Regional species richness in an obligate subterranean dwelling fauna – epikarst copepods

Aim  The diversity of the obligate cave-dwelling fauna has proved difficult to measure because of the highly localized distributions of most species. We investigated: (1) the local and regional diversity patterns of a major component of the obligate cave-dwelling fauna living in the epikarst zone, the karst layer closest to the surface; (2) variations in local and regional patterns of species richness; and (3) sampling sufficiency at multiple scales.
Location  Caves in the Dinaric Mountains of Slovenia.
Methods  We sampled continuously the abundance of 37 species of copepods dislodged from the epikarst from 35 ceiling drips in six caves for a period of one year. Copepods were collected in a specially designed net that allowed continuous collection.
Results  Based on species accumulation curves and Chao estimates of total diversity, we determined that 3–4 months of continuous sampling were sufficient to find 90% of the species in a drip, that five drips were sufficient to find 90% of the species in a cave, and that five caves were sufficient to find 90% of the species in a region.
Main conclusions  The epikarst copepod fauna is a significant part of the aquatic cave fauna, contributing about 20% at the regional level. Because of the scale of variation, much of which occurs within a cave, and because of the availability of continuous sampling devices, the epikarst component of subterranean diversity seems to be more thoroughly and accurately measured than do other components.     

Stygobiotic crustacean species richness: a question of numbers,a matter of scale

Species richness in ground water is still largely underestimated, and this situation stems from two different impediments: the Linnaean (i.e. the taxonomic) and the Wallacean (i.e. the biogeographical) shortfalls. Within this fragmented frame of knowledge of subterranean biodiversity, this review was aimed at (i) assessing species richness in ground water at different spatial scales, and its contribution to overall freshwater species richness at the continental scale; (ii) analysing the contribution of historical and ecological determinants in shaping spatial patterns of stygobiotic species richness across multiple spatial scales; (iii) analysing the role of β-diversity in shaping patterns of species richness at each scale analysed. From data of the present study, a nested hierarchy of environmental factors appeared to determine stygobiotic species richness. At the broad European scale, historical factors were the major determinants in explaining species richness patterns in ground water. In particular, Quaternary glaciations have strongly affected stygobiotic species richness, leading to a marked latitudinal gradient across Europe, whereas little effects were observed in surface fresh water. Most surface-dwelling fauna is of recent origin, and colonized this realm by means of post-glacial dispersal. Historical factors seemed to have also operated at the smaller stygoregional and regional scales, where different karstic and porous aquifers showed different values of species richness. Species richness at the small, local scale was more difficult to be explained, because the analyses revealed that point-diversity in ground water was rather low, and at increasing values of regional species richness, reached a plateau. This observation supports the coarse-grained role of truncated food webs and oligotrophy, potentially reflected in competition for food resources among co-occurring species, in shaping groundwater species diversity at the local scale. Alpha-diversity resulted decoupled from γ-diversity, suggesting that β-diversity accounted for the highest values of total species richness at the spatial scales analysed.     

Assessing and conserving groundwater biodiversity: synthesis and perspectives

1. This paper is a synthesis of a special issue on groundwater biodiversity with a focus on obligate subterranean species, the stygobionts. The series of papers constitutes a great leap forward in assessing and understanding biodiversity patterns because of the use of large quantitative data sets obtained over a broad geographic scale. They also represent a conceptual shift, away from a purely taxonomic and phylogenetic focus to the analysis of whole groundwater assemblages.
2. The general patterns emerging for groundwater fauna are: very high levels of endemism, low local diversity relative to regional diversity, a limited number of lineages, occurrence of many relicts, and truncated food webs with very few predators.
3. β-Diversity is at least as important as α-diversity in determining total richness at different scales (aquifer, basin and region) and overall taxa richness increases across spatial scales.
4. Advances in understanding groundwater biodiversity patterns further include identification of several important factors related to geology and hydrology that determine the composition of European stygobiotic assemblages.
5. Important challenges for future research include improving sampling strategies, filling gaps in sampling coverage, intensifying research on theoretical and statistical models, and including functional and genetic diversity components in biodiversity assessments.
6. Strategies are proposed for protecting groundwater biodiversity and an argument is made to integrate biodiversity in groundwater management. Applying principles such as complementarity and flexibility for groundwater biodiversity conservation is a major step toward delineating a reserve network that maximise species representation at the European scale.     

The importance of local and landscape-scale processes to the occupancy of wetlands by pond-breeding amphibians

Variation in the distribution and abundance of species across landscapes has traditionally been attributed to processes operating at fine spatial scales (i.e., environmental conditions at the scale of the sampling unit), but processes that operate across larger spatial scales such as seasonal migration or dispersal are also important. To determine the relative importance of these processes, we evaluated hypothesized relationships between the probability of occupancy in wetlands by two amphibians [wood frogs (Lithobates sylvaticus) and boreal chorus frogs (Pseudacris maculata)] and attributes of the landscape measured at three spatial scales in Rocky Mountain National Park, Colorado. We used cost-based buffers and least-cost distances to derive estimates of landscape attributes that may affect occupancy patterns from the broader spatial scales. The most highly ranked models provide strong support for a positive relationship between occupancy by breeding wood frogs and the amount of streamside habitat adjacent to a wetland. The model selection results for boreal chorus frogs are highly uncertain, though several of the most highly ranked models indicate a positive association between occupancy and the number of neighboring, occupied wetlands. We found little evidence that occupancy of either species was correlated with local-scale attributes measured at the scale of individual wetlands, suggesting that processes operating at broader scales may be more important in influencing occupancy patterns in amphibian populations.     

Environmental and dispersal controls of an annual plant’s distribution: how similar are patterns and apparent processes at two spatial scales?

At scales from microsites to entire ranges, species’ distributions reflect limited adaptation and/or limited dispersal. To what extent are specific distribution patterns and processes similar across scales? We investigated environmental effects—presumed because of adaptation—and independent spatial effects—presumed because of dispersal—on distribution at two scales (landscape patches of approximately 1,300 m², sampled along transects, and 4-m² cells, sampled in contiguous grids within populations) and on individual performance (water status, reproduction) in the California annual, Clarkia xantiana ssp. xantiana. Because water limitation helps set this species’ regional borders, we expected occupancy and performance at smaller scales to correlate with topographic and soil features affecting water relations. At the patch scale, environmental features associated with reduced water stress (i.e., steep slopes that face north; coarse, soft soils; igneous rather than metasedimentary parent rock) predicted occupancy. Spatial aggregation was not detected, but incomplete occupancy of apparently suitable patches indicated that dispersal limits occupancy. At the scale of small cells, relationships between environmental variables, occupancy, density, and performance varied among populations. Associations sometimes resembled those at the patch scale but sometimes opposed them. Spatial aggregation in cell occupancy and/or density occurred in all populations, implying limited dispersal, whereas spatial aggregation of water potential values in some populations might have arisen from spatially structured unmeasured environmental variables. Limited adaptation to drought and limited patch colonization appear to affect patch occupancy in C. xantiana ssp. xantiana, whereas smaller-scale patterns indicate consistent effects of limited dispersal and somewhat variable environmental effects.     

Trans-oceanic and endemic origins of the small minnow mayflies (Ephemeroptera, Baetidae) of Madagascar

We investigated the relative importance of dispersal and vicariance in forming the Madagascar insect fauna, sequencing approximately 2300bp from three rRNA gene regions to investigate the phylogeny of Afrotropical small minnow mayflies (Ephemeroptera: Baetidae). Six lineages contained trans-oceanic sister taxa, and variation in genetic divergence between sister taxa revealed relationships that range from very recent dispersal to ancient vicariance. Dispersal was most recent and frequent in species that spend the larval stage in standing water, adding to evidence that these evolutionarily unstable habitats may select for ecological traits that increase dispersal in insects. Ancestral state likelihood analysis suggested at least one Afrotropical lineage had its origin in Madagascar, demonstrating that unidirectional dispersal from a continental source may be too simplistic. We conclude that the Malagasy mayfly fauna should be considered in a biogeographical context that extends beyond Madagascar itself, encompassing trans-oceanic dispersal within multiple lineages.     

Obligate groundwater fauna of France: diversity patterns and conservation implications

We examined taxonomic and geographic patterns of the obligate groundwater fauna (i.e. stygobiotic fauna) by assembling in a distributional data base all species occurrences reported from France since 1805. A simulated annealing algorithm was used to identify conservation targets. Until the 60s, biological surveys were restricted to caves but the proportion of sampling sites in unconsolidated sediments increased from 1 to 16% over the last 40 years. A total of 380 species and subspecies in 40 families were collected, 70% of which being restricted to France. As observed in other temperate regions, the stygobiotic fauna was dominated by crustaceans (65% of species) and molluscs (22%). The cumulative number of species did not level off over time, clearly showing that biodiversity was underestimated. Temporal trends in the cumulative number of obligate groundwater and surface water species suggested that groundwater comprised more crustaceans than surface freshwater. Endemism was high although the geographic range size of species increased as distributional data accumulated. Of 380 species, 156 were known from a single 400-km² cell, among which 73% were located in the southern third of France. The distribution map of species richness changed dramatically over time, indicating that the location of richness hotspots was sensitive to sampling effort. Less than 2% of the French landscape was needed to capture 60% of known species. Thus, a large proportion of species could be protected by focusing habitat conservation efforts on a few complementary species-rich aquifers located in distinct regions.     

Molecular phylogeny and phylogeography of the Cuban cave-fishes of the genus Lucifuga: evidence for cryptic allopatric diversity

Underground environments are increasingly recognized as reservoirs of faunal diversity. Extreme environmental conditions and limited dispersal ability of underground organisms have been acknowledged as important factors promoting divergence between species and conspecific populations. However, in many instances, there is no correlation between genetic divergence and morphological differentiation. Lucifuga Poey is a stygobiotic fish genus that lives in Cuban and Bahamian caves. In Cuba, it offers a unique opportunity to study the influence of habitat fragmentation on the genetic divergence of stygobiotic species and populations. The genus includes four species and one morphological variant that have contrasting geographical distributions. In this study, we first performed a molecular phylogenetic analysis of the Lucifuga Cuban species using mitochondrial and nuclear markers. The mitochondrial phylogeny revealed three deeply divergent clades that were supported by nuclear and morphological characters. Within two of these main clades, we identified five lineages that are candidate cryptic species and a taxonomical synonymy between Lucifuga subterranea and Lucifuga teresinarum. Secondly, phylogeographic analysis using a fragment of the cytochrome b gene was performed for Lucifuga dentata, the most widely distributed species. We found strong geographical organization of the haplotype clades at different geographic scales that can be explained by episodes of dispersal and population expansion followed by population fragmentation and restricted gene flow. At a larger temporal scale, these processes could also explain the diversification and the distribution of the different species.     

Biodiversity indicators in European ground waters: towards a predictive model of stygobiotic species richness

1. Estimates of species richness obtained from exhaustive field inventories over large spatial scales are expensive and time-consuming. For this reason, efficiency demands the use of indicators as 'surrogates' of species richness. Biodiversity indicators are defined herein as a limited suite of taxonomic groups the species richness of which is correlated with the species richness of all other taxonomic groups present in the survey area.
2. Species richness in ground water was assessed at different spatial scales using data collected from six regions in Europe. In total, 375 stygobiotic species were recorded across 1157 sites and 96 aquifers. The taxonomic groups collected from more than one site and with more than two species (Oligochaeta, Gastropoda, Cyclopoida, Harpacticoida, Ostracoda, Isopoda, Amphipoda, Bathynellacea and Acari) were used to develop nonparametric models to predict stygobiotic biodiversity at the aquifer scale.
3. Pair-wise correlations between taxonomic groups were low, i.e. variation in species richness of a single taxonomic group did not usually reflect variation of the other groups. In contrast, multiple regressions calculated between species richness of any combination of taxa and extra-group species richness along the six regions resulted in a number of significant relationships.
4. These results suggest that some taxonomic groups (mainly Copepoda and Amphipoda and, to a lesser extent, Oligochaeta and Gastropoda) combined in different ways across the regions, were good biodiversity indicators in European groundwater ecosystems. However, the uneven distribution of taxonomic groups prevented selection of a common set of indicators for all six regions. Faunal differences among regions are presumably related to both historical and ecological factors, including palaeogeography, palaeoecology, geology, aquifer fragmentation and isolation, and, less clearly, anthropogenic disturbance.     

Geographical patterns of genetic structure in marine species with contrasting life histories

Aim  Phylogeographical breaks may reflect historical or present-day impediments to gene flow, and the congruence of these breaks across multiple species lends insight into evolutionary history and connectivity among populations. In marine systems, examining the concordance of phylogeographical breaks is challenging due to the varied sampling scales in population genetics studies and the diverse life histories of marine organisms. A quantitative approach that considers the effects of sampling scale and species life history is needed.
Location  The south-east and south-west coasts of the United States.
Methods  We quantitatively analysed previously published datasets of marine fauna to look for concordance among phylogeographical breaks. We used a bootstrap approach to determine the regions where phylogeographical breaks are more common than expected by chance among species with planktonic dispersal as well as those with restricted dispersal.
Results  On the south-west coast, breaks were clustered near Point Conception among planktonic dispersers and near Los Angeles among restricted dispersers. On the south-east coast, breaks were most common near the southern tip of Florida for planktonic dispersers and near Cape Canaveral for restricted dispersers.
Main conclusions  Dispersal ability is an important determinant of phylogeographical patterns in marine species. Breaks among planktonic dispersers on both coasts are congruent with present-day flow-mediated barriers to dispersal, suggesting that phylogeographical structure in species with planktonic larvae may reflect contemporary oceanography, while breaks in restricted dispersers reflect historical processes. These results highlight the importance of explicitly considering sampling scale and life history when evaluating phylogeographical patterns.     

Biogeography of the wax scales (Insecta: Hemiptera: Coccidae: Ceroplastinae)

The modern and native distributions of wax scales are documented and an area cladogram including seventy species is presented. Wax scales are distributed worldwide, but most species are native to either South America or Africa. Their native distribution pattern is discussed in relation to their host-plant specificity and to the dispersal and vicariance theories of biogeography. The vicariance theory is preferred, because the pattern can be explained satisfactorily by plate tectonics but not by dispersal from a centre of origin. The wax scale group probably originated in the combined South American–African continent at least 97 million yr ago.     

Subsocial spiders in space and time: A fine scale approach to the dynamics of dispersal

Less than 0.2% of all spider species live in close associations with conspecifics. Among these, subsocial spiders show characteristics of both solitary spiders (e.g., individuals disperse for breeding) and social spiders (e.g., prolonged cooperative behaviours at least prior to independent reproduction). Dispersing individuals build small webs, usually with one inhabitant, whereas colonies are large webs with plant debris and harbouring multiple females. We studied the spatiotemporal dynamics of dispersal in the subsocial spider Anelosimus baeza. We followed the occupancy of all colonies and dispersal webs over the breeding season by mapping the number and sex of spiders with respect to their location in three dimensions. We studied the settlement patterns of new webs and fluctuation in web occupancy through movement between occupied and abandoned webs of colonies and dispersal webs. The occupancy of webs was highly dynamic with changes occurring at small time scales. The similarity in the patterns of web occupancy by females among dispersal webs was partially explained by their spatial and their temporal proximity. Our results suggest that dispersal webs may be used by spiders as a temporary refuge by both sexes during the breeding season. Patterns described here suggest new approaches to dispersal studies in group living spiders.     

Phylogeography of cave pseudoscorpions in southern Australia

Aim  To investigate molecular phylogenetic divergence and historical biogeography of the cave-dwelling pseudoscorpion genus Protochelifer.
Location  Caves and nearby epigean habitats in southern Australia were sampled from western Victoria, Naracoorte Caves, Flinders Ranges, Kangaroo Island, Nullarbor Plain and south-west Western Australia.
Methods  Allozyme electrophoresis (57 individuals) and a 569-base-pair section of the mtDNA COI gene (22 individuals) were used to reconstruct phylogenetic relationships among four cave species and three epigean species from 13 locations.
Results  Phylogenetic reconstruction using the allozyme and mtDNA sequence data revealed a similar topology, showing recent speciation of several Protochelifer populations in caves from Naracoorte to the Nullarbor Plain. Naracoorte Caves contained a single species, Protochelifer naracoortensis , found in four separate caves, while all other cave species appear to be restricted to single caves.
Main conclusions  At a local scale, as indicated by the four Naracoorte caves, dispersal is thought to occur via micro- and mesocaverns, and possibly by phoresy using insect or bat vectors. With current data we are unable to determine if cavernicolous species of Protochelifer have arisen from a single cave colonization event followed by phoretic dispersal on bats to other caves, or multiple cave-invasion events from independent epigean ancestors. Genetic heterogeneity among Protochelifer populations from Nullarbor caves suggest that P. cavernarum , the only species presently recorded from this region, is likely to constitute a species complex requiring further study to fully resolve its relationships.     

Spatial genetic differentiation correlates with species assemblage turnover across tropical reef fish lineages

Aim

Evaluating the similarity of diversity patterns across micro- to macroevolutionary scales in natural communities, such as species–genetic diversity correlations (SGDCs), may inform on processes shaping community assembly. However, whether SGDCs not only hold across communities but also across lineages has never been explored so far. Here we investigated SGDCs across co-distributed taxa for different spatial components (α, β, γ), and formally tested the influence of dispersal traits on β-SGDCs.

Location

Western Indian Ocean.

Time period

2016–2017.

Major taxa studied

Tropical reef fish species with contrasting dispersal traits.

Methods

Using double-digest restriction-site associated DNA sequencing (ddRADseq) Single Nucleotide Polymorphism data for 20 tropical reef fishes and distribution data of 2,446 species belonging to 12 families, we analysed the correlations between within-species genetic diversity and within-family species diversity (i.e., lineage diversity) for the three spatial components (α, β, γ-SGDCs). We then related the strength of β-SGDCs per species to proxies of larval dispersal abilities.

Results

We detected positive and significant lineage-based SGDC only for the β component, that is, the families showing the greatest level of species turnover among sites contain the species with the greatest levels of genetic differentiation. We showed that the Monsoon Drift mainly explained the β-diversity patterns at both intraspecific and interspecific levels. Higher β-SGDCs were found for species with short pelagic larval duration and weak larval swimming capacity.

Main conclusions

Our study reveals a strong correlation between genetic and species β-diversity, a result explained by the presence of a ‘soft’ barrier and mediated by larval dispersal processes. This suggests that vicariance and dispersal limitation are major processes shaping β-diversity patterns from microevolutionary to macroevolutionary scales in tropical reef fishes.     

Abundance–occupancy relationships

1.  The abundance and distribution of species tend to be linked, such that species declining in abundance often tend also to show declines in the number of sites they occupy, while species increasing in abundance tend also to be increasing in occupancy. Therefore, intraspecific abundance–occupancy relationships are commonly positive.
2.  The intraspecific pattern is mirrored by more general positive interspecific abundance–occupancy relationships: widespread species tend to be abundant, and narrowly distributed species rare.
3.  Here, we review recent research on these patterns based on the flora and fauna of the British Isles. We assess their generality, describe what is currently known about their structure, and summarize the results of tests of the several hypotheses proposed to explain their existence.
4.  The positive form generally exhibited by abundance–occupancy relationships, intraspecific or interspecific, has consequences for several areas of applied ecology, including conservation, harvesting, biological invasions and biodiversity inventorying. These implications are discussed briefly.     

Gondwanan break-up: legacies of a lost world?

Fierce debate surrounds the history of organisms in the southern hemisphere; did Gondwanan break-up produce ocean barriers that imposed distribution patterns on phylogenies (vicariance)? Or have organisms modified their distributions through trans-oceanic dispersal? Recent advances in biogeographical theory suggest that the current focus on vicariance versus dispersal is too narrow because it ignores 'geodispersal' (i.e. expansion of species into areas when geographical barriers disappear), extinction and sampling errors. Geodispersal produces multiple, conflicting vicariance patterns, and extinction and sampling errors destroy vicariance patterns. This perspective suggests that it is more difficult to detect vicariance than trans-oceanic dispersal and that specialized methods must be applied if an unbiased understanding of southern hemisphere biogeography is to be achieved.     

Latitudinal variation of diversity in European freshwater animals is not concordant across habitat types

Aim   We analysed the variation of species richness in the European freshwater fauna across latitude. In particular, we compared latitudinal patterns in species richness and β-diversity among species adapted to different habitat types.
Location   Europe.
Methods   We compiled data on occurrence for 14,020 animal species across 25 pre-defined biogeographical regions of European freshwaters from the Limnofauna Europaea . Furthermore, we extracted information on the habitat preferences of species. We assigned species to three habitat types: species adapted to groundwater, lotic (running water) and lentic (standing water) habitats. We analysed latitudinal patterns of species richness, the proportion of lentic species and β-diversity.
Results   Only lentic species showed a significant species–area relationship. We found a monotonic decline of species richness with latitude for groundwater and lotic habitats, but a hump-shaped relationship for lentic habitats. The proportion of lentic species increased from southern to northern latitudes. β-Diversity declined from groundwater to lentic habitats and from southern to northern latitudes.
Main conclusions   The differences in the latitudinal variation of species richness among species adapted to different habitat types are in part due to differences in the propensity for dispersal. Since lentic habitats are less persistent than lotic or groundwater habitats, lentic species evolved more efficient strategies for dispersal. The dispersal propensity of lentic species facilitated the recolonization of central Europe after the last glaciation. Overall, we stress the importance of considering the history of regions and lineages as well as the ecological traits of species for understanding patterns of biodiversity.     

Quantitative palaeobiogeography: GIS, phylogenetic biogeographical analysis, and conservation insights

Aim  The utility of GIS-based and phylogenetic biogeographical analysis in palaeobiogeography is reviewed with reference to its ability to elucidate patterns of interest for modern conservation biology, specifically the long-term effects of invasive species.
Location  Emphasis is on biogeographical patterns in the Appalachian basin and mid-continent of North America during the Devonian. Global palaeobiogeographical patterns of the Cambrian are also considered.
Methods  Palaeobiogeographical patterns are assessed within a GIS framework, including both direct range reconstruction and niche modelling methods, and within phylogenetic biogeographical analysis. Biogeographical patterns are considered within multiple clades of fossil invertebrates, including trilobites, crustaceans, brachiopods, and bivalves.
Results  GIS-based analysis (including niche modelling methods) of Devonian invertebrates demonstrates a tightly correlated relationship between sea-level rises and range expansion, dispersal events, and species invasions. The predominance of range expansion and species invasions during the Late Devonian reduced opportunities for vicariant speciation during this interval. Comparison of phylogenetic biogeographical patterns between Cambrian and Devonian trilobites allows discernment of the relative roles of tectonics and eustacy in driving biogeographical patterns.
Main conclusions  GIS analysis and phylogenetic biogeography are powerful tools for analysing the coevolution of the Earth and its biota. Analyses can identify episodes of vicariance and geo-dispersal and produce testable hypotheses for further analysis within the fossil record.     

Mountaintop island age determines species richness of boreal mammals in the American Southwest

Models that describe the mechanisms responsible for insular patterns of species richness include the equilibrium theory of island biogeography and the nonequilibrium vicariance model. The relative importance of dispersal or vicariance in structuring insular distribution patterns can be inferred from these models. Predictions of the alternative models were tested for boreal mammals in the American Southwest. Age of mountaintop islands of boreal habitat was determined by constructing a geographic cladogram based on characteristics of intervening valley barriers. Other independent variables included area and isolation of mountaintop islands. Island age was the most important predictor of species richness. In contrast with previous studies of species richness patterns in this system, these results supported the nonequilibrium vicariance model, which indicates that vicariance has been the primary determinant of species distribution patterns in this system.     

Ecological correlates of geographical range occupancy in North American birds

Aim  The degree to which a species is predictably encountered within its range varies tremendously across species. Understanding why some species occur less frequently within their range than others has important consequences for conservation and for analyses of ecological patterns based on range maps. We examined whether patterns in geographical range occupancy can be explained by species-level traits.
Location  North America.
Methods  We used survey data from 1993 to 2002 from the North American Breeding Bird Survey along with digital range maps produced by NatureServe to calculate range occupancy for 298 species of terrestrial birds. We tested whether species traits explained variation in range occupancy values using linear regression techniques.
Results  We found three species traits that together explained more than half of the variation in range occupancy. Population density and niche breadth were positively correlated with occupancy, while niche position was negatively correlated with occupancy.
Main conclusions  Our results suggest that high range occupancy will occur in species that are common at sites on which they occur, that tolerate a relatively wide range of ecological conditions and that tend to have ranges centred on areas with common environmental conditions. Furthermore, it appears that niche-based characteristics may explain patterns of distribution and abundance from local habitats up to the scale of geographical ranges.