Taxonomic complexity,population genetics,and plant conservation in Scotland

Summary

Groups of plants that are undergoing active diversification often do not fall into neat and tidy taxonomies. In such groups it can sometimes be very difficult to establish what does, and what does not, constitute a species. This presents problems for species-based conservation programmes that are based around prioritised species-lists (e.g. the UK Biodiversity Action Plans; BAPs), particularly as the inclusion or exclusion of taxa on these lists largely determines the allocation of conservation resources. This is an important issue as almost half of the BAP priority higher plant species for which Scotland has prime responsibility are taxonomically controversial.

Recent research using population genetic approaches to tackle some taxonomically complex plant groups has enhanced our understanding of their biology. Such approaches provide objective and independent assessments of whether a given entity is distinct or not. This information can then be used to contribute towards the decision making process of which taxa to prioritise for conservation, and address specific questions regarding BAP listed species. In the long term, however, a broader issue needs tackling. Actively evolving groups often contain a series of localised lineages, as well as complex populations that exhibit atypical levels of morphological diversity. These types of diversity do not fit well into a ‘standard’ species-based conservation system. In most cases protection will best be supplied by designated site protection or wider countryside habitat schemes. Where additional protection is need, a conservation policy is required that accepts the diversity in these actively evolving groups for what it is, rather than trying to squeeze it into conservation legislation derived for taxa whose delimitation is routine.     

Process‐Based Species Action Plans: an approach to conserve contemporary evolutionary processes that sustain diversity in taxonomically complex groups

Many endemic plant species belong to taxonomically complex groups. These endemics have often arisen as a consequence of recent and rapid evolutionary divergence facilitated by processes such as hybridization, polyploidy and/or breeding system transitions. The rapid and dynamic nature of divergence in taxonomically complex groups leads to problems in the implementation of traditional species‐based approaches for the conservation of the biodiversity that they contain. Firstly, the taxa of interest can be difficult to define and identify, leading to practical difficulties in implementing conservation measures. Secondly, a species‐based approach often fails to capture the complexity of diversity present in the taxonomically complex group. To accommodate these challenges, we have developed a Process‐Based Species Action Plan approach. This is designed to conserve the processes leading to the generation of biodiversity, rather than focusing on the preservation of individual named taxa. We illustrate the approach using a group of endemic tree species (Sorbus) on the Scottish island of Arran that have originated via a combination of multiple recent hybridization events and apomixis. The plan focuses on the optimization of habitat management to ensure the reproduction and regeneration of Sorbus in the zone in which these evolutionary processes operate, and to facilitate hybridization that will ensure the continued generation of diversity in this group. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 194–203.     

Lack of adequate taxonomic knowledge may hinder endemic mammal conservation in the Brazilian Atlantic Forest

The Atlantic Forest is one of the most diverse and threatened ecosystems of the world, being thus classified as one of the most important biodiversity hotspots. However, habitat loss, overexploitation, alien species, disease and pollution are not the only threats faced by native fauna and flora. The lack of adequate taxonomic knowledge hinders conservation and management efforts of endemic species. This is true even for mammals, which is the most charismatic group of animals and traditionally receive a good deal of attention from scientists and the public in general. A few examples show how this gap in local fauna information can be demise for species conservation, even misguiding management strategies: molecular data reveal a hidden marsupial diversity; the lack of taxonomic studies at the species level seriously threatens rodent conservation; and the taxonomic rearrangement of the genusBrachyteles revealed a new species and had a great impact on management strategies. New species are discovered, described and taxonomically rearranged at an astounding rate. We can only be successful in biodiversity conservation if we have at least a minimum level of knowledge about what we are trying to preserve. That is true both for researchers and for the general public. Recent taxonomic revisions may represent the turning point in Neotropical fauna knowledge, which, coupled with a greater awareness of local people about the rich biodiversity that dot their backyards, can represent a better conservation prospect for the endemics of the Atlantic Forest.     

Contrasting functional traits maintain lichen epiphyte diversity in response to climate and autogenic succession

Aim Lichen epiphytes are important for biodiversity conservation and are also widely applied as environmental indicators. However, biogeographical and ecological knowledge underpinning lichen epiphyte conservation, and the use of lichens as indicators, is based primarily on a limited range of ‘macrolichen’ species. Wider trends in epiphyte biodiversity remain largely unexplored. This paper examines the community structure of lichen epiphytes on aspen (Populus tremula L.) in Scotland, including species across all functional groups and comprising, therefore, taxonomically difficult ‘microlichens’. Location Northern Britain (Scotland). Methods Epiphytes were sampled from 12 sites throughout Scotland and examined at two scales: between and within aspen stands. Species were classified into contrasting functional groups and ordination by detrended correspondence analysis was used to summarize community structure. Results Within aspen stands (between trees) epiphyte communities showed successional patterns related to tree age. These successional patterns changed predictably for stands aligned along a climatic gradient (between stands). Main conclusions A dual climatic–successional trend in epiphyte community structure is presented. Large‐scale trends in epiphyte diversity are explained as the local response of species with contrasting functional traits to climate and autogenic succession. Turnover of functional groups between stands is positively related to β‐diversity, and ecological limits to the frequency of contrasting functional groups are presented. Accordingly, the study and application of lichen species with similar functional traits may inadequately represent patterns of biodiversity. This prompts criticism of the currently accepted conservation strategy, i.e. (1) an emphasis in the conservation literature on ‘macrolichen’ species with similar ecologies and (2) the application of lichen indices over climatically variable geographical areas.     

Genetics,taxonomy and the conservation of British <Emphasis Type="Italic">Euphrasia</Emphasis>

In Britain the genus Euphrasia comprises ca 20 diploid and tetraploid plant species, including several endemics. However, their conservation is impeded by taxonomic uncertainty. Analysis of cpDNA and AFLP variation was used to assess their taxonomic status and establish the extent of barriers to gene exchange among them. Differences in ploidy level constitute a very strong barrier to genetic exchange, although this is not absolute. The diploid endemics E. vigursii and E. rivularis form morphologically and genetically definable units which show some level of reproductive isolation. Within tetraploid Euphrasia, the species showed varying degrees of distinctness. Analysis of geographically paired samples from two widespread outcrossing taxa E. arctica and E. nemorosa provides evidence for extensive genetic exchange between them. However AFLP data indicate that this outbreeding species complex possesses a gene pool distinct from that of the widespread inbreeding tetraploids. The widespread and endemic inbreeding tetraploids contain examples of morphologically and genetically definable taxa, but also species whose distinctness is more equivocal. The conservation implications of this study are that species-based action plans are potentially suitable for conservation of the diploid endemics E. vigursii and E. rivularis. In contrast we contend that a species-based conservation framework, developed with reproductively isolated and genetically distinct groups in mind, requires modification for conservation of the complex and dynamic diversity found within the tetraploids. The adoption of ‘taxonomic’ action plans, designed to protect the evolutionary processes generating Euphrasia diversity, may provide a supplementary solution for conserving this type of variation.     

The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project

The PREDICTS project—Projecting Responses of Ecological Diversity In Changing Terrestrial Systems ( www.predicts.org.uk )—has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.     

Beyond barcodes: complex DNA taxonomy of a South Pacific Island radiation

DNA barcodes can provide rapid species identification and aid species inventories in taxonomically unstudied groups. However, the approach may fail in recently diverged groups with complex gene histories, such as those typically found on oceanic islands. We produced a DNA-based inventory of taxonomically little known diving beetles (genus Copelatus) in the Fiji archipelago, where they are a dominant component of the aquatic invertebrate fauna. Sampling from 25 localities on five islands and analysis of sequences from one nuclear (328bp histone 3) and three mitochondrial (492bp rrnL, 786bp cox1, 333bp cob) gene regions revealed high haplotype diversity, mainly originated since the Pleistocene, and subdivided into three major phylogenetic lineages and 22 statistical parsimony networks. A traditional taxonomic study delineated 25 morphologically defined species that were largely incongruent with the DNA-based groups. Haplotype diversity and their spatial arrangement demonstrated a continuum of relatedness in Fijian Copelatus, with evidence for introgression at various hierarchical levels. The study illustrates the difficulties for formal classification in evolutionarily complex lineages, and the potentially misleading conclusions obtained from either DNA barcodes or morphological traits alone. However, the sequence profile of Fijian Copelatus provides an evolutionary framework for the group and a DNA-based reference system for the integration of ecological and other biodiversity data, independent of the Linnaean naming system.     

Discovering and developing primary biodiversity data from social networking sites: A novel approach

Detailed, authoritative Digital Accessible Knowledge (DAK) about biodiversity is crucial to any biodiversity informatics or conservation project. In most developing nations, significant DAK gaps exist both geographically and taxonomically. This paper explores a novel source of photo-vouchered biodiversity occurrence data, in the form of records associated with photos posted on social networking sites (SNSs). SNSs like Flickr, Facebook, and Picasaweb allow naturalists to share images and associated metadata with other users. I explore the idea of discovering and organizing massive numbers of biodiversity occurrence records now available on SNSs. I present a proof-of-concept with Flickr as the SNS and the Snowy Owl (Bubo scandiacus) and the Monarch Butterfly (Danaus plexippus) as target species, but methods presented here can easily be used for any other SNS, region, or species group, particularly for developing, mega-diverse countries where the need for biodiversity DAK is particularly acute. These approaches are broadly applicable to animal and plant groups that are photographed and that can be identified from photographs with some degree of confidence (e.g., birds, butterflies, cetaceans, orchids, dragonflies, amphibians, plants), and thus offer a rich new source of biodiversity data.     

Mammals on the EDGE: conservation priorities based on threat and phylogeny

Conservation priority setting based on phylogenetic diversity has frequently been proposed but rarely implemented. Here, we define a simple index that measures the contribution made by different species to phylogenetic diversity and show how the index might contribute towards species-based conservation priorities. We describe procedures to control for missing species, incomplete phylogenetic resolution and uncertainty in node ages that make it possible to apply the method in poorly known clades. We also show that the index is independent of clade size in phylogenies of more than 100 species, indicating that scores from unrelated taxonomic groups are likely to be comparable. Similar scores are returned under two different species concepts, suggesting that the index is robust to taxonomic changes. The approach is applied to a near-complete species-level phylogeny of the Mammalia to generate a global priority list incorporating both phylogenetic diversity and extinction risk. The 100 highest-ranking species represent a high proportion of total mammalian diversity and include many species not usually recognised as conservation priorities. Many species that are both evolutionarily distinct and globally endangered (EDGE species) do not benefit from existing conservation projects or protected areas. The results suggest that global conservation priorities may have to be reassessed in order to prevent a disproportionately large amount of mammalian evolutionary history becoming extinct in the near future.     

Why conserve biodiversity? A multi-national exploration of stakeholders’ views on the arguments for biodiversity conservation

Given the concern about biodiversity loss, there are a number of arguments used for biodiversity conservation ranging from those emphasising the intrinsic value of biodiversity to those on the direct use value of ecosystems. Yet arguing the case for biodiversity conservation effectively requires an understanding of why people value biodiversity. We used Q methodology to explore and understand how different conservation practitioners (social and natural science researchers, environmental non-Governmental organisations and decision-makers) in nine European countries argue for conservation. We found that there was a plurality of views about biodiversity and its conservation. A moral argument and some arguments around the intrinsic and ecological value of biodiversity were held by all stakeholder groups. They also shared the view that species valuation does not justify the destruction of nature. However, there were also some differences within and between the groups, which primarily reflected the espousal of either ecocentric or anthropocentric viewpoints. Our findings suggest that moral arguments and those around biodiversity’s intrinsic and ecological value could potentially serve as a starting point for building consensus among conservation practitioners.     

Polychaetes as surrogates for marine biodiversity: lower taxonomic resolution and indicator groups

Due to conservation needs, reliable rapid-assessment methods for mapping of biodiversity are needed. One approach is to use surrogates, i.e. quantities that correlate strongly with the number of species, but are easier to obtain. The purpose of this paper is to test two polychaete surrogates, one for higher taxa and one for indicator groups, that will facilitate prediction of species richness in marine soft-bottom communities. Soft sediment is an important habitat which covers most of the ocean bottom. Data on polychaetes from the North Atlantic were used since polychaetes are often numerically dominant in the benthic assemblages, both with regard to the number of species and their abundance. In the polychaete assemblages along the Norwegian coast, richness at the genus, family and order level were significantly, linearly correlated to total species richness (r 0.92). Polychaetes in the order Terebellida were found to be a good indicator of polychaete species richness and to a lesser extent also of whole benthic assemblages. The group Terebellida is potentially well suited as an indicator group, since it contains long-lived, large species that are easy to sort from the sediment and it is well defined taxonomically. Although promising as proxies for species richness in marine biodiversity studies, the use of lower taxonomic resolution and indicator groups requires further investigations in more local areas where there are conservation issues.     

Biodiversity hotspots: hot for what?

In complex areas of international policy, such as biodiversity conservation, there is a risk that well-promoted strategies will be received by decision makers as a cure-all. The U.S.-based Conservation International is promoting biodiversity hotspots as a 'silver bullet' strategy for conserving most species for least cost. We assess the degree to which this goal is compatible with four social values that characterize the conservation movement. We find that biodiversity hotspots provide only a partial response because conservation does not treat all species as equal. We argue that explicit recognition of such values is fundamental to a structured debate contributing to the development of a common strategy for biodiversity conservation.     

Mismatched outcomes for biodiversity and ecosystem services: testing the responses of crop pollinators and wild bee biodiversity to habitat enhancement

Supporting ecosystem services and conserving biodiversity may be compatible goals, but there is concern that service‐focused interventions mostly benefit a few common species. We use a spatially replicated, multiyear experiment in four agricultural settings to test if enhancing habitat adjacent to crops increases wild bee diversity and abundance on and off crops. We found that enhanced field edges harbored more taxonomically and functionally abundant, diverse, and compositionally different bee communities compared to control edges. Enhancements did not increase the abundance or diversity of bees visiting crops, indicating that the supply of pollination services was unchanged following enhancement. We find that actions to promote crop pollination improve multiple dimensions of biodiversity, underscoring their conservation value, but these benefits may not be spilling over to crops. More work is needed to identify the conditions that promote effective co‐management of biodiversity and ecosystem services.     

Indicator groups and congruence of assemblage similarity, species richness and environmental relationships in littoral macroinvertebrates

The rapid decrease of biodiversity and limited resources for surveying it have forced researchers to devise short-cuts for biodiversity surveys and conservation planning. These short-cuts include environmental surrogates, higher taxon surrogates, indicator species and indicator groups. We considered indicator groups as surrogates for wholesale biodiversity and cross-taxon congruence in biodiversity patterns in littoral macroinvertebrates of boreal lakes. Despite the fact that we considered indicator groups amongst a wide variety of taxa, such as two-winged flies, mayflies, caddisflies, beetles, bugs and molluscs, none of the proposed groups possessed all of the qualities of a good indicator taxon for biodiversity surveys and conservation planning. We found generally weak, yet typically significant, relationships between the proposed indicator groups and remaining taxa in both species richness and assemblage similarity. Low congruence was paralleled by somewhat differing relationships of the taxonomic groups to various environmental features of lakes. Furthermore, the relationships of most indicator groups to the environmental features of lakes were not particularly strong. The present findings are unfortunate, because indicator groups did not perform well in predicting the wholesale biodiversity of littoral macroinvertebrates. Thus, there appears to be no short-cut for considering all groups of macroinvertebrates in biodiversity surveys, conservation planning and characterisation of environmental relationships of lake littoral assemblages.     

Broken barriers: human-induced changes to gene flow and introgression in animals: an examination of the ways in which humans increase genetic exchange among populations and species and the consequences for biodiversity

We identify two processes by which humans increase genetic exchange among groups of individuals: by affecting the distribution of groups and dispersal patterns across a landscape, and by affecting interbreeding among sympatric or parapatric groups. Each of these processes might then have two different effects on biodiversity: changes in the number of taxa through merging or splitting of groups, and the extinction/extirpation of taxa through effects on fitness. We review the various ways in which humans are affecting genetic exchange, and highlight the difficulties in predicting the impacts on biodiversity. Gene flow and hybridization are crucially important evolutionary forces influencing biodiversity. Humans alter natural patterns of genetic exchange in myriad ways, and these anthropogenic effects are likely to influence the genetic integrity of populations and species. We argue that taking a gene-centric view towards conservation will help resolve issues pertaining to conservation and management. Editor's suggested further reading in BioEssays A systemic view of biodiversity and its conservation: Processes, interrelationships, and human culture Abstract.     

Neutral biogeography of phylogenetically structured interaction networks

Little is known about how biogeographic processes affect the dynamics of species interactions in space and time, although it is widely accepted that they drive community assemblage. In functional interactions, such as pollination and seed dispersal, species that share common ancestry tend to retain a common number of interactions and interact with similar sets of species, a pattern more commonly observed for animals than plants. On the one hand, the most coherent explanation for the phylogenetic structure of pollination and seed dispersal networks is that species retain ecological traits over evolution, which would cause the conservation of interaction partners. On the other hand, fundamental processes of biodiversity, such as dispersal and evolutionary rates seem to have important roles shaping the observed phylogenetic structure of mutualistic networks, but no model has been created to study the effect of these processes in the phylogenetic structure of mutualistic interactions. Here, we developed a stochastic simulation model to study the evolution of two interacting groups of species, which evolve independently over the same geographical domain. In our model, individuals of the same interaction group share ecological traits, whereas individuals of different trophic groups are ecologically distinct. We show that even in the absence of ecological differences between individuals, and disregarding any conservation of phenotypical and phenological traits between species, the interplay of dispersal and speciation is still a major driver of complex phylogenetic structure of functional interactions, such as pollination and seed dispersal.     

Eco‐evolution on the edge during climate change

We urgently need to predict species responses to climate change to minimize future biodiversity loss and ensure we do not waste limited resources on ineffective conservation strategies. Currently, most predictions of species responses to climate change ignore the potential for evolution. However, evolution can alter species ecological responses, and different aspects of evolution and ecology can interact to produce complex eco‐evolutionary dynamics under climate change. Here we review how evolution could alter ecological responses to climate change on species warm and cool range margins, where evolution could be especially important. We discuss different aspects of evolution in isolation, and then synthesize results to consider how multiple evolutionary processes might interact and affect conservation strategies. On species cool range margins, the evolution of dispersal could increase range expansion rates and allow species to adapt to novel conditions in their new range. However, low genetic variation and genetic drift in small range‐front populations could also slow or halt range expansions. Together, these eco‐evolutionary effects could cause a three‐step, stop‐and‐go expansion pattern for many species. On warm range margins, isolation among populations could maintain high genetic variation that facilitates evolution to novel climates and allows species to persist longer than expected without evolution. This ‘evolutionary extinction debt’ could then prevent other species from shifting their ranges. However, as climate change increases isolation among populations, increasing dispersal mortality could select for decreased dispersal and cause rapid range contractions. Some of these eco‐evolutionary dynamics could explain why many species are not responding to climate change as predicted. We conclude by suggesting that resurveying historical studies that measured trait frequencies, the strength of selection, or heritabilities could be an efficient way to increase our eco‐evolutionary knowledge in climate change biology.     

Taxonomic and functional approaches reveal different responses of ant assemblages to land-use changes

Land-use change is well documented to cause species loss. However, our understanding of the effects of land-use change on other aspects of biodiversity is still limited. We evaluated if different land-use changes (Eucalyptus plantation and planted pasture) affect ant species and functional groups in similar ways across three Cerrado vegetation types (grassland, savanna and savanna-forest). We found that ant species and functional responses differed with land-use change in relation to frequency of occurrence and habitat specificity and fidelity. Land-use change affected species frequency of occurrence but not functional groups, indicating that species are more sensitive than functional groups to habitat transformation. Native habitats had different indicator species and functional groups compared with converted habitats. However, we did not find functional group indicators of converted habitats in any vegetation type; indicating that there is no specificity and fidelity of functional group to converted habitats and that such an approach is less sensitive to land-use changes. In savanna and savanna-forest, species and functional groups showed the same response in relation to composition with differences between native and converted habitats. Thus, functional groups will be lost when ant species are lost. In grasslands, functional group composition was similar between native and converted habitats indicating a turnover of species within functional groups. We demonstrate that both Eucalyptus plantation and planted pasture affect ant species and functional groups in different ways, with negative impacts both taxonomically and less so functionally. Therefore, we show that the two aspects of biodiversity can respond independently to land-use changes and, hence, the importance of using both taxonomic and functional group approaches to evaluate the effects of land-use change on biodiversity in savanna systems.     

The cost of policy simplification in conservation incentive programs

Incentive payments to private landowners provide a common strategy to conserve biodiversity and enhance the supply of goods and services from ecosystems. To deliver cost-effective improvements in biodiversity, payment schemes must trade-off inefficiencies that result from over-simplified policies with the administrative burden of implementing more complex incentive designs. We examine the effectiveness of different payment schemes using field parameterized, ecological economic models of extensive grazing farms. We focus on profit maximising farm management plans and use bird species as a policy-relevant indicator of biodiversity. Common policy simplifications result in a 49-100% loss in biodiversity benefits depending on the conservation target chosen. Failure to differentiate prices for conservation improvements in space is particularly problematic. Additional implementation costs that accompany more complicated policies are worth bearing even when these constitute a substantial proportion (70% or more) of the payments that would otherwise have been given to farmers.     

Shape-shifting corals: Molecular markers show morphology is evolutionarily plastic in Porites

Background  

Corals are notoriously difficult to identify at the species-level due to few diagnostic characters and variable skeletal morphology. This 'coral species problem' is an impediment to understanding the evolution and biodiversity of this important and threatened group of organisms. We examined the evolution of the nuclear ribosomal internal transcribed spacer (ITS) and mitochondrial markers (COI, putative control region) in Porites, one of the most taxonomically challenging and ecologically important genera of reef-building corals.