Phylogenetic analysis of conservation priorities for aquatic mammals and their terrestrial relatives, with a comparison of methods

Background

Habitat loss and overexploitation are among the primary factors threatening populations of many mammal species. Recently, aquatic mammals have been highlighted as particularly vulnerable. Here we test (1) if aquatic mammals emerge as more phylogenetically urgent conservation priorities than their terrestrial relatives, and (2) if high priority species are receiving sufficient conservation effort. We also compare results among some phylogenetic conservation methods.

Methodology/Principal Findings

A phylogenetic analysis of conservation priorities for all 620 species of Cetartiodactyla and Carnivora, including most aquatic mammals. Conservation priority ranking of aquatic versus terrestrial species is approximately proportional to their diversity. However, nearly all obligated freshwater cetartiodactylans are among the top conservation priority species. Further, ∼74% and 40% of fully aquatic cetartiodactylans and carnivores, respectively, are either threatened or data deficient, more so than their terrestrial relatives. Strikingly, only 3% of all ‘high priority’ species are thought to be stable. An overwhelming 97% of these species thus either show decreasing population trends (87%) or are insufficiently known (10%). Furthermore, a disproportional number of highly evolutionarily distinct species are experiencing population decline, thus, such species should be closely monitored even if not currently threatened. Comparison among methods reveals that exact species ranking differs considerably among methods, nevertheless, most top priority species consistently rank high under any method. While we here favor one approach, we also suggest that a consensus approach may be useful when methods disagree.

Conclusions/Significance

These results reinforce prior findings, suggesting there is an urgent need to gather basic conservation data for aquatic mammals, and special conservation focus is needed on those confined to freshwater. That evolutionarily distinct—and thus ‘biodiverse’—species are faring relatively poorly is alarming and requires further study. Our results offer a detailed guide to phylogeny-based conservation prioritization for these two orders.     

Global diversity of tardigrades (Tardigrada) in freshwater

Tardigrada is a phylum closely allied with the arthropods. They are usually less than 0.5 mm in length, have four pairs of lobe-like legs and are either carnivorous or feed on plant material. Most of the 900+ described tardigrade species are limnoterrestrial and live in the thin film of water on the surface of moss, lichens, algae, and other plants and depend on water to remain active and complete their life cycle. In this review of 910 tardigrade species, only 62 species representing13 genera are truly aquatic and not found in limnoterrestrial habitats although many other genera contain limnoterrestrial species occasionally found in freshwater. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Role of fungi in freshwater ecosystems

There are more than 600 species of freshwater fungi with a greater number known from temperate, as compared to tropical, regions. Three main groups can be considered which include Ingoldian fungi, aquatic ascomycetes and non-Ingoldian hyphomycetes, chytrids and, oomycetes. The fungi occurring in lentic habitats mostly differ from those occurring in lotic habitats. Although there is no comprehensive work dealing with the biogeography of all groups of freshwater fungi, their distribution probably follows that of Ingoldian fungi, which are either cosmopolitan, restricted to pantemperate or pantropical regions, or in a few cases, have a restricted distribution. Freshwater fungi are thought to have evolved from terrestrial ancestors. Many species are clearly adapted to life in freshwater as their propagules have specialised aquatic dispersal abilities. Freshwater fungi are involved in the decay of wood and leafy material and also cause diseases of plants and animals. These areas are briefly reviewed. Gaps in our knowledge of freshwater fungi are discussed and areas in need of research are suggested.     

Global diversity of large branchiopods (Crustacea: Branchiopoda) in freshwater

With about 500 known species worldwide, the large brachiopods are a relatively small group of primitive crustaceans. With few exceptions they live in temporary aquatic systems that are most abundant in arid and semi arid areas. As many regions remain unexplored and as especially the number of species in clam shrimps and tadpole shrimps is underestimated due to difficult identification, the species list will increase with future surveys. The Branchiopoda are monophyletic, but inter-ordinal relationships, as well as many evolutionary relationships at lower taxonomic levels are still unclear. Ongoing molecular studies will more accurately depict species diversity and phylogenetic patterns. With the exception of some anostracan families, most families are not restricted to the northern or southern hemisphere or specific zoogeographical regions. Large branchiopods are used for the assessment of the quality and function of temporary wetlands. Due to the reduction in number and quality of temporary wetlands, several species became endangered and are red listed by the IUCN. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

A study of the salt lakes and salt springs of Eyre Peninsula, South Australia

An 18-month-study of 40 saline wetlands, ranging from 6 to 336 g l⁻¹, on the west and southern coasts of Eyre Peninsula yielded 88 species of invertebrates, some aquatic plants and a fish. The invertebrates are taxonomically diverse and include 38 crustaceans, 28 insects, 12 molluscs and significantly an aquatic spider, a nemertean, two polychaetes, two sea anemones, a sponge and a bryzoan. Most were tolerant of wide fluctuations in salinity, there being 51 halobionts, 21 halophils and only 16 salt-tolerant freshwater species. Many invertebrates are restricted to the thalassic springs where marine molluscs dominated. Athalassic wetlands were dominated by crustaceans and were of two basic types—coastal and continental. There is evidence of the former evolving biologically into the later, and for some lakes to be still in transition. There is also evidence of increasing salinity in recent decades and already two lakes exhibit severe secondary salinity. Like other salt lakes in Australia the fauna is regionally distinctive. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest Editors: J. John & B. Timms Salt Lake Research: Biodiversity and Conservation—Selected papers from the 9th Conference of the International Society for Salt Lake Research     

The nature of biodiversity in hypogean waters and how it is endangered

The specialised aquatic hypogean, i.e. stygobiotic, fauna has been recognised in some regions moderately rich. Slovenia, the broader Dinaric region, and Europe are particularly rich with about 7–8% of all Metazoa and about 40% of Crustacea species being stygobionts. The hypogean biotic diversity is in general predominantly a crustacean diversity. The high number of stygobiont Crustacea–Malacostraca species can be explained by the near absence of Insecta as well as by their high endemicity and sometimes additional specialisation, i.e. the spatial and ecological partition of the environment by the species. Although one cave system may exceptionally shelter up to 40 stygobiont species, they are distributed there into separate associations. Among more than 2000 described stygobiontic Malacostraca species, which include close to 950 Amphipoda, the species numbers within some genera are very high (e.g. Niphargus with 275 spp.). With 10 orders represented the higher taxonomic diversity of stygobiont Malacostraca matches that of fresh waters or the sea. Comparison of some faunas shows that the limiting factors for biodiversity might be the lower ecological diversity of habitats and restricted food resources underground, both brought about to a high degree by the darkness and absence of plants. Being K-strategists, stygobionts are endangered by any sudden changes in their environment. In the case of an increased food input by modest organic pollution, they can be outcompeted by energetically demanding but competitively stronger recent immigrants from surface.     

How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species

1. How species reach and persist in isolated habitats remains an open question in many cases, especially for rapidly spreading invasive species. This is particularly true for temporary freshwater ponds, which can be remote and may dry out annually, but may still harbour high biodiversity. Persistence in such habitats depends on recurrent colonisation or species survival capacity, and ponds therefore provide an ideal system to investigate dispersal and connectivity. 2. Here, we test the hypothesis that the wide distributions and invasive potential of aquatic snails is due to their ability to exploit several dispersal vectors in different landscapes. We explored the population structure of Physa acuta (recent synonyms: Haitia acuta, Physella acuta, Pulmonata: Gastropoda), an invasive aquatic snail originating from North America, but established in temporary ponds in Doñana National Park, southern Spain. In this area, snails face land barriers when attempting to colonise other suitable habitat. 3. Genetic analyses using six microsatellite loci from 271 snails in 21 sites indicated that (i) geographically and hydrologically isolated snail populations in the park were genetically similar to a large snail population in rice fields more than 15 km away; (ii) these isolated ponds showed an isolation‐by‐distance pattern. This pattern broke down, however, for those ponds visited frequently by large mammals such as cattle, deer and wild boar; (iii) snail populations were panmictic in flooded and hydrologically connected rice fields. 4. These results support the notion that aquatic snails disperse readily by direct water connections in the flooded rice fields, can be carried by waterbirds flying between the rice fields and the park and may disperse between ponds within the park by attaching to large mammals. 5. The potential for aquatic snails such as Physa acuta to exploit several dispersal vectors may contribute to their wide distribution on various continents and their success as invasive species. We suggest that the interaction between different dispersal vectors, their relation to specific habitats and consequences at different geographic scales should be considered both when attempting to control invasive freshwater species and when protecting endangered species.     

Distribution of the freshwater fishes of Japan: an historical overview

Japanese freshwater fishes, including lampreys, comprise 15 orders, 35 families, and 96 genera, with 211 species and subspecies. Most belong to the families Cyprinidae (29% of species and subspecies), Gobiidae (21%), Salmonidae (10%), and Cobitidae (8%). Cyprinids and cobitids presumably originated from east Asia, gobiids from southeast Asia, and cottids and salmonids from the north Pacific. Japanese freshwater fishes include 88 endemic species and subspecies, of which three have been extirpated. Fishes introduced into natural rivers and lakes for inland commercial fisheries and sport fishing, and by accident, include many exotic species, of which 23 now inhabit natural freshwaters. These often have destroyed the local fish fauna by predation, and caused genetic pollution by hybridization with local strains. Destruction of freshwater environments by land development also poses a threat to Japanese freshwater fish communities. In addition Japanese freshwater systems have been markedly altered by development of rice paddy fields which have caused some species to decline but others to flourish, and changed the distribution patterns of fishes between upstream and downstream areas. To conserve endangered species and declining communities of Japanese freshwater fishes, we need to clarify the characteristics of their original habitats and the effects of developing paddy fields, from both the ecological and historical points of view.     

Global diversity of crayfish (Astacidae, Cambaridae, and Parastacidae––Decapoda) in freshwater

The freshwater crayfishes are distributed across all but the Indian and Antarctic continents with centers of diversity in the southeastern Appalachian Mountains in the Northern Hemisphere and in south–east Australia in the Southern Hemisphere. There are currently over 640 described species of freshwater crayfishes with an average of 5–10 species still being described each year. Freshwater crayfishes can serve as keystone species in aquatic habitats, but a few species are also significantly invasive and can cause impressive damage to the fragile freshwater habitat. Crayfishes inhabit caves, burrows, streams, lakes and strong burrowers can even be found in terrestrial habitats where they have burrowed to the water table or where rainfall is sufficiently abundant to provide the needed moisture. The freshwater crayfishes, like the habitats in which they are encountered, are generally endangered to some degree and conservation efforts would do well to focus on them as key elements of the freshwater ecosystem. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment     

Pervasive decline of subtropical aquatic insects over 20 years driven by water transparency,non-native fish and stoichiometric imbalance

Insect abundance and diversity are declining worldwide. Although recent research found freshwater insect populations to be increasing in some regions, there is a critical lack of data from tropical and subtropical regions. Here, we examine a 20-year monitoring dataset of freshwater insects from a subtropical floodplain comprising a diverse suite of rivers, shallow lakes, channels and backwaters. We found a pervasive decline in abundance of all major insect orders (Odonata, Ephemeroptera, Trichoptera, Megaloptera, Coleoptera, Hemiptera and Diptera) and families, regardless of their functional role or body size. Similarly, Chironomidae species richness decreased over the same time period. The main drivers of this pervasive insect decline were increased concurrent invasions of non-native insectivorous fish, water transparency and changes to water stoichiometry (i.e. N : P ratios) over time. All these drivers represent human impacts caused by reservoir construction. This work sheds light on the importance of long-term studies for a deeper understanding of human-induced impacts on aquatic insects. We highlight that extended anthropogenic impact monitoring and mitigation actions are pivotal in maintaining freshwater ecosystem integrity.     

Relating fish kills to upwellings and wind patterns in the Salton Sea

Awareness of pond conservation value is growing all over Europe. Ponds are recognized as important ecosystems supporting large numbers of species and several rare and threatened aquatic plants, macroinvertebrates and amphibians. Notwithstanding ponds, particularly temporary ones, are still neglected in Italy. There are some gaps in our understanding of the macrophyte ecology and the conservation value of Mediterranean small still waters. Therefore, this study investigated the macrophyte communities and physico-chemical characteristics of 8 permanent and 13 temporary ponds along the Tyrrhenian coast near Rome, with the aim to relate the distribution of aquatic plants to environmental variables, and to define the botanical conservation value of ponds. Throughout the study period (Spring 2002), Principal Component Analysis performed on abiotic variables clearly discriminated temporary ponds, smaller and more eutrophic, from permanent ponds, larger and with higher pH and oxygen concentration. A total of 73 macrophyte taxa were collected in the study ponds. Temporary waters hosted a smaller number of plant species than permanent ones. Besides hydroperiod length, the environmental factors related to plant richness were maximum depth, surface area, dissolved oxygen and nitrogen concentration in the water. Moreover, the Non-metric Multidimensional Scaling showed a high dissimilarity in the taxonomic composition of aquatic plants between temporary and permanent ponds. The former contained more annual fast-growing species (Callitriche sp. pl. and Ranunculus sp. pl.), while in the latter species with long life-cycles (i.e. Potamogeton sp. pl.) were more abundant. Our results highlighted that temporary and permanent ponds in central Italy have different macrophyte assemblages, with aquatic species (including some of conservation interest at regional scale) exclusively found in each pond type. This suggested that both type of ponds could give an irreplaceable contribution to the conservation of aquatic plant diversity of these freshwater ecosystems. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: R. Céréghino, J. Biggs, B. Oertli & S. Declerck The ecology of European ponds: defining the characteristics of a neglected freshwater habitat     

Management of an ornamental pond as a conservation site for a threatened native fish species, crucian carp Carassius carassius

Ornamental ponds are important sites for conserving threatened native fish species (e.g. crucian carp Carassius carassius L.), but pond management plans rarely include considerations of native fishes. We developed and implemented a management plan for a small (0.8 h), ornamental estate pond in Hertfordshire (England) using historical information (aquatic plant and animal surveys) and a 9-year data set on climatic variables and crucian carp body condition. Crucian carp growth was not correlated with climatic variables, but body condition decreased with increasing temperature (in degree-days), which suggests that temperature influences on growth are counter-balanced by environmental factors. Management included the removal of one fish species (to eliminate hybridization with another species) and the introduction of two native species (to re-balance the fish assemblage), a reduction in floating aquatic plants (to reduce shading of the sediments) as well as the use of a chemical agent to compact the pond’s fine sediments and barley straw to enhance invertebrate habitat and thus fish prey production. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: R. Céréghino, J. Biggs, B. Oertli and S. Declerck The ecology of European ponds: defining the characteristics of a neglected freshwater habitat     

Threatened native freshwater fishes in Australia–some case histories

Case histories of some of Australia's most threatened native freshwater fishes are presented. These include: six endangered species, Galaxias fontanus, G. johnsroni, G. pedderensis (Galaxiidae), Melanataenia euchamensis (Melanotaeniidae), Maccullochella sp. nov. and M. macquariensis (Percichthyidae): one vulnerable species, Galaxias tanycephalus: two potentially threatened species. Galaxias parvus and Prototroctes maraena (Prototroctidae); one indeterminate species. Maccllochella sp.; one restricted species, Macquaria australasica (Percichthyidae). Aspects of their taxonomy, distribution and reasons for their decline are discussed. Conservation management strategies that have been or are being applied to most of these species include protection of the fish and their habitats, establishment of refuge populations, and artificial propagation and re-establishment programmes.     

Endemism and diversification in freshwater insects of Madagascar revealed by coalescent and phylogenetic analysis of museum and field collections

The biodiversity and endemism of Madagascar are among the most extraordinary and endangered in the world. This includes the island’s freshwater biodiversity, although detailed knowledge of the diversity, endemism, and biogeographic origin of freshwater invertebrates is lacking. The aquatic immature stages of mayflies (Ephemeroptera) are widely used as bio-indicators and form an important component of Malagasy freshwater biodiversity. Many species are thought to be microendemics, restricted to single river basins in forested areas, making them particularly sensitive to habitat reduction and degradation. The Heptageniidae are a globally diverse family of mayflies (>500 species) but remain practically unknown in Madagascar except for two species described in 1996. The standard approach to understanding their diversity, endemism, and origin would require extensive field sampling on several continents and years of taxonomic work followed by phylogenetic analysis. Here we circumvent this using museum collections and freshly collected individuals in a combined approach of DNA taxonomy and phylogeny. The coalescent-based GMYC analysis of DNA barcode data (mitochondrial COI) revealed 14 putative species on Madagascar, 70% of which were microendemics. A phylogenetic analysis that included African and Asian species and data from two mitochondrial and four nuclear loci indicated the Malagasy Heptageniidae are monophyletic and sister to African species. The genus Compsoneuria is shown to be paraphyletic and the genus Notonurus is reinstalled for African and Malagasy species previously placed in Compsoneuria. A molecular clock excluded a Gondwanan vicariance origin and instead favoured a more recent overseas colonization of Madagascar. The observed monophyly and high microendemism highlight their conservation importance and suggest the DNA-based approach can rapidly provide information on the diversity, endemism, and origin of freshwater biodiversity. Our results underline the important role that museum collections can play in molecular studies, especially in critically endangered biodiversity hotspots like Madagascar where entire species or populations may go extinct very quickly.     

Comparative approaches to understand metal bioaccumulation in aquatic animals

Over the past decades, comparative physiology and biochemistry approaches have played a significant role in understanding the complexity of metal bioaccumulation in aquatic animals. Such a comparative approach is now further aided by the biokinetic modeling approach which can be used to predict the rates and routes of metal bioaccumulation and assist in the interpretation of accumulated body metal concentrations in aquatic animals. In this review, we illustrate a few examples of using the combined comparative and biokinetic modeling approaches to further our understanding of metal accumulation in aquatic animals. We highlight recent studies on the different accumulation patterns of metals in different species of invertebrates and fish, and between various aquatic systems (freshwater and marine). Comparative metal biokinetics can explain the differences in metal bioaccumulation among bivalves, although it is still difficult to explain the evolutionary basis for the different accumulated metal body concentrations (e.g., why some species have high metal concentrations). Both physiological/biochemical responses and metal geochemistry are responsible for the differences in metal concentrations observed in different populations of aquatic species, or between freshwater and marine species. A comparative approach is especially important for metal biology research, due to the very complicated and potentially variable physiological handling of metals during their accumulation, sequestration, distribution and elimination in different aquatic species or between different aquatic systems.     

环境DNA技术在淡水底栖大型无脊椎动物多样性监测中的应用

环境DNA (eDNA)是指生物有机体在环境中(例如土壤、沉积物或水体)遗留下的DNA片段。eDNA技术是指从环境中提取DNA片段进行测序以及数据分析来反映环境中的物种或群落信息。与传统方法相比, eDNA技术具有高灵敏度、省时省力、无损伤等优点。目前, eDNA技术已成为一种新的水生生物监测方法, 主要应用于水生生物的多样性研究、濒危和稀有动物的物种状态及外来入侵动物扩散动态的监测等。本文从eDNA技术在水生生物多样性监测应用领域的发展历程、eDNA技术的操作流程以及其在监测淡水底栖大型无脊椎动物方面的应用进展、技术优势和局限性五个方面进行了综述。最后, 本文对eDNA技术在淡水底栖大型无脊椎动物多样性监测应用的发展趋势和前景作出展望。     

Turtles in trouble. Conservation ecology and priorities for Australian freshwater turtles

The Australian freshwater turtle fauna is dominated by species in the family Chelidae. The extant fauna comprises a series of distinct lineages, each of considerable antiquity, relicts of a more extensive and perhaps diverse fauna that existed when wetter climes prevailed. Several phylogenetically distinctive species are restricted to single, often small, drainage basins, which presents challenges for their conservation. Specific threats include water resource development, which alters the magnitude, frequency, and timing of flows and converts lentic to lotic habitat via dams and weirs, fragmentation of habitat, sedimentation, nutrification, and a reduction in the frequency and extent of floodplain flooding. Drainage of wetlands and altered land use are of particular concern for some species that are now very restricted in range and critically endangered. The introduced European red fox is a devastatingly efficient predator of turtle nests and can have a major impact on recruitment. In the north, species such as the northern snake-necked turtle are heavily depredated by feral pigs. Other invasive animals and aquatic weeds dramatically alter freshwater habitats, with consequential impacts on freshwater turtles. Novel pathogens such as viruses have brought at least one species to the brink of extinction. Species that routinely migrate across land are impacted by structural simplification of habitat, reduction in availability of terrestrial refugia, fencing (including conservation fencing), and in some areas, by high levels of road mortality. We report on the listing process and challenges for listing freshwater turtles under the Australian Environment Protection and Biodiversity Conservation Act, summarize the state of knowledge relevant to listing decisions, identify the key threatening processes impacting turtles, and identify key knowledge gaps that impede the setting of priorities. We also focus on how to best incorporate First Nations Knowledge into decisions on listing and discuss opportunities to engage Indigenous communities in on-ground work to achieve conservation outcomes.     

A trait-based approach to assess the vulnerability of European aquatic insects to climate change

Aquatic insects are the dominant taxon group in most freshwater ecosystems. As temperature is the main driver of their life cycle development, metabolic activity, and geographic distribution, these macroinvertebrates are particularly suitable for large scale and comparative studies of freshwater community responses to climate change. A dataset of bio-ecological traits of 1,942 Ephemeroptera, Plecoptera, and Trichoptera (EPT) taxa was used to analyze (1) the relationships among traits, (2) the potential vulnerability of EPT species to climate change, and (3) the geographical occurrence patterns of these potentially endangered species at the scale of European ecoregions. By means of a fuzzy correspondence analysis (FCA), two gradients emerged: (1) a longitudinal gradient, describing successive upstream–downstream features, and (2) a biogeographical gradient, separating endemic and micro-endemic species from widely distributed taxa. Moreover, aquatic insects of southern European ecoregions emerged as those most endangered in terms of potential vulnerability to climate change. Comparative multi-taxon studies provide important new insights into freshwater ecosystem functioning and responses to climate change, and could be the first step toward developing integrative monitoring or assessment tools (e.g., trait-based indicators at the species level) by means of non-arbitrary statistical methods.     

Environmental DNA (eDNA): Powerful technique for biodiversity conservation

Environmental DNA metabarcoding is a non-invasive method for discovering and identifying rare and endangered species in a variety of ecosystems, including aquatic environments, based on the retrieval of genetic traces emitted into the environment by animals. Environmental (e) DNA research has grown in popularity over the last decade as a result of a rise in the number of studies that employ DNA taken from the environment, particularly in freshwater and marine ecosystems. In terms of detecting diversity patterns, we may claim that DNA retrieved from the environment (eDNA) is altering the game. For resource management in fisheries, information on species composition and biomass/abundance of commercially and noncommercially harvested species is critical. The eDNA is a truly non-invasive method that inflicts no damage on the species or habitats under study even during sampling, the eDNA technique never harms any ecosystems or threatened species. This novel molecular method never affects any endangered species or ecosystem during sampling. Environmental DNA analysis has become more widely accepted and is used in the detection of the presence and absence of aquatic macrofauna, such as freshwater and marine fish. This review study may aid researchers in better understanding the current state of eDNA technology. Despite the fact that various scientists have used eDNA to investigate the worldwide biodiversity of aquatic environments, no one in India is focusing on this new technology. We conclude that the eDNA technique has the potential to become a next-generation tool for biodiversity research and aquatic ecosystem conservation.     

Global diversity of oribatids (Oribatida: Acari: Arachnida)

Oribatid mites are primarily terrestrial. Only about 90 species (less than 1% of all known oribatid species) from 10 genera are truly aquatic, with reproduction and all stages of their life cycle living in freshwater. Adaptation to aquatic conditions evolved independently in different taxa. However, many terrestrial species can also be found in aquatic habitats, either as chance stragglers from the surrounding habitats, or from periodic or unpredictable floodings, where they can survive for long periods. In spite of their low species richness aquatic oribatids can be very abundant in different freshwater habitats as in lentic (pools, lakes, water-filled microhabitats) or flowing waters (springs, rivers, streams), mainly on submerged plants. The heavily sclerotized exoskeletons of several species enables subfossil or fossil preservation in lakes or bog sediments. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment