemertodermatida, both recently established at the Phylum level, and considered of crucial phylogenetical importance as sister taxa of the remaining bilateria, and leading to the grouping of the remaining orders in the phylum Rhabditophora (Ruiz-Trillo et al., 1999; Jondelius et al., 2001). Furthermore, phylogenetical relationships among meiofaunal taxa are still debated (see the ascription of Rotifera, Gnatosthomulida and Micrognathozoa to Gnatifera (Alhrichs, 1997) or the position of Gastrotricha (see Schmidt-Rhaes, 2002 and Garey, 2001 for radically diverging opinions). In addition, entire phyla, such as Gastrotricha, Kinorhyncha, Loricifera and Tardigrada, include exclusively meiofaunal organisms. The description of new taxa of meiofauna, of any rank, continues unrelented. Due to its taxonomic diversity, and species richness, meiofauna represents an important component of marine biodiversity. Therefore, it should be included in any study aimed to the individuation of high diversity areas for conservation purposes. In fact, recent researches suggest that environmental alterations (such as construction of harbours or artificial beaches, and removal of the 'banquette' of the sea-grass Posidonia oceanica) may lead to the extinction of populations of interstitial flatworms (Casu & Curini-Galletti, in press; Cognetti & Curini-Galletti, 1993), rising serious concerns in the case species with limited distributions are involved. Present lack of knowledge about composition and distribution of meiofauna raises concerns also in the light of the phenomena of global change, which are presently affecting the whole planet. The Earth's climate, in fact, has warmed by approximately 0.6°C over the past 100 years, with two main periods of warming, between 1910 and 1945, and from 1976 onward. The rate of warming during the latter period has been approximately double than that of the first and, thus, greater than any other time during the last 1000 years, and further warming is predicted to continue for the next 50-100 years (Parmesan et al., 1999). In present century, greenhouse gases are likely to cause the most rapid climate change that the Earth has experienced since the end of the last glaciation (Stuart Chapin et al., 2000). There is now ample evidence that these recent climatic changes have affected a broad range of organisms with diverse geographical distributions. The evidence indicates that only 30 years of warmer temperatures at the end of the twentieth century have affected the phenology of organisms, the range and distribution of species, the composition and dynamics of communities, as well as influenced the diffusion of pathogens (Gryj, 1998; Harvell et al., 2002; Walther et al., 2002). The synergism of temperature rise and modification of range, together with other stresses, such as habitat destruction and introduction of exotic species, could disrupt the connectedness among species and lead to a reformulation of species communities, reflecting differential changes in species composition, and to numerous extirpations and possibly extinctions (Root et al., 2003). Climatic fluctuations exert an overriding role on the marine biota (Cushing & Dickson, 1976; Glemarec, 1979; Southward & Boalch, 1994; Wilkinson & Buddemeier, 1994; Barry et al., 1995; Southward et al., 1995; Bianchi, 1997; Ruckelshaus & Hays, 1998). There is some evidence that Mediterranean biodiversity patterns are presently facing changes that can be related to increasing seawater temperatures (Francour et al., 1994; Danovaro et al., 2001; Chevaldonnè & Lejeusne, 2003). Evidence of a warming trend in Ligurian sea waters has been documented (Astraldi et al., 1995). As a consequence, the presence of warm water species in the Ligurian sea greatly increased from 1985 onwards, suggesting establishment of stable populations (Bianchi & Morri, 1993; 1994). Similar poleward expansions of the geographical range of warm water species have been observed in many other sites of the Mediterranean, as well as elsewhere (ref. in Bianchi & Morri, 2000; Stebbings et al., 2002; Guidetti & Boero, 2002). Meiofauna, characterized by short life cycles, poor dispersal, and, at least in a few documented cases (Casu & Curini-Galletti, in press), with restricted distributions, may allow documentation of the phenomenon in the sea, with a degree of confidence greater than that given by particularly vagile species (such as fishes) where it is not always easy to discriminate whether recent reports, sometimes of single specimens, outside the species' normal range may reflect an actual modification of the range or rather accidental events. The need of an extensive and updated data-base of the specific composition and distribution of meiofaunal taxa along the Italian coasts is particularly felt, also in the light of the impact of exotic species on the Mediterranean marine ecosystem (Bianchi & Morri, 2000). At present, there are no reports of invasions of species belonging to the 'soft bodied meiofauna'. However, this seems related to lack of investigations, which affects the group. In fact, just as an example, the banks of the Suez Canal, sandy for most of its length, cannot result in an effective barrier to migration of meiofaunal taxa, given also the present salinity range in the area. The problem of cryptogenicity (i.e. the impossibility to assess the geographical origin of newly described taxa, due to lack of previous taxonomic and biogeographical knowledge) is expected, due to the rising chances for many species to be dispersed by human-related activities, to assume more and more relevance in meiofaunal groups. This may eventually lead to the underestimation of changes in local specific composition, and even of extinctions.
The recent symposium of the Italian Society of Biogeography (Ischia, October 21-24, 2002), devoted to the marine biogeography of the Mediterranean, has singled out meiofauna among the categories of the Italian fauna whose systematic and biogeographical knowledge is particularly poor. Such state of knowledge has been similarly stigmatized in other areas of the world (Hutchings & Ponder, 2003). At present, in fact, only few areas of the world appear adeguately investigated as far as specific composition of meiofauna is concerned. Among these, a particular mention goes to North Sea area, and in particular the island of Sylt (cf Armonies & Reise, 2000), where a zoological station particularly devoted to meiofaunal studies is located. The same German school contributed significantly to the detailed knowledge of the meiofauna of the Galapagos Islands (through the series 'Interstizielle Fauna von Galapagos', published on 'Microfauna Marina', formerly 'Mikrofauna des Meeresbodens'), after extensive collections at the beginning of the '70s (cf Ax & Schmidt, 1973). For the rest of the world, broad-range taxonomic investigations are mostly still wanting, and the number of studies and of researchers in the field of meiofauna is dwindling worldwide. The so-called 'taxonomy crisis', with the progressive disappearance of experts of entire taxonomic groups, and lack of recruitment, has in fact particularly affected meiofaunal research. In fact, most meiofaunal taxa are renowned for the difficulties inherent to their study, which needs particular expertise, resulting from several years of formation. Furthermore, the relative abundance of sibling species in many meiofaunal taxa, with few diagnostic characters, makes species attributions particularly problematical. Exemplificative of the relevance of the phenomenon is the striking finding of 8 siblings of the Gyratrix hermaphroditus species complex ('Platyhelminthes': Kalyptorhynchia) in a single sample from northern Sardinia (Casu et al., 2001, Curini-Galletti et al., 2000). Present lack of knowledge is particularly marked in groups of the so-called 'soft bodied meiofauna', which need to be studied alive. The paucity of quantitative data of members of this fraction in ecological studies is in many cases related to difficulties of their identification and isolation in fixed samples, as a rule in many ecological studies. In reality, taxa of the fraction may be locally abundant. 'Platyhelminthes', in fact, may constitute between 7-25% of total meiobenthos in sandy bottoms, and, in coarse sediments, they may represent up to 95 % of total meiobenthos (Martens & Schockaert, 1986; Radziejewska & Stankowska-Radziun, 1979; Remane, 1933). Similarly, Gastrotricha may locally result as the most abundant meiofaunal group (Coull, 1985; Hochberg, 1999). However, present state of taxonomic knowledge, and the lack of identification keys on regional bases, has so far hindered the use of meiobenthos as a tool for ecological studies, such as environmental monitoring. It is apparent that without a change of sensibility towards systematic studies, present state is not likely to change. This is the rationale of the plea to the Australian government, signed by a team of marine researchers, which we fully subscribe: 'We have explored such a minuscule part of the marine environment and documented only a small fraction of its biota. It is clear that some, if not many, invertebrates may be effective indicators of stress or change in the marine environment (...). What opportunities are being lost, and how many backbone-less canaries are dying unnoticed in their watery cages?' (Hutchings & Ponder, 2003). <<<