Louis Deharveng

Subterranean Ecosystems: A Truncated Functional Biodiversity

T biodiversity varies among habitats is a basic tenet of ecology. Many hypotheses have been advanced to explain these variations: ecosystem stability and complexity (e.g., Pimm 1984), ecosystem predictability, habitat heterogeneity (e.g., Tilman 1982), and disturbance (the intermediate disturbance hypothesis; Grime 1973). Whatever the cause of its fluctuations, there is evidence that, at a certain threshold, biodiversity is critical to the maintenance of ecosystems. The link between biodiversity and ecosystem function depends on the dissipation of energy, and productivity might be the ultimate factor that controls species richness at local and, to some degree, at regional scales (Ricklefs and Schluter 1993). Ecosystem function accounts for the relative stability of biodiversity ratios between similar habitats of different continents (Caley and Schluter 1997). In contrast, absolute measures of biodiversity in similar habitats of different regions may differ greatly, which has been interpreted as a result of historical processes (Ricklefs and Schluter 1993). Biodiversity patterns of subterranean terrestrial and aquatic ecosystems are in line with these general observations. However, the features of this environment (absence of light, limited variations in temperature, paucity of food, high physical fragmentation) (Ginet and Decou 1977, Camacho 1992) provide unique opportunities to explore biodiversity issues and to test some of the general hypotheses listed above. Subterranean habitats predominate on the continental and ocean margins. Considering the continental earth, 97% of all unfrozen freshwater is subsurface, whereas lakes and rivers represent less than 2%. Terrestrial subterranean habitats encompass the whole unsaturated zone (vadose zone) of underground, most evident in karstic areas (caves, fissures, cracks, etc.), which represent nearly 4% of the rock outcrops of the world. Because they develop in rocks or sediments that protect them against surface environmental changes, these subterranean ecosystems, in contrast to most surface ecosystems which are short-lived (rivers, wetlands, or forests), may persist relatively unchanged for millions of years. In the last two decades groundwater ecology has developed rapidly, forming an important branch of limnology (Stanford and Simon 1992, Gibert et al. 1994, Stanford and Valett 1994, Danielopol et al. 1999). Recent literature has focused on general characteristics of subterranean ecosystems and interac-

New Caledonia: a very old Darwinian island?

New Caledonia has generally been considered a continental island, the biota of which largely dates back to Gondwanan times owing to its geological origin and the presence of phylogenetic relicts. This view is contradicted by geological evidence indicating long Palaeocene and Eocene submersions and by recent biogeographic and phylogenetic studies, with molecular or geophysical dating placing the biota no older than the Oligocene. Phylogenetic relicts do not provide conclusive information in this respect, as their presence cannot be explained by simple hypotheses but requires assumption of many ad hoc extinction events. The implication of this new scenario is that all the New Caledonian biota colonized the island since 37 Ma Local richness can be explained by local radiation and adaptation after colonization but also by many dispersal events, often repeated within the same groups of organisms. Local microendemism is another remarkable feature of the biota. It seems to be related to recent speciation mediated by climate, orography, soil type and perhaps unbalanced biotic interactions created by colonization disharmonies. New Caledonia must be considered as a very old Darwinian island, a concept that offers many more fascinating opportunities of study.

New Species in the Old World: Europe as a Frontier in Biodiversity Exploration, a Test Bed for 21st Century Taxonomy

The number of described species on the planet is about 1.9 million, with ca. 17,000 new species described annually, mostly from the tropics. However, taxonomy is usually described as a science in crisis, lacking manpower and funding, a politically acknowledged problem known as the Taxonomic Impediment. Using data from the Fauna Europaea database and the Zoological Record, we show that contrary to general belief, developed and heavily-studied parts of the world are important reservoirs of unknown species. In Europe, new species of multicellular terrestrial and freshwater animals are being discovered and named at an unprecedented rate: since the 1950s, more than 770 new species are on average described each year from Europe, which add to the 125,000 terrestrial and freshwater multicellular species already known in this region. There is no sign of having reached a plateau that would allow for the assessment of the magnitude of European biodiversity. More remarkably, over 60% of these new species are described by non-professional taxonomists. Amateurs are recognized as an essential part of the workforce in ecology and astronomy, but the magnitude of non-professional taxonomist contributions to alpha-taxonomy has not been fully realized until now. Our results stress the importance of developing a system that better supports and guides this formidable workforce, as we seek to overcome the Taxonomic Impediment and speed up the process of describing the planetary biodiversity before it is too late.

A molecular phylogeny shows the single origin of the Pyrenean subterranean Trechini ground beetles (Coleoptera: Carabidae)

Trechini ground beetles include some of the most spectacular radiations of cave and endogean Coleoptera, but the origin of the subterranean taxa and their typical morphological adaptations (loss of eyes and wings, depigmentation, elongation of body and appendages) have never been studied in a formal phylogenetic framework. We provide here a molecular phylogeny of the Pyrenean subterranean Trechini based on a combination of mitochondrial (cox1, cyb, rrnL, tRNA-Leu, nad1) and nuclear (SSU, LSU) markers of 102 specimens of 90 species. We found all Pyrenean highly modified subterranean taxa to be monophyletic, to the exclusion of all epigean and all subterranean species from other geographical areas (Cantabrian and Iberian mountains, Alps). Within the Pyrenean subterranean clade the three genera (Geotrechus, Aphaenops and Hydraphaenops) were polyphyletic, indicating multiple origins of their special adaptations to different ways of life (endogean, troglobitic or living in deep fissures). Diversification followed a geographical pattern, with two main clades in the western and central-eastern Pyrenees respectively, and several smaller lineages of more restricted range. Based on a Bayesian relaxed-clock approach, and using as an approximation a standard mitochondrial mutation rate of 2.3% MY, we estimate the origin of the subterranean clade at ca. 10 MY. Cladogenetic events in the Pliocene and Pleistocene were almost exclusively within the same geographical area and involving species of the same morphological type.

Biological invasions in soil: DNA barcoding as a monitoring tool in a multiple taxa survey targeting European earthworms and springtails in North America

Biological invasions are increasingly recognized as a potent force altering native ecosystems worldwide. Many of the best documented cases involve the massive invasions of North America by plant and animal taxa native to Europe. In this study, we use DNA barcoding to survey the occurrence and genetic structure of two major groups of soil invertebrates in both their native and introduced ranges: Collembola and earthworms. Populations of ten species of earthworms and five species of Collembola were barcoded from both continents. Most of these species exhibited a similar genetic structure of large and stable populations in North America and Europe, a result supporting a scenario of multiple invasions. This was expected for earthworm species involved in human economic activities, but not foreseen for Collembola species de facto unintentionally introduced. This study also establishes that invasive species surveys employing DNA barcoding gain additional resolution over those based on morphology as they allow evaluation of cryptic lineages exhibiting different invasion histories.

Challenging species delimitation in Collembola: cryptic diversity among common springtails unveiled by DNA barcoding

Abstract. Collembola is one of the major functional groups in soil as well as a model taxon in numerous disciplines. Therefore the accurate identification of specimens is critical, but could be jeopardised by cases of cryptic diversity. Several populations of six well characterised species of springtails were sequenced using the COI barcode fragment as a contribution to the global Collembola barcoding campaign. Each species showed high intraspecific divergence, comparable to interspecific sequence divergence values observed in previous studies and in 10 congeneric species barcoded here as a reference. The nuclear marker, 28S, confirmed all the intraspecific lineages found with COI, supporting the potential specific status of these entities. The implications of this finding for taxonomy and for disciplines relying on species names, such as evolution and ecology, are discussed.

Coupling non-destructive DNA extraction and voucher retrieval for small soft-bodied Arthropods in a high-throughput context: the example of Collembola.

Here, we describe a simple method adapted for high‐throughput protocols allowing voucher specimen recovery for Collembola and by extension for other soft‐bodied small arthropods. A standard extraction protocol was tested to examine the effects of lysis duration (1, 2, 4, 12 h) on DNA concentration, amplification success and specimen condition. Good quality DNA was obtained after 1 h of lysis, while voucher condition was fine for up to 12 h. The lysis step substantially shortens the clearing process necessary for morphological examination.

Cryptic Diversity in the Ubiquist Species Parisotoma notabilis (Collembola, Isotomidae): A Long-Used Chimeric Species?

Parisotoma notabilis is the most common species of Collembola in Europe and is currently designated as ubiquist. This species has been extensively used in numerous studies and is considered as well characterized on a morphological ground. Despite the homogeneity of its morphology, the sequencing of the barcoding fragment (5′ end of COI) for several populations throughout Europe and North America revealed four distinct genetic lineages. The divergence found between these lineages was similar to the genetic distance among other species of the genus Parisotoma included in the analysis. All four lineages have been confirmed by the nuclear gene 28S. This congruence between mitochondrial and nuclear signals, as well as the geographical distribution pattern of lineages observed in Europe, supports the potential specific status of these lineages. Based on specimens from the type locality (Hamburg), the species name was successfully assigned to one of these lineages. This finding raises several problems as Parisotoma notabilis has been widely used in many ecological studies. Accumulation of new data for the different lineages detected, especially ecological information and life history traits, is needed to help resolve this situation.

Predictive models of collembolan diversity and abundance in a riparian habitat

The artificial neural network (ANN) was used in this work for modelling the abundance and diversity of hydrophilous Collembola on the microhabitat scale. The procedure was applied to a Collembolan assemblage of the northern Pyrenees. Six variables were retained to describe its structure: abundance of the three dominant species, species richness, overall abundance of Collembola, and Shannon index. Seven environmental variables were selected as explanatory variables: distance to water, soil temperature, water content, and proportion of mineral soil, moss, litter and rotten wood in the substrate. Correlations between observed values and values estimated by ANN models of the six dependent variables were all highly significant. The ANN models were developed from 83 samples chosen at random and were validated on the 21 remaining samples. The role of each variable was evaluated by inputting fictitious configurations of independent variables and by checking the response of the model. The resulting habitat profiles depict the complex influence of each environmental variable on the biological parameters of the assemblage, and the non-linear relationships between dependent and independent variables. The main results and the ANN potential to predict biodiversity and structural characteristics of species assemblages are discussed.

Systematic revision of Entomobryidae (Collembola) by integrating molecular and new morphological evidence

Entomobryidae, the largest collembolan family, is traditionally classified at suprageneric level using a limited set of morphological structures, such as scales, antennal segmentation. Most tribal and subfamilial delimitations appear, however, disputable in the light of recent works. Integrating molecular and morphological evidence, we propose here a revision of the systematics of the family. In addition to traditional taxonomic characters, tergal specialized chaetae (S‐chaetae) are newly introduced, and their patterns are shown to be diversified at all levels from species to subfamilies. S‐chaetotaxic pattern on phylogenetic tree shows that evolution of S‐chaetae is not parallel between the different terga and that their patterns coincide well with the known molecular phylogeny, providing a powerful tool for the systematics of Entomobryidae. Orchesellinae sensu Soto‐Adames et al. (Annals of the Entomological Society of America, 101, 2008, 501); is divided into three subfamilies: Orchesellinae s. s., Bessoniellinae and Heteromurinae, the latter two upgraded from the original tribal level. Entomobryinae sensu Szeptycki (Morpho‐Systematic Studies on Collembola. IV. Chaetotaxy of the Entomobryidae and its Phylogenetical Significance, 1979), is no longer divided into scaled and unscaled tribes, and Lepidosira‐group is transferred from Seirinae to Entomobryinae. A key to subfamilies and tribes and a comparison with previous classifications of the Entomobryidae are provided. This study greatly improves the understanding of primary and secondary characters and erects the fundamental framework for the taxonomy of Entomobryidae.