Cesc Múrria

Small but mighty: headwaters are vital to stream network biodiversity at two levels of organization

Abstract Headwaters (stream orders 1–2) traditionally have been considered depauperate compared to mid-order streams (orders 3–4)—a conclusion that arises from a perception of streams as linear systems and emphasizes change in average &agr; (local) diversity along streams. We hypothesized an opposite pattern for &bgr; (among-site) diversity and suggest that headwaters might account for a large degree of basin-scale biodiversity if considered within the more realistic framework of streams as branching networks. We assembled pre-existing biodiversity data from across the globe to test this hypothesis broadly at the population-genetic (mitochondrial haplotype diversity within species) and community (species/taxonomic diversity) levels, with a focus on macroinvertebrates. We standardized 18 (9 headwater and 9 mid-order) population-genetic and 16 (10 headwater and 6 mid-order) community-level ecoregional data sets from 5 global ecozones for robust comparisons of &bgr;-diversity estimates between the 2 stream-size categories. At the population-genetic level, we applied measures of among-site variation commonly used at both population-genetic (FST and &PHgr;ST) and community (Sørensens dissimilarity with both presence/absence and abundance data) levels and developed a novel strategy to compare expected rates of loss of &ggr; (regional) diversity as individual sites are eliminated sequentially from regions. At the community level, we limited analyses to Sørensens presence/absence measures. We found that Sørensens dissimilarity was significantly greater among headwaters than among mid-order streams at both population-genetic and community levels. We also showed that individual headwater reaches accounted for greater proportions of genetic &ggr; diversity than did mid-order reaches. However, neither FST nor &PHgr;ST was significantly different between stream-size categories. These measures, which have been used traditionally for comparisons of population-genetic variation, measure proportions of total variation rather than solely among-site variation (i.e., they also are influenced by within-site variation). In contrast, Sørensens dissimilarity measures only among-site variation and, therefore, is presumably more useful for reflecting general &bgr; diversity. Overall results suggest that, on average, headwaters probably contribute disproportionately to biodiversity at the network scale. This finding demands a shift in thinking about the biodiversity contributions of small headwaters and has strong conservation implications for imperiled headwater streams around the world.

Drawing ecological inferences from coincident patterns of population- and community-level biodiversity.

Biodiversity is comprised of genetic and phenotypic variation among individual organisms, which might belong to the same species or to different species. Spatial patterns of biodiversity are of central interest in ecology and evolution for several reasons: to identify general patterns in nature (e.g. species–area relationships, latitudinal gradients), to inform conservation priorities (e.g. identifying hotspots, prioritizing management efforts) and to draw inferences about processes, historical or otherwise (e.g. adaptation, the centre of origin of particular clades). There are long traditions in ecology and evolutionary biology of examining spatial patterns of biodiversity among species (i.e. in multispecies communities) and within species, respectively, and there has been a recent surge of interest in studying these two types of pattern simultaneously. The idea is that examining both levels of diversity can materially advance the above‐stated goals and perhaps lead to entirely novel lines of inquiry. Here, we review two broad categories of approach to merging studies of inter‐ and intraspecific variation: (i) the study of phenotypic trait variation along environmental gradients and (ii) the study of relationships between patterns of molecular genetic variation within species and patterns of distribution and diversity across species. For the latter, we report a new meta‐analysis in which we find that correlations between species diversity and genetic diversity are generally positive and significantly stronger in studies with discrete sampling units (e.g. islands, lakes, forest fragments) than in studies with nondiscrete sampling units (e.g. equal‐area study plots). For each topic, we summarize the current state of knowledge and key future directions.

The dark side of an island radiation: systematics and evolution of troglobitic spiders of the genus Dysdera Latreille (Araneae : Dysderidae) in the Canary Islands

The spider genus Dysdera Latreille is an excellent model for the study of the evolution of cave life: ten species are known to exist exclusively in the subterranean environment of the Canary Islands, where the genus has undergone local diversification. In the present paper, two new troglobitic species (Dysdera madai, sp. nov. and D. sibyllina, sp. nov.) and the previously unknown sex of five additional species are described and illustrated: the males of D. gollumi Ribera & Arnedo, 1994, D. hernandezi Arnedo & Ribera, 1999 and D. labradaensis Wunderlich, 1991; and the females of D. andamanae Arnedo & Ribera, 1997 and D. gibbifera Wunderlich, 1991. The first direct evidence of troglobitic members of Dysdera in micro- and mesocaverns are reported. The evolution of cave life as hypothesised following a combined morphological and molecular phylogeny is investigated. Troglobitic Canarian Dysdera species have colonised the under- ground on eight independent occasions. The Dysderidae groundplan represents a preadaptation to cave life and has facil- itated the colonisation of caves. Canarian members of Dysdera have a predominantly parapatric mode of speciation, although postspeciation changes in distribution may have obscured allopatric processes. Eye regression and, to a lesser extent, larger body size and appendage elongation characterise troglobitic species. The different levels of troglobiomor- phism are interpreted as local adaptations to heterogeneous subterranean conditions. The high levels of sympatry among troglobites are explained by trophic segregation and changes in prey capture strategy were involved in the single identi- fied case of subterranean speciation in the group.

Effects of the invasive species Potamopyrgus antipodarum (Hydrobiidae, Mollusca) on community structure in a small Mediterranean stream

Resistance to biological invasions can depend on the properties of the host ecosystem and on the richness of native species. Mediterranean streams are characterized by natural seasonal disturbances, a high capability of resistance and resilience, and high diversity and endemism, which may reduce the establishment of invaders. One example of freshwater invasive species in Mediterranean streams is Potamopyrgus antipodarum, a grazing mudsnail which arrived in Europe in the late 19th century from New Zealand. We studied the effects during one year of the invasion of P. antipodarum on macroinvertebrate community structure at two different scales along a pollution gradient in a small Mediterranean catchment at the Iberian Peninsula. At reach scale, we analyzed environmental tolerance of P. antipodarum, changes of macroinvertebrate community structure along the stream, and chlorophyll-a standing stocks in field experiments. At microhabitat scale, we assessed how the abundance of P. antipodarum was mediated by biotic and abiotic factors. The abundance of P. antipodarum along the pollution gradient showed a unimodal distribution, being higher at intermediate impaired conditions. Sites with a dominance of P. antipodarum did not necessarily have a different taxonomical structure than sites without it. The effect of P. antipodarum on chlorophyll-a standing stocks was not significant. At microhabitat scale, both the biotic (competition with other taxa) and abiotic (flow velocity and substrate) factors are supposed to interfere with the abundance of P. antipodarum generating structural differences among microhabitats. Our results show that P. antipodarum had relatively high abundances in our stream but with relatively low impact, what strongly contrasts to some western US studies. Its weak effect on community structure suggested low abilities of P. antipodarum to get higher densities in the harsh hydrologic condition of Mediterranean streams characterized by seasonal droughts and floods.

Evidence from Recently Deglaciated Mountain Ranges That Baetis alpinus (Ephemeroptera) Could Lose Significant Genetic Diversity as Alpine Glaciers Disappear

Abstract: Climate change will cause relict alpine glaciers to disappear within decades. Associated high-altitude streams will face significant hydrological changes that might affect population genetic diversity of lotic species. In a recent study of glacier-fed streams in the Pyrenees, Finn et al. (2013) predicted that a large proportion of regional genetic diversity of the mayfly Baetis alpinus would be lost as glacial meltwater sources disappear. We expanded the analysis of Finn et al. to include genetic data (mitochondrial barcoding region) collected from B. alpinus occupying recently deglaciated locations including multiple basins in 2 mountain ranges (Sierra Nevada and Picos de Europa) on the Iberian Peninsula and 1 additional, deglaciated Pyrenean basin. We hypothesized that regional genetic diversity at scales of entire mountain ranges (&ggr; diversity) and population structure within ranges (&bgr; diversity) would be lower in recently deglaciated mountain ranges than in the still-glaciated Pyrenees. For 4 cryptic lineages of the B. alpinus species complex in 3 mountain ranges, we found significantly lower genetic diversity in recently deglaciated than glaciated regions. &bgr; and &ggr; genetic diversity were correlated, suggesting that population structure (&bgr;) strongly influences total regional diversity. Results support the hypothesis of Finn et al. (2013) that disappearance of alpine glaciers will result in substantial loss of genetic diversity. The distinctive hydrological environment created by glacial meltwater might drive an interaction between reproductive barriers (between highly and minimally glacier-influenced reaches within basins) and physical barriers (isolating highly glacier-influenced reaches among basins) that amplifies regional genetic diversity in mountain ranges still containing alpine glaciers.

DNA-based taxonomy of larval stages reveals huge unknown species diversity in neotropical seed weevils (genus Conotrachelus): relevance to evolutionary ecology

High diversity in tropical phytophagous insects may be linked to narrow host specificity and host shifts, but tests are complicated by incomplete taxonomy and difficulties in food source identification. Specimens of the highly diverse New World genus Conotrachelus (Coleoptera: Curculionoidea) were reared from >17,500 fruits (seeds) at six Central American rain forests. Interception traps were used for comparison with assemblages flying in the forest. Mitochondrial cox1 and the nuclear 28S genes were sequenced for 483 larval and adult specimens. A Yule-Coalescent technique was used to group cox1 sequences into putative species (17 from traps, 48 from rearing). Cox1 sequences of 24 species from museum collections provided matches for three species from traps and no match for the reared species. Inga (Fabaceae) was the predominant host among 15 other genera and 67% of the weevils were monophagous. A three gene tree (cox1, rrnL, 28S) recovered four well-supported clades feeding on Inga confirmed by phylogenetic community analyzes that showed phylogenetic conservation of host plant utilization. This suggests that host shifts are not directly involved in speciation, while the broad taxonomic host range and the evolutionary repeated shifts still contribute to the high species richness in Conotrachelus. The DNA-based approach combining species delimitation and phylogenetic analysis elucidated the evolutionary diversification of this lineage, despite insufficient taxonomic knowledge. Conotrachelus is an example of the diverse tropical groups that require DNA-based taxonomy to study their evolutionary ecology.

Homage to the Virgin of Ecology, or why an aquatic insect unadapted to desiccation may maintain populations in very small, temporary Mediterranean streams

In temporary streams, the annual constriction of drying is associated with high local extinction risk. To survive in such habitats, organisms with no specific biological traits for coping with dry periods should experience high colonisation rates from permanent reaches of the same basin or from other basins. Hydropsyche siltalai is a widespread caddisfly common in permanent and temporary headwaters reaches in the Mediterranean climate region of the Iberian Peninsula. In this study, we used genetic analyses to test if populations of H. siltalai in temporary streams are resettled from populations of the same basin or from other basins. The geographical distribution of H. siltalai was surveyed in 97 temporary and permanent reaches across four basins; larvae were found in 22 reaches (12 temporary and 10 permanent). Population genetic analyses of 11 selected reaches (6 temporary and 5 permanent) revealed low genetic diversity and no genetic population structure among and within basins. Overall, H. siltalai appeared to disperse well among basins independent of stream temporality. Permanent reaches from different basins act as a source of the individuals that recolonise temporary reaches after local extinctions, indicating a metapopulation structure at regional scale. Moreover, our results support other studies that showed that dispersal among basins is a recurrent pattern in aquatic insects.

Genetic and morphological approaches to the problematic presence of three Hydropsyche species of the pellucidula group (Trichoptera: Hydropsychidae) in the westernmost Mediterranean Basin

Hydropsyche pellucidula and Hydropsyche incognita (Trichoptera, Hydropsychidae) are common and distinguishable species in central Europe. After a review of adult material, the existence of H. pellucidula in the westernmost Mediterranean Basin was considered doubtful and determined that only H. incognita and another close species, Hydropsyche iberomaroccana, were present. Larvae of these three species are indistinguishable when applying traditional morphological keys. Using molecular analyses (cox1 gene sequences), we investigated larvae–adult associations in order to find morphological characteristics to distinguish and identify larvae. Genetic analyses detected the presence of these three species in the westernmost Mediterranean. H. pellucidula was found to be widespread along the Iberian Peninsula while H. incognita was only found in basins draining from high mountain ranges. H. iberomaroccana was distributed in the south of the Iberian Peninsula and North Africa. Using genetically identified material, a morphological key is presented for these three species.

Prospects and challenges of environmental DNA (eDNA) monitoring in freshwater ponds

Environmental DNA (eDNA) analysis is a rapid, non-invasive, cost-efficient biodiversity monitoring tool with enormous potential to inform aquatic conservation and management. Development is ongoing, with strong commercial interest, and new uses are continually being discovered. General applications of eDNA and guidelines for best practice in freshwater systems have been established, but habitat-specific assessments are lacking. Ponds are highly diverse, yet understudied systems that could benefit from eDNA monitoring. However, eDNA applications in ponds and methodological constraints specific to these environments remain unaddressed. Following a stakeholder workshop in 2017, researchers combined knowledge and expertise to review these applications and challenges that must be addressed for the future and consistency of eDNA monitoring in ponds. The greatest challenges for pond eDNA surveys are representative sampling, eDNA capture, and potential PCR inhibition. We provide recommendations for sampling, eDNA capture, inhibition testing, and laboratory practice, which should aid new and ongoing eDNA projects in ponds. If implemented, these recommendations will contribute towards an eventual broad standardisation of eDNA research and practice, with room to tailor workflows for optimal analysis and different applications. Such standardisation will provide more robust, comparable, and ecologically meaningful data to enable effective conservation and management of pond biodiversity.

Ecological constraints from incumbent clades drive trait evolution across the tree-of-life of freshwater macroinvertebrates

The rates of species and trait diversification vary across the Tree-of-Life and over time. Whereas species richness and clade age generally are decoupled, the correlation of accumulated trait diversity of clades (trait disparity) with clade age remains poorly explored. Total trait disparity may be coupled with clade age if the growth of disparity (disparification) within and across clades is continuous with time in an additive niche expansion process (linear-cumulative model), or alternatively if the rate of trait disparification varies over time and decreases as ecological space becomes gradually saturated (disparity-dependent model). Using a clock-calibrated phylogenetic tree for 143 freshwater macroinvertebrate families and richness and trait databases covering  6400 species, we measured trait disparity in 18 independent clades that successively transitioned to freshwater ecosystems and analyzed its relation with clade age. We found a positive correlation between clade age and total disparity within clades, but no relationship for most individual traits. Traits unique to freshwater lifestyle were highly variable within older clades, while disparity in younger clades shifted towards partially terrestrial lifestyles and saline tolerance to occupy habitats previously inaccessible or underutilized. These results argue that constraints from incumbent lineages limit trait disparity in younger clades that evolved for filling unoccupied regions of the trait space, which suggests that trait disparification may follow a disparity-dependent model. Overall, we provide an empirical pattern that reveals the potential of the disparity-dependent model for understanding fundamental processes shaping trait dynamics across the Tree-of-Life.