Publications by category
Journal articles
Laing LV, Viana J, Dempster EL, Trznadel M, Trunkfield LA, Uren Webster TM, van Aerle R, Paull GC, Wilson RJ, Mill J, et al (In Press). Bisphenol a causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio).
Epigenetics,
11(7), 526-538.
Abstract:
Bisphenol a causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio).
Bisphenol a (BPA) is a commercially important high production chemical widely used in epoxy resins and polycarbonate plastics, and is ubiquitous in the environment. Previous studies demonstrated that BPA activates estrogenic signaling pathways associated with adverse effects on reproduction in vertebrates and that exposure can induce epigenetic changes. We aimed to investigate the reproductive effects of BPA in a fish model and to document its mechanisms of toxicity. We exposed breeding groups of zebrafish (Danio rerio) to 0.01, 0.1, and 1 mg/L BPA for 15 d. We observed a significant increase in egg production, together with a reduced rate of fertilization in fish exposed to 1 mg/L BPA, associated with significant alterations in the transcription of genes involved in reproductive function and epigenetic processes in both liver and gonad tissue at concentrations representing hotspots of environmental contamination (0.1 mg/L) and above. of note, we observed reduced expression of DNA methyltransferase 1 (dnmt1) at environmentally relevant concentrations of BPA, along with a significant reduction in global DNA methylation, in testes and ovaries following exposure to 1 mg/L BPA. Our findings demonstrate that BPA disrupts reproductive processes in zebrafish, likely via estrogenic mechanisms, and that environmentally relevant concentrations of BPA are associated with altered transcription of key enzymes involved in DNA methylation maintenance. These findings provide evidence of the mechanisms of action of BPA in a model vertebrate and advocate for its reduction in the environment.
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Mosedale JR, Abernethy KE, Smart RE, Wilson RJ, Maclean IMD (In Press). Climate change impacts and adaptive strategies: lessons from the grapevine.
Glob Chang Biol,
22(11), 3814-3828.
Abstract:
Climate change impacts and adaptive strategies: lessons from the grapevine.
The cultivation of grapevines for winemaking, known as viticulture, is widely cited as a climate-sensitive agricultural system that has been used as an indicator of both historic and contemporary climate change. Numerous studies have questioned the viability of major viticulture regions under future climate projections. We review the methods used to study the impacts of climate change on viticulture in the light of what is known about the effects of climate and weather on the yields and quality of vineyard harvests. Many potential impacts of climate change on viticulture, particularly those associated with a change in climate variability or seasonal weather patterns, are rarely captured. Key biophysical characteristics of viticulture are often unaccounted for, including the variability of grapevine phenology and the exploitation of microclimatic niches that permit successful cultivation under suboptimal macroclimatic conditions. We consider how these same biophysical characteristics permit a variety of strategies by which viticulture can adapt to changing climatic conditions. The ability to realize these strategies, however, is affected by uneven exposure to risks across the winemaking sector, and the evolving capacity for decision-making within and across organizational boundaries. The role grape provenance plays in shaping perceptions of wine value and quality illustrates how conflicts of interest influence decisions about adaptive strategies within the industry. We conclude by considering what lessons can be taken from viticulture for studies of climate change impacts and the capacity for adaptation in other agricultural and natural systems.
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Maclean IMD, Suggitt AJ, Wilson RJ, Duffy JP, Bennie JJ (In Press). Fine-scale climate change: modelling spatial variation in biologically meaningful rates of warming.
Glob Chang Biol,
23(1), 256-268.
Abstract:
Fine-scale climate change: modelling spatial variation in biologically meaningful rates of warming.
The existence of fine-grain climate heterogeneity has prompted suggestions that species may be able to survive future climate change in pockets of suitable microclimate, termed 'microrefugia'. However, evidence for microrefugia is hindered by lack of understanding of how rates of warming vary across a landscape. Here, we present a model that is applied to provide fine-grained, multidecadal estimates of temperature change based on the underlying physical processes that influence microclimate. Weather station and remotely derived environmental data were used to construct physical variables that capture the effects of terrain, sea surface temperatures, altitude and surface albedo on local temperatures, which were then calibrated statistically to derive gridded estimates of temperature. We apply the model to the Lizard Peninsula, United Kingdom, to provide accurate (mean error = 1.21 °C; RMS error = 1.63 °C) hourly estimates of temperature at a resolution of 100 m for the period 1977-2014. We show that rates of warming vary across a landscape primarily due to long-term trends in weather conditions. Total warming varied from 0.87 to 1.16 °C, with the slowest rates of warming evident on north-east-facing slopes. This variation contributed to substantial spatial heterogeneity in trends in bioclimatic variables: for example, the change in the length of the frost-free season varied from +11 to -54 days and the increase in annual growing degree-days from 51 to 267 °C days. Spatial variation in warming was caused primarily by a decrease in daytime cloud cover with a resulting increase in received solar radiation, and secondarily by a decrease in the strength of westerly winds, which has amplified the effects on temperature of solar radiation on west-facing slopes. We emphasize the importance of multidecadal trends in weather conditions in determining spatial variation in rates of warming, suggesting that locations experiencing least warming may not remain consistent under future climate change.
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Hamston TJ, Wilson RJ, de Vere N, Rich TCG, Stevens JR, Cresswell JE (2017). Breeding system and spatial isolation from congeners strongly constrain seed set in an insect-pollinated apomictic tree: Sorbus subcuneata (Rosaceae).
Sci Rep,
7Abstract:
Breeding system and spatial isolation from congeners strongly constrain seed set in an insect-pollinated apomictic tree: Sorbus subcuneata (Rosaceae).
In plants, apomixis results in the production of clonal offspring via seed and can provide reproductive assurance for isolated individuals. However, many apomicts require pollination to develop functional endosperm for successful seed set (pseudogamy) and therefore risk pollination-limitation, particularly in self-incompatible species that require heterospecific pollen. We used microsatellite paternity analysis and hand pollinations to investigate pollen-limitation in Sorbus subcuneata, a threatened endemic tree that co-occurs with its congener, S. admonitor. We confirmed that S. subcuneata is an obligate pseudogamous apomict, but open-pollinated flowers rarely produced seed (flower-to-seed conversion
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Zografou K, Wilson RJ, Halley JM, Tzirkalli E, Kati V (2017). How are arthopod communities structured and why are they so diverse? Answers from Mediterranean mountains using hierarchical additive partitioning.
Biodiversity and Conservation,
26(6), 1333-1351.
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How are arthopod communities structured and why are they so diverse? Answers from Mediterranean mountains using hierarchical additive partitioning
© 2017, Springer Science+Business Media Dordrecht. Mountains are complex ecosystems supporting a great variety of taxa. Here, we explored the diversity patterns of arthropods in two mountains, pinpointing the spatial scale that accounts most for overall diversity variation, using an additive partitioning framework. Butterflies and Orthoptera were sampled in Rodopi (2012) and Grammos (2013) mountains. Diversity was partitioned into five hierarchical levels (mountain, elevational zone, habitat, transect and plot). We compared the estimated diversity values for each level to the respective permuted values expected by chance, for all species, as well as for species identified as “rare” or “common”. At broader spatial levels, the variation in total diversity was attributed to the beta diversity component: mountains accounted for 20.94 and 26.25% of butterfly and Orthoptera diversity, and elevational zones accounted for 28.94 and 35.87% respectively. At finer spatial scales, beta diversity was higher than expected by chance in terms of the Shannon index. The type of habitat was found to play a significant role only for rare orthopterans. Finally, common species were recognized for shaping overall species diversity. We highlight the importance of the spatial levels of elevation zone and then mountain position in conservation planning, due to the greater beta diversity recorded at this scale as compared to habitat or more finite scales. Monitoring programs might need to adapt different strategies with respect to the focal organisms, and consider patterns of common rather than rare species that found to drive the patterns of the entire community.
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Donaldson L, Wilson RJ, Maclean IMD (2017). Old concepts, new challenges: adapting landscape-scale conservation to the twenty-first century.
Biodiversity and Conservation,
26(3), 527-552.
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Old concepts, new challenges: adapting landscape-scale conservation to the twenty-first century
� 2016, the Author(s). Landscape-scale approaches to conservation stem largely from the classic ideas of reserve design: encouraging bigger and more sites, enhancing connectivity among sites, and improving habitat quality. Trade-offs are imposed between these four strategies by the limited resources and opportunities available for conservation programmes, including the establishment and management of protected areas, and wildlife-friendly farming and forestry. Although debate regarding trade-offs between the size, number, connectivity and quality of protected areas was prevalent in the 1970–1990s, the implications of the same trade-offs for ongoing conservation responses to threats from accelerating environmental change have rarely been addressed. Here, we reassess the implications of reserve design theory for landscape-scale conservation, and present a blueprint to help practitioners to prioritise among the four strategies. We consider the new perspectives placed on landscape-scale conservation programmes by twenty-first century pressures including climate change, invasive species and the need to marry food security with biodiversity conservation. A framework of the situations under which available theory and evidence recommend that each of the four strategies be prioritized is provided, seeking to increase the clarity required for urgent conservation decision-making.
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Gutierrez D, Vila R, Wilson RJ (2016). Asymmetric constraints on limits to species ranges influence consumer-resource richness over an environmental gradient.
Global Ecology and Biogeography: a journal of macroecologyAbstract:
Asymmetric constraints on limits to species ranges influence consumer-resource richness over an environmental gradient
ABSTRACT
Aim There is little consensus about the relative roles of biotic versus abiotic factors in setting limits to species distributions or in generating geographical patterns of species richness. However, despite the probable importance of host availability in governing the distribution and diversity of consumers, few studies have simultaneously tested the effects of resource distribution and diversity on consumer ranges and richness patterns.
Location
Sierra de Guadarrama, central Spain.
Methods
We examined the effects of biotic resources, consumer attributes and climate on the ranges and species richness patterns of 43 specialist
butterflies at 40 sites over a 1800-m elevational gradient. Evidence for resource use was based on comprehensive field records of oviposition and larval feeding on host plants.
Results
We show that limitation by either biotic interactions with resources (the distributions and parts eaten of the larval host plants) or intrinsic dispersal ability was stronger at upper than lower elevational range limits for butterflies. Both resource and consumer richness followed a unimodal, humped pattern over the elevational gradient, but host plant richness peaked 300 m lower than butterfly richness. In addition, whereas changes in butterfly species richness were roughly symmetrical around peak richness over the gradient studied, the host plants showed markedly lower species richness at high elevations (> 1750 m). Butterfly species richness increased with host plant resource diversity and relative humidity, with a steeper response to host plant richness in cooler sites (at higher elevations).
Main conclusions
The results demonstrate the role of bottom-up control by resource availability in limiting consumer distributions and richness. Importantly, resource limitation had increasing relevance towards the coolest parts of environmental gradients and those poorest in resource species, with potential consequences for ecological responses to environmental change.
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Fitzgerald JA, Jameson HM, Fowler VHD, Bond GL, Bickley LK, Webster TMU, Bury NR, Wilson RJ, Santos EM (2016). Hypoxia Suppressed Copper Toxicity during Early Development in Zebrafish Embryos in a Process Mediated by the Activation of the HIF Signaling Pathway.
Environ Sci Technol,
50(8), 4502-4512.
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Hypoxia Suppressed Copper Toxicity during Early Development in Zebrafish Embryos in a Process Mediated by the Activation of the HIF Signaling Pathway.
Hypoxia is a global and increasingly important stressor in aquatic ecosystems, with major impacts on biodiversity worldwide. Hypoxic waters are often contaminated with a wide range of chemicals but little is known about the interactions between these stressors. We investigated the effects of hypoxia on the responses of zebrafish (Danio rerio) embryos to copper, a widespread aquatic contaminant. We showed that during continuous exposures copper toxicity was reduced by over 2-fold under hypoxia compared to normoxia. When exposures were conducted during 24 h windows, hypoxia reduced copper toxicity during early development and increased its toxicity in hatched larvae. To investigate the role of the hypoxia signaling pathway on the suppression of copper toxicity during early development, we stabilized the hypoxia inducible factor (HIF) pathway under normoxia using a prolyl-4-hydroxylase inhibitor, dimethyloxalylglycine (DMOG) and demonstrated that HIF activation results in a strong reduction in copper toxicity. We also established that the reduction in copper toxicity during early development was independent of copper uptake, while after hatching, copper uptake was increased under hypoxia, corresponding to an increase in copper toxicity. These findings change our understanding of the current and future impacts of worldwide oxygen depletion on fish communities challenged by anthropogenic toxicants.
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Donaldson L, Woodhead AJ, Wilson RJ, Maclean IM (2016). Subsistence use of papyrus is compatible with wetland bird conservation.
Biological Conservation,
201, 414-422.
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Suggitt AJ, Jones RT, Caseldine CJ, Huntley B, Stewart JR, Brooks SJ, Brown E, Fletcher D, Gillingham PK, Larwood J, et al (2015). A meta-database of Holocene sediment cores for England.
Vegetation History and Archaeobotany,
24(6), 743-747.
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A meta-database of Holocene sediment cores for England
© 2015, Springer-Verlag Berlin Heidelberg. Extracting sediment cores for palaeoecological and archaeological investigations has occurred extensively across England since the early 20th century. Surprisingly, there has been comparatively little collation of these valuable publications and potential sources of data; for example, a search on the European Pollen Database (1st Aug 2014 edition) found just 118 core sites for the whole of Great Britain. Here, using a combination of systematic meta-searching and knowledge of the unpublished (‘grey’) literature, we have assembled a meta-database of some 763 sediment cores for palaeoecological records, documented across 273 scientific studies. The majority of these ( > 90 %) were sediment cores upon which pollen analyses had been performed, but other types of evidence, such as plant macrofossil and faunal records were also identified. We are making this meta-database publicly available, in the hope that it will assist further investigations into Holocene vegetation history, palaeoecology, geoarchaeology and environmental change.
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Suggitt AJ, Jones RT, Caseldine CJ, Huntley B, Stewart JR, Brooks SJ, Brown E, Fletcher D, Gillingham PK, Larwood J, et al (2015). A reply to ‘A meta-database of Holocene sediment cores for England: missing data’ (Tooley 2015). Vegetation History and Archaeobotany
Mosedale J, Wilson RJ, Maclean IMD (2015). Climate Change and Crop Exposure to Adverse Weather: Changes to Frost Risk and Grapevine Flowering Conditions.
PLOS ONE,
10(10).
Abstract:
Climate Change and Crop Exposure to Adverse Weather: Changes to Frost Risk and Grapevine Flowering Conditions
The cultivation of grapevines in the UK and many other cool climate regions is expected to benefit from the higher growing season temperatures predicted under future climate scenarios. Yet the effects of climate change on the risk of adverse weather conditions or events at key stages of crop development are not always captured by aggregated measures of seasonal or yearly climates, or by downscaling techniques that assume climate variability will remain unchanged under future scenarios. Using fine resolution projections of future climate scenarios for south-west England and grapevine phenology models we explore how risks to cool-climate vineyard harvests vary under future climate conditions. Results indicate that the risk of adverse conditions during flowering declines under all future climate scenarios. In contrast, the risk of late spring frosts increases under many future climate projections due to advancement in the timing of budbreak. Estimates of frost risk, however, were highly sensitive to the choice of phenology model, and future frost exposure declined when budbreak was calculated using models that included a winter chill requirement for dormancy break. The lack of robust phenological models is a major source of uncertainty concerning the impacts of future climate change on the development of cool-climate viticulture in historically marginal climatic regions.
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Nieto-Sanchez S, Gutierrez D, Wilson RJ (2015). Long-term change and spatial variation in butterfly communities over an elevation gradient: driven by climate, buffered by habitat.
Diversity and Distributions: a journal of conservation biogeographyAbstract:
Long-term change and spatial variation in butterfly communities over an elevation gradient: driven by climate, buffered by habitat.
(A) Abstract
(B) Aim
Efforts to adapt conservation to climate change are hampered by a scarcity of studies of community-level ecological responses. We examined temporal (40 years) and spatial (1700 m elevation gradient) variation in butterfly communities, aiming to test whether the composition of communities in terms of species’ thermal envelopes tracked regional warming, and whether local habitat influenced community responses to climate variation.
(B) Location
Sierra de Guadarrama (central Spain).
(B) Methods
Butterfly assemblages were sampled at sites between 550 m and 2250 m elevation, in 1967-1973 and 2006-2012. Changes in community composition over time and space were evaluated using the community temperature index, or CTI, which reflects for local assemblages the balance between species whose geographic ranges occupy regions of low versus high temperatures. We used multiple regressions and an information-theoretic approach to test: 1) whether relationships of CTI with elevation or temperature remained consistent after an estimated 1.78 °C regional warming; and 2) how spatial variation in CTI was related to air temperature and land cover.
(B) Results
CTI decreased consistently with increasing elevation, and increased after 40 years of warming, as communities were increasingly composed by species with warmer geographic ranges. Long-term CTI change represented a c. 160 m uphill shift in community thermal composition, whereas isotherms shifted 307 m upwards. In 2006-2012, CTI was influenced positively by temperature, and negatively by forest and meadow cover.
(B) Main Conclusions
Variation in community composition over space and time suggested a role of climate in structuring butterfly assemblages. Despite this, changing spatial patterns of community composition (CTI) did not appear to keep pace with climate change. In addition, lower values of CTI recorded for sites with greater forest and meadow/pasture cover suggested a role for local habitat in buffering the effects of climate change on community composition.
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Suggitt AJ, Wilson RJ, August TA, Fox R, Isaac NJB, Macgregor NA, Morecroft MD, Maclean IMD (2015). Microclimate affects landscape level persistence in the British Lepidoptera.
Journal of Insect Conservation,
19(2), 237-253.
Abstract:
Microclimate affects landscape level persistence in the British Lepidoptera
© 2014, Springer International Publishing Switzerland. Microclimate has been known to drive variation in the distribution and abundance of insects for some time. Until recently however, quantification of microclimatic effects has been limited by computing constraints and the availability of fine-scale biological data. Here, we tested fine-scale patterns of persistence/extinction in butterflies and moths against two computed indices of microclimate derived from Digital Elevation Models: a summer solar index, representing fine-scale variation in temperature, and a topographic wetness index, representing fine-scale variation in moisture availability. We found evidence of microclimate effects on persistence in each of four 20 × 20 km British landscapes selected for study (the Brecks, the Broads, Dartmoor, and Exmoor). Broadly, local extinctions occurred more frequently in areas with higher minimum or maximum solar radiation input, while responses to wetness varied with landscape context. This negative response. to solar radiation is consistent with a response to climatic warming, wherein grid squares with particularly high minimum or maximum insolation values provided an increasingly adverse microclimate as the climate warmed. The variable response to wetness in different landscapes may have reflected spatially variable trends in precipitation. We suggest that locations in the landscape featuring cooler minimum and/or maximum temperatures could act as refugia from climatic warming, and may therefore have a valuable role in adapting conservation to climatic change.
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Maclean IMD, Hopkins JJ, Bennie J, Lawson CR, Wilson RJ (2015). Microclimates buffer the responses of plant communities to climate change.
Global Ecology and Biogeography,
24(11), 1340-1350.
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Microclimates buffer the responses of plant communities to climate change
© 2015 John Wiley. &. Sons Ltd. Aim: Despite predictions of high extinction risk resulting from climate change, range expansions have been documented more frequently than range retractions, prompting suggestions that species can endure climatic changes by persisting in cool or damp microclimates. We test whether such 'microrefugia' exist. Location: the United Kingdom. Methods: We examine fine-scale changes in the plant communities of a coastal grassland over a 30-year period in which spring temperatures increased by 1.4°C. We look at whether changes in community composition and local colonizations and extinctions are related to microclimatic conditions. Results: Our findings suggest that while community reassembly was consistent with warming, changes were smaller on cooler, north-facing slopes. Closer inspection of the patterns of species turnover revealed that species with low temperature requirements were able to persist on cooler slopes, while those with high moisture requirements suffered similar decreases in occupancy across all microclimates. Main conclusions: Our results suggest that cooler slopes may act as microrefugia, buffering the effects on plant communities of increases in temperature by delaying extinctions of species with low temperature requirements.
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Wilson RJ, Bennie J, Lawson CR, Pearson D, Ortúzar-Ugarte G, Gutiérrez D (2015). Population turnover, habitat use and microclimate at the contracting range margin of a butterfly.
Journal of Insect Conservation,
19(2), 205-216.
Abstract:
Population turnover, habitat use and microclimate at the contracting range margin of a butterfly
© 2014, Springer International Publishing Switzerland. Climate change is expected to drive patterns of extinction and colonisation that are correlated with geographic gradients in the climate, such as latitude and elevation. However, local population dynamics also depend on the fine-scale effects of vegetation and topography on resource availability and microclimate. Understanding how this fine-scale variation influences population survival in the face of changing climatic favourability could provide clues for adapting conservation to climate change. Here, we document a long-term decline of the butterfly Parnassius apollo in the Sierra de Guadarrama mountain range in central Spain, and examine recent population turnover and habitat use by the species to make inferences about its ecology and conservation. A decline since the 1960s throughout the elevation range suggests a regional deterioration in favourability for the species. Since 2006, local habitat quality has been the main correlate of population persistence, with populations that persisted from 2006 to 2012 associated with high availability of larval host plants. At a finer resolution, the larval distribution in a network of suitable habitat in 2011 and 2012 was most closely related to bare ground cover. Thus, although slope, aspect and elevation lead to considerable variation in microhabitat temperatures during the perio d of P. apollo larval development, vegetation structure appears to have been the most critical factor for local habitat use and population persistence. The results show that site selection and management retain key roles in conservation despite the broad-scale effects of environmental change.
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Hodgson JA, Bennie JJ, Dale G, Longley N, Wilson RJ, Thomas CD (2015). Predicting microscale shifts in the distribution of the butterfly Plebejus argus at the northern edge of its range.
Ecography,
38(10), 998-1005.
Abstract:
Predicting microscale shifts in the distribution of the butterfly Plebejus argus at the northern edge of its range
© 2015 Nordic Society Oikos. Species are often observed to occur in restricted patches of particularly warm microclimate at their high latitude/altitude geographic range margin. In these areas, global warming is expected to cause small-scale expansion of the occupied area, but most previous studies of range expansion have used very coarse scale data. Using high resolution microclimate models together with detailed field surveys, we tested whether the butterfly Plebejus argus, occurring on limestone grassland in north Wales, was responding as might be expected due to climate change in the last 30-40 yr. The abundance of adult Plebejus argus at 100 m resolution in 2011 was strongly affected by elevation and near-ground temperatures in May. A statistical model including microclimate, fitted to 2011 data, was successful (67% correct) at hindcasting the occurrence of Plebejus argus in 1983 when the average May air temperature was 1.4°C cooler. However, the model was less accurate at hindcasting occurrences in 1972 (50% correct). Given the distribution of micro-sites in this landscape, we predict that further warming of approximately 1°C would make the majority of sites highly microclimatically suitable for this species. There are a growing number of long-term studies of range change, and investigations into the mechanisms driving them, but still surprisingly few that explicitly make and test predictions with independent data. Our tests are a valuable example of how accurate predictions of distribution change can be, but also of the inevitable uncertainties. Improved understanding of how well models predict will be very important to plan robust climate change adaptation measures.
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Gillingham PK, Bradbury RB, Roy DB, Anderson BJ, Baxter JM, Bourn NAD, Crick HQP, Findon RA, Fox R, Franco A, et al (2015). The effectiveness of protected areas in the conservation of species with changing geographical ranges.
Biological Journal of the Linnean Society,
115(3), 707-717.
Abstract:
The effectiveness of protected areas in the conservation of species with changing geographical ranges
© 2015 the Linnean Society of London. A cornerstone of conservation is the designation and management of protected areas (PAs): locations often under conservation management containing species of conservation concern, where some development and other detrimental influences are prevented or mitigated. However, the value of PAs for conserving biodiversity in the long term has been questioned given that species are changing their distributions in response to climatic change. There is a concern that PAs may become climatically unsuitable for those species that they were designated to protect, and may not be located appropriately to receive newly-colonizing species for which the climate is improving. In the present study, we analyze fine-scale distribution data from detailed resurveys of seven butterfly and 11 bird species in Great Britain aiming to examine any effect of PA designation in preventing extinctions and promoting colonizations. We found a positive effect of PA designation on species' persistence at trailing-edge warm range margins, although with a decreased magnitude at higher latitudes and altitudes. In addition, colonizations by range expanding species were more likely to occur on PAs even after altitude and latitude were taken into account. PAs will therefore remain an important strategy for conservation. The potential for PA management to mitigate the effects of climatic change for retracting species deserves further investigation.
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Zografou K, Adamidis GC, Grill A, Kati V, Wilson RJ, Halley JM (2015). Who flies first? - habitat-specific phenological shifts of butterflies and orthopterans in the light of climate change: a case study from the south-east Mediterranean.
Ecological Entomology,
40(5), 562-574.
Abstract:
Who flies first? - habitat-specific phenological shifts of butterflies and orthopterans in the light of climate change: a case study from the south-east Mediterranean
© 2015 the Royal Entomological Society. 1. Insects undergo phenological change at different rates, showing no consistent trend between habitats, time periods, species or groups. Understanding how and why this variability occurs is crucial. 2. Phenological patterns of butterflies and Orthoptera were analysed using a novel approach of standardised major axis (SMA) analysis. It was investigated whether: (i) phenology (the mean date and duration of flight) of butterflies and Orthoptera changed from one survey (1998 and 1999 respectively) to another (2011), (ii) the rate at which phenology changed differed between taxa and (iii) phenological change was significantly different across habitat types (agriculture fields, grasslands, and forests). Using the 2011 dataset, we investigated relationships between habitat-specific variables and species phenology. 3. For both groups, late-emerging species had an advanced onset on the second survey while the duration showed no consistent trend for butterflies and did not change for Orthoptera. Although the rate at which phenology changed was consistent between the two groups, at the habitat level, a longer duration of flight period emerged for butterflies in agriculture fields while Orthoptera showed no differentiation in flight duration between habitats. We found an earlier emergence of butterflies in grasslands compared to forests, attributed to habitat-specific temperature, whereas spatial variation in humidity had a significantly lower effect on butterflies' phenology in grasslands compared to forests. A gradual delay of butterfly appearances as the canopy cover increased was also found. 4. The utility of SMA analysis was demonstrated in phenological studies and evidence was detected that both habitat type and habitat-specific variables refine species' phenological responses.
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Lawson CR, Bennie JJ, Thomas CD, Hodgson JA, Wilson RJ (2014). Active Management of Protected Areas Enhances Metapopulation Expansion Under Climate Change.
Conservation Letters,
7(2), 111-118.
Abstract:
Active Management of Protected Areas Enhances Metapopulation Expansion Under Climate Change
There is a need to adapt biodiversity conservation to climate change, but few empirical studies are available to guide decision-making. Existing networks of protected areas (PAs) have been preferentially colonized during species' range expansions, but this could be due to their original habitat quality and/or to ongoing management activity. Here, we examine how PA status and active conservation management have influenced the range expansion of a butterfly Hesperia comma through fragmented landscapes. PAs under active conservation management were over three times more likely to be colonized than unprotected, unmanaged sites of the same basic vegetation type. Conservation action also increased the survival rate of existing populations inside and outside of PAs. We conclude that PAs facilitate range expansions by preventing habitat degradation and encouraging active conservation that improves habitat quality, and that conservation interventions on nondesignated sites also have a role to play in adapting conservation to climate change. © 2013 the Authors. Conservation Letters published by Wiley Periodicals, Inc.
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Gutiérrez D, Wilson RJ (2014). Climate conditions and resource availability drive return elevational migrations in a single-brooded insect.
Oecologia,
175(3), 861-873.
Abstract:
Climate conditions and resource availability drive return elevational migrations in a single-brooded insect.
Seasonal elevational migrations have important implications for life-history evolution and ecological responses to environmental change. However, for most species, particularly invertebrates, evidence is still scarce for the existence of such migrations, as well as for the potential causes. We tested the extent to which seasonal abundance patterns in central Spain for overwintering (breeding) and summer (non-breeding) individuals of the butterfly Gonepteryx rhamni were consistent with three hypotheses explaining elevational migration: resource limitation (host plant and flower availability), physiological constraints of weather (maximum temperatures) and habitat limitation (forest cover for overwintering). For overwintering adults, abundance was positively associated with host plant density during two intensive survey seasons (2007-2008), and the elevational distribution was relatively stable over a 7-year period (2006-2012). The elevational distribution of summer adults was highly variable, apparently related both to temperature and habitat type. Sites occupied by adults in the summer were on average 3 °C cooler than their breeding sites, and abundance showed negative associations with summer temperature, and positive associations with forest cover and host plant density in 2007 and 2008. The results suggest that the extent of uphill migration in summer could be driven by different factors, depending on the year, and are mostly consistent with the physiological constraint and habitat limitation hypotheses. In contrast, the patterns for overwintering adults suggest that downhill migration can be explained by resource availability. Climate change could generate bottlenecks in the populations of elevational migrant species by constraining the area of specific seasonal habitat networks or by reducing the proximity of environments used at different times of year.
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Voskamp A, Rode EJ, Coudrat CNZ, Wirdateti, Abinawanto, Wilson RJ, Nekaris KAI (2014). Modelling the habitat use and distribution of the threatened Javan slow loris Nycticebus javanicus.
Endangered Species Research,
23(3), 277-286.
Abstract:
Modelling the habitat use and distribution of the threatened Javan slow loris Nycticebus javanicus
© Inter-Research 2014. The Javan slow loris Nycticebus javanicus is threatened by habitat decline and is classified as Critically Endangered on the IUCN Red List. Information on its distribution and habitat preferences is still lacking, and so far the distribution of the Javan slow loris has only been quantified via ecological niche modelling based on museum specimens and remotely derived environmental layers. We aimed to refine the modelled predictions and to verify the distribution of the Javan slow loris by collecting up-to-date occurrence data, which are fundamental for conservation and management of the species. Furthermore, we identify variables that predict its presence and give recommendations for future survey sites and conservation actions. From April to June 2012 we collected data on species presence, habitat preferences and levels of disturbance at priority sites throughout Java. We present a map of the predicted distribution of N. javanicus based on a maxi mum entropy model. We investigated habitat preferences using R (v. 2.14.1). During the study we sighted 52 lorises in 9 out of 14 investigated areas. The amount of bamboo in a forest had a positive effect on the encounter rates. Furthermore, we made 86% of sightings in forest plantations and agricultural areas located outside protected areas, with the majority located in areas with measured high levels of disturbance. We suggest that further ecological studies are needed to understand if and why densities may be higher in anthropogenically disturbed areas.
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Wilson RJ, Bennie J, Lawson CR, Pearson D, Ortúzar-Ugarte G, Gutiérrez D (2014). Population turnover, habitat use and microclimate at the contracting range margin of a butterfly.
Journal of Insect ConservationAbstract:
Population turnover, habitat use and microclimate at the contracting range margin of a butterfly
Climate change is expected to drive patterns of extinction and colonisation that are correlated with geographic gradients in the climate, such as latitude and elevation. However, local population dynamics also depend on the fine-scale effects of vegetation and topography on resource availability and microclimate. Understanding how this fine-scale variation influences population survival in the face of changing climatic favourability could provide clues for adapting conservation to climate change. Here, we document a long-term decline of the butterfly Parnassius apollo in the Sierra de Guadarrama mountain range in central Spain, and examine recent population turnover and habitat use by the species to make inferences about its ecology and conservation. A decline since the 1960s throughout the elevation range suggests a regional deterioration in favourability for the species. Since 2006, local habitat quality has been the main correlate of population persistence, with populations that persisted from 2006 to 2012 associated with high availability of larval host plants. At a finer resolution, the larval distribution in a network of suitable habitat in 2011 and 2012 was most closely related to bare ground cover. Thus, although slope, aspect and elevation lead to considerable variation in microhabitat temperatures during the period of P. apollo larval development, vegetation structure appears to have been the most critical factor for local habitat use and population persistence. The results show that site selection and management retain key roles in conservation despite the broad-scale effects of environmental change.
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Lawson CR, Hodgson JA, Wilson RJ, Richards SA (2014). Prevalence, thresholds and the performance of presence-absence models.
Methods in Ecology and Evolution,
5(1), 54-64.
Abstract:
Prevalence, thresholds and the performance of presence-absence models
Summary: the use of species distribution models to understand and predict species' distributions necessitates tests of fit to empirical data. Numerous performance metrics have been proposed, many of which require continuous occurrence probabilities to be converted to binary 'present or absent' predictions using threshold transformations. It is widely accepted that both continuous and binary performance metrics should be independent of prevalence (the proportion of locations that are occupied). However, because these metrics have been mostly assessed on a case-specific basis, there are few general guidelines for measuring performance. Here, we develop a conceptual framework for classifying performance metrics, based on whether they are sensitive to prevalence, and whether they require binary predictions. We use this framework to investigate how these performance metric properties influence the predictions made by the models they select. A literature survey reveals that binary metrics are widely employed and that prevalence-independent metrics are used more frequently than prevalence-dependent metrics. However, we show that prevalence-dependent metrics are essential to assess the numerical accuracy of model predictions and are more useful in applications that require occupancy estimates. Furthermore, we demonstrate that in comparison with continuous metrics, binary metrics often select models that have reduced ability to separate presences from absences, make predictions which over- or underestimate occupancy and give misleading estimates of uncertainty. Importantly, models selected using binary metrics will often be of reduced practical use even when applied to ecological problems that require binary decision-making. We suggest that SDM performance should be assessed using prevalence-dependent performance metrics whenever the absolute values of occurrence predictions are important and that continuous metrics should be used instead of binary metrics whenever possible. We thus recommend the wider application of prevalence-dependent continuous metrics, particularly likelihood-based metrics such as Akaike's Information Criterion (AIC), to assess the performance of presence-absence models. © 2013 British Ecological Society.
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Bennie J, Wilson RJ, Maclean IMD, Suggitt AJ (2014). Seeing the woods for the trees - when is microclimate important in species distribution models?.
Global Change Biology,
20(9), 2699-2700.
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Zografou K, Kati V, Grill A, Wilson RJ, Tzirkalli E, Pamperis LN, Halley JM (2014). Signals of climate change in butterfly communities in a Mediterranean protected area.
PLoS One,
9(1).
Abstract:
Signals of climate change in butterfly communities in a Mediterranean protected area.
The European protected-area network will cease to be efficient for biodiversity conservation, particularly in the Mediterranean region, if species are driven out of protected areas by climate warming. Yet, no empirical evidence of how climate change influences ecological communities in Mediterranean nature reserves really exists. Here, we examine long-term (1998-2011/2012) and short-term (2011-2012) changes in the butterfly fauna of Dadia National Park (Greece) by revisiting 21 and 18 transects in 2011 and 2012 respectively, that were initially surveyed in 1998. We evaluate the temperature trend for the study area for a 22-year-period (1990-2012) in which all three butterfly surveys are included. We also assess changes in community composition and species richness in butterfly communities using information on (a) species' elevational distributions in Greece and (b) Community Temperature Index (calculated from the average temperature of species' geographical ranges in Europe, weighted by species' abundance per transect and year). Despite the protected status of Dadia NP and the subsequent stability of land use regimes, we found a marked change in butterfly community composition over a 13 year period, concomitant with an increase of annual average temperature of 0.95°C. Our analysis gave no evidence of significant year-to-year (2011-2012) variability in butterfly community composition, suggesting that the community composition change we recorded is likely the consequence of long-term environmental change, such as climate warming. We observe an increased abundance of low-elevation species whereas species mainly occurring at higher elevations in the region declined. The Community Temperature Index was found to increase in all habitats except agricultural areas. If equivalent changes occur in other protected areas and taxonomic groups across Mediterranean Europe, new conservation options and approaches for increasing species' resilience may have to be devised.
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Lawson CR, Bennie J, Hodgson JA, Thomas CD, Wilson RJ (2014). Topographic microclimates drive microhabitat associations at the range margin of a butterfly.
Ecography,
37(8), 732-740.
Abstract:
Topographic microclimates drive microhabitat associations at the range margin of a butterfly
The habitat associations of individuals underpin the dynamics of species distributions. Broad-scale gradients in climate can alter habitat associations across species' geographic ranges, but topographic heterogeneity creates local microclimates which could generate variation in habitat use at finer spatial scales. We examined the selection of microhabitats for egg-laying by populations of a thermally-constrained butterfly, the skipper Hesperia comma, across 16 sites with different regional temperatures and topographic microclimates. Using models of thermal microclimate, we examined how the association between eggs and warm bare ground microhabitats varied with ambient temperature, and predicted bare ground associations in 287 existing H. comma populations, to investigate the relative impacts of regional temperatures and topographic microclimates on microhabitat use. Eggs were most strongly associated with bare ground in relatively cool sites, indicating climate-driven changes in microhabitat use. The majority of temperature variation between study sites was attributable to topographic microclimates rather than regional temperature differences, such that changes in microhabitat associations occurred principally between north- and south-facing slopes within the same region. Predicted microhabitat associations across the UK distribution of H. comma showed that, due to the large temperature differences generated by topography, most of the between-population variation in microhabitat use occurs locally within 5 km grid squares, with a smaller proportion occurring at a regional level between 5 km squares. Our findings show how microclimatic variation generated by topography alters the habitat associations of populations at fine spatial scales, suggesting that microclimate-driven changes in habitat suitability could shape species' distribution dynamics and their responses to environmental change. © 2014 the Authors. Ecography published by Nordic Society Oikos.
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Gutiérrez D, Harcourt J, Díez SB, Gutiérrez Illán J, Wilson RJ (2013). Models of presence-absence estimate abundance as well as (or even better than) models of abundance: the case of the butterfly Parnassius apollo.
Landscape Ecology,
28(3), 401-413.
Abstract:
Models of presence-absence estimate abundance as well as (or even better than) models of abundance: the case of the butterfly Parnassius apollo
Models relating species distribution records to environmental variables are increasingly applied to biodiversity conservation. Such techniques could be valuable to predict the distribution, abundance or habitat requirements of species that are rare or otherwise difficult to survey. However, despite widely-documented positive intraspecific relationships between occupancy and abundance, few studies have demonstrated convincing associations between models of habitat suitability based on species occurrence, and observed measures of habitat quality such as abundance. Here we compared models based on field-derived abundance and distribution (presence-absence) data for a rare mountain butterfly in 2006-2008. Both model types selected consistent effects of environmental variables, which corresponded to known ecological associations of the species, suggesting that abundance and distribution may be a function of similar factors. However, the models based on occurrence data identified stronger effects of a smaller number of environmental variables, indicating less uncertainty in the factors controlling distribution. Furthermore, cross-validation of the models using observed abundance data from different years, or averaged across years, suggested a marginally stronger ability of models based on occurrence data to predict observed abundance. The results suggest that, for some species, distribution models could be efficient tools for estimating habitat quality in conservation planning or management, when information on abundance or habitat requirements is costly or impractical to obtain. © 2013 Springer Science+Business Media Dordrecht.
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Bennie J, Hodgson JA, Lawson CR, Holloway CTR, Roy DB, Brereton T, Thomas CD, Wilson RJ (2013). Range expansion through fragmented landscapes under a variable climate.
Ecol Lett,
16(7), 921-929.
Abstract:
Range expansion through fragmented landscapes under a variable climate.
Ecological responses to climate change may depend on complex patterns of variability in weather and local microclimate that overlay global increases in mean temperature. Here, we show that high-resolution temporal and spatial variability in temperature drives the dynamics of range expansion for an exemplar species, the butterfly Hesperia comma. Using fine-resolution (5 m) models of vegetation surface microclimate, we estimate the thermal suitability of 906 habitat patches at the species' range margin for 27 years. Population and metapopulation models that incorporate this dynamic microclimate surface improve predictions of observed annual changes to population density and patch occupancy dynamics during the species' range expansion from 1982 to 2009. Our findings reveal how fine-scale, short-term environmental variability drives rates and patterns of range expansion through spatially localised, intermittent episodes of expansion and contraction. Incorporating dynamic microclimates can thus improve models of species range shifts at spatial and temporal scales relevant to conservation interventions.
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Maclean IMD, Bennie JJ, Scott AJ, Wilson RJ (2012). A high-resolution model of soil and surface water conditions.
Ecological Modelling,
237-238, 109-119.
Abstract:
A high-resolution model of soil and surface water conditions
Soil moisture and surface water conditions are key determinants of plant community composition and ecosystem function, and predicting such conditions is an important step in understanding the ecological consequences of environmental change. Typically, hydrological models that use real landscape features do not simulate water conditions at the fine spatial and temporal scales that are meaningful to many plant species and ecological processes. We present a hydrological model that simulates daily soil moisture and surface water conditions at a spatial resolution of 1m×1m. The model is applied to 16km 2 of the Lizard Peninsula, UK. The model is kept computationally efficient by combining a simple lumped parameter basin approach with the distributed hydrological effects of basin topography. We also model the complex flows occurring between small basins. Code for running the model using R statistical software is provided as supplementary material. As inputs, the model uses widely available daily weather variables, 1m×1m resolution digital elevation data (LiDAR) and some simple vegetation and soil characteristics identifiable from aerial photographs. Our results indicate that when inter-basin water exchanges and the distributed effects of topography within each basin are not accounted for, the model performs less well than just assuming average conditions in time or space. However, modelling inter-basin water flow also substantially increases computer run-time. The full model is capable of correctly simulating a broad range of hydrological and soil moisture conditions, providing accurate predictions for areas that range from permanently wet through to permanently dry, as well as for ephemeral wetlands with highly variable water levels. We discuss some potential ecological applications of the model, for example in guiding conservation management. © 2012 Elsevier B.V.
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Illán JG, Gutiérrez D, Díez SB, Wilson RJ (2012). Elevational trends in butterfly phenology: Implications for species responses to climate change.
Ecological Entomology,
37(2), 134-144.
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Elevational trends in butterfly phenology: Implications for species responses to climate change
Impacts of global change on the distribution, abundance, and phenology of species have been widely documented. In particular, recent climate change has led to widespread changes in animal and plant seasonality, leading to debate about its potential to cause phenological mismatches among interacting taxa. In mountainous regions, populations of many species show pronounced phenological gradients over short geographic distances, presenting the opportunity to test for effects of climate on phenology, independent of variation in confounding fac tors such as photoperiod. Here we show for 32 butterfly species sampled for five years over a 1700 m gradient (560-2260 m) in a Mediterranean mountain range that, on average, annual flight period is delayed with elevation by 15-22 days per kilometre. Species mainly occurring at low elevations in the region, and to some extent those flying earlier in the year, showed phenological delays of 23-36 days per kilometre, whereas the flight periods of species that occupy high elevations, or fly in late summer, were consistently more synchronised over the elevation gradient. Elevational patterns in phenology appear to reflect a narrowing phenological window of opportunity for larval and adult butterfly activity of high elevation and late-flying species. Here, we speculate as to the causes of these patterns, and the consequences for our ability to predict species responses to climate change. Our results raise questions about the use of space-time substitutions in predicting phenological responses to climate change, since traits relating to flight period and environmental associations may influence the capacity of species to adapt to changing climates. © 2012 the Authors. Ecological Entomology © 2012 the Royal Entomological Society.
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Lawson CR, Bennie JJ, Thomas CD, Hodgson JA, Wilson RJ (2012). Local and landscape management of an expanding range margin under climate change.
Journal of Applied Ecology,
49(3), 552-561.
Abstract:
Local and landscape management of an expanding range margin under climate change
1.There is a pressing need to understand how to facilitate species' range shifts under climate change. However, few empirical studies are available to inform decision-making, particularly at fine spatial and temporal resolutions. 2.We present a case study of a thermally constrained habitat specialist, the silver-spotted skipper butterfly Hesperia comma, at its expanding range margin in south-eastern Britain. Using data from 724 habitat patches over a 9-year interval (2000-2009), we examined local and landscape determinants of colonization, survival and population density. We then predicted probabilities of colonization and survival for habitat patches under the observed 1982 and 2009 distributions to investigate how the factors limiting range expansions change through space and time. 3.Between 2000 and 2009, Hesperia comma continued to expand its range in Britain, but the 67 recorded colonization events were offset by 48 local extinctions. Extinctions were strongly linked to climate, occurring predominantly in cooler regions and on shaded north-facing slopes. 4.Population density and probability of survival were closely related to conditions within a site, whereas probability of colonization was largely determined by functional connectivity. Survival probability was also influenced by connectivity, suggesting that immigration helped to support extinction-prone populations (a 'rescue effect'). 5.Patch occupancy beyond the range margin was primarily constrained by colonization, but close to the expanding front, population survival became the key limiting factor. This pattern was conserved during range expansion, altering management priorities at individual sites. 6.Synthesis and applications. Previous studies on facilitating range shifts have stressed the need to increase landscape-scale connectivity to remove constraints on colonization, and our data substantiate this advice. However, we show that enhancing population survival can also help to facilitate range expansions, because populations at leading range edges face high extinction risk. Population survival can be improved directly through local management actions, such as enlarging patch size and increasing habitat quality, or indirectly by improving connectivity. Thus, local management can secure vulnerable populations at the range edge and provide larger and more stable migrant sources for future expansion and deserves consideration when facilitating range shifts under climate change. © 2012 the Authors. Journal of Applied Ecology © 2012 British Ecological Society.
Abstract.
Thomas CD, Gillingham PK, Bradbury RB, Roy DB, Anderson BJ, Baxter JM, Bourne NAD, Crick HQP, Findon RA, Fox R, et al (2012). Protected areas facilitate species' range expansions.
Proceedings of the National Academy of Sciences of the United States of America,
109(35), 14063-14068.
Abstract:
Protected areas facilitate species' range expansions
The benefits of protected areas (PAs) for biodiversity have been questioned in the context of climate change because PAs are static, whereas the distributions of species are dynamic. Current PAs may, however, continue to be important if they provide suitable locations for species to colonize at their leading-edge range boundaries, thereby enabling spread into new regions. Here, we present an empirical assessment of the role of PAs as targets for colonization during recent range expansions. Records from intensive surveys revealed that seven bird and butterfly species have colonized PAs 4.2 (median) times more frequently than expected from the availability of PAs in the landscapes colonized. Records of an additional 256 invertebrate species with less-intensive surveys supported these findings and showed that 98% of species are disproportionately associated with PAs in newly colonized parts of their ranges. Although colonizing species favor PAs in general, species vary greatly in their reliance on PAs, reflecting differences in the dependence of individual species on particular habitats and other conditions that are available only in PAs. These findings highlight the importance of current PAs for facilitating range expansions and show that a small subset of the landscape receives a high proportion of colonizations by range-expanding species.
Abstract.
Wilson RJ, Roy DB (2011). Butterflies reset the calendar. Nature Climate Change, 1(2), 101-102.
Maclean IMD, Wilson RJ, Hassall M (2011). Predicting changes in the abundance of African wetland birds by incorporating abundance-occupancy relationships into habitat association models. Diversity and Distributions, 17, 480-490.
Maclean IMD, Wilson RJ (2011). Recent ecological responses to climate change support predictions of high extinction risk. Proceedings of the National Academy of Sciences, 108, 12337-12342.
Wilson RJ, Maclean IMD (2011). Recent evidence for the climate change threat to Lepidoptera and other insects. Journal of Insect Conservation, 15(1-2), 259-268.
Illán JG, Gutiérrez D, Wilson RJ (2010). Fine-scale determinants of butterfly species richness and composition in a mountain region.
Journal of Biogeography,
37(9), 1706-1720.
Abstract:
Fine-scale determinants of butterfly species richness and composition in a mountain region
Aim: Global patterns of species richness are often considered to depend primarily on climate. We aimed to determine how topography and land cover affect species richness and composition at finer scales. Location: Sierra de Guadarrama (central Iberian Peninsula). Methods: We sampled the butterfly fauna of 180 locations (89 in 2004, 91 in 2005) at 600-2300 m elevation in a region of 10800 km 2. We recorded environmental variables at 100-m resolution using GIS, and derived generalized linear models for species density (number of species per unit area) and expected richness (number of species standardized to number of individua ls) based on variables of topoclimate (elevation and insolation) or land cover (vegetation type, geology and hydrology), or both (combined). We evaluated the models against independent data from the alternative study year. We also tested for differences in species composition among sites and years using constrained ordination (canonical correspondence analysis), and used variation partitioning analyses to quantify the independent and combined roles of topoclimate and land cover. Results: Topoclimatic, land cover and combined models were significantly related to observed species density and expected richness. Topoclimatic and combined models outperformed models based on land cover variables, showing a humped elevational diversity gradient. Both topoclimate and land cover made significant contributions to models of species composition. Main conclusions: Topoclimatic factors may dominate species richness patterns in regions with pronounced elevational gradients, as long as large areas of natural habitat remain. In contrast, both topoclimate and land cover may have important effects on species composition. Biodiversity conservation in mountainous regions therefore requires protection and management of natural habitats over a wide range of topoclimatic conditions, which may assist in facilitating range shifts and alleviating declines in species richness related to climate change. © 2010 Blackwell Publishing Ltd.
Abstract.
Wilson RJ, Davies ZG, Thomas CD (2010). Linking habitat use to range expansion rates in fragmented landscapes: a metapopulation approach. Ecography, 33, 73-82.
Illán JG, Gutiérrez D, Wilson RJ (2010). The contributions of topoclimate and land cover to species distributions and abundance: Fine-resolution tests for a mountain butterfly fauna.
Global Ecology and Biogeography,
19(2), 159-173.
Abstract:
The contributions of topoclimate and land cover to species distributions and abundance: Fine-resolution tests for a mountain butterfly fauna
Aim: Models relating species distributions to climate or habitat are widely used to predict the effects of global change on biodiversity. Most such approaches assume that climate governs coarse-scale species ranges, whereas habitat limits fine-scale distributions. We tested the influence of topoclimate and land cover on butterfly distributions and abundance in a mountain range, where climate may vary as markedly at a fine scale as land cover. Location: Sierra de Guadarrama (Spain, southern Europe). Methods: We sampled the butterfly fauna of 180 locations (89 in 2004, 91 in 2005) in a 10,800 km 2. region, and derived generalized linear models (GLMs) for species occurrence and abundance based on topoclimatic (elevation and insolation) or habitat (land cover, geology and hydrology) variables sampled at 100-m resolution using GIS. Models for each year were tested against independent data from the alternate year, using the area under the receiver operating characteristic curve (AUC) (distribution) or Spearman's rank correlation coefficient (r s ) (abundance). Results: in independent model tests, 74% of occurrence models achieved AUCs of. >. 0.7, and 85% of abundance models were significantly related to observed abundance. Topoclimatic models outperformed models based purely on land cover in 72% of occurrence models and 66% of abundance models. Including both types of variables often explained most variation in model calibration, but did not significantly improve model cross-validation relative to topoclimatic models. Hierarchical partitioning analysis confirmed the overriding effect of topoclimatic factors on species distributions, with the exception of several species for which the importance of land cover was confirmed. Main conclusions: Topoclimatic factors may dominate fine-resolution species distributions in mountain ranges where climate conditions vary markedly over short distances and large areas of natural habitat remain. Climate change is likely to be a key driver of species distributions in such systems and could have important effects on biodiversity. However, continued habitat protection may be vital to facilitate range shifts in resp onse to climate change. © 2010 Blackwell Publishing Ltd.
Abstract.
Ashton S, Gutierrez D, Wilson RJ (2009). Effects of temperature and elevation on habitat use by a rare mountain butterfly: implications for species responses to climate change. ECOL ENTOMOL
Wilson RJ, Davies ZG, Thomas CD (2009). Modelling the effect of habitat fragmentation on range expansion in a butterfly. P ROY SOC LOND B BIO
Merrill RM, Gutiérrez, D. Lewis, O.T. Gutiérrez, J. Diez SB, Wilson RJ (2008). Combined effects of climate and biotic interactions on the elevational range of a phytophagous insect. Journal of Animal Ecology, 77, 145-155.
Thomas CD, Bulman CR, Wilson RJ (2008). Where within a geographical range do species survive best? a matter of scale. Insect Conservation & Diversity, 1, 2-8.
Wilson RJ, Gutiérrez, D. Gutiérrez, J. Monserrat, V.J. (2007). An elevational shift in butterfly species richness and composition accompanying recent climate change. Global Change Biology, 13, 1873-1887.
Dormann CF, McPherson JM, Araujo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, et al (2007). Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. ECOGRAPHY, 30, 609-628.
Bulman CR, Wilson RJ, Holt AR, Early RI, Galvez Bravo L, Warren MS, Thomas CD (2007). Minimum viable metapopulation size, extinction debt and the conservation of a declining species.
ECOL APPL,
17, 1460-1473.
Abstract:
Minimum viable metapopulation size, extinction debt and the conservation of a declining species.
A key question facing conservation biologists is whether declines in species' distributions are keeping pace with landscape change, or whether current distributions overestimate probabilities of future persistence. We use metapopulations of the marsh fritillary butterfly Euphydryas aurinia in the United Kingdom as a model system to test for extinction debt in a declining species. We derive parameters for a metapopulation model (incidence function model, IFM) using information from a 625-km2 landscape where habitat patch occupancy, colonization, and extinction rates for E. aurinia depend on patch connectivity, area, and quality. We then show that habitat networks in six extant metapopulations in 16-km2 squares were larger, had longer modeled persistence times (using IFM), and higher metapopulation capacity (λM) than six extinct metapopulations. However, there was a >99% chance that one or more of the six extant metapopulations would go extinct in 100 years in the absence of further habitat loss. For 11 out of 12 networks, minimum areas of habitat needed for 95% persistence of metapopulation simulations after 100 years ranged from 80 to 142 ha (∼5–9% of land area), depending on the spatial location of habitat. The area of habitat exceeded the estimated minimum viable metapopulation size (MVM) in only two of the six extant metapopulations, and even then by only 20%. The remaining four extant networks were expected to suffer extinction in 15–126 years. MVM was consistently estimated as ∼5% of land area based on a sensitivity analysis of IFM parameters and was reduced only marginally (to ∼4%) by modeling the potential impact of long-distance colonization over wider landscapes. The results suggest a widespread extinction debt among extant metapopulations of a declining species, necessitating conservation management or reserve designation even in apparent strongholds. For threatened species, metapopulation modeling is a potential means to identify landscapes near to extinction thresholds, to which conservation measures can be targeted for the best chance of success.
Abstract.
Davies ZG, Wilson, R.J. Coles, S. Thomas, C.D. (2006). Changing habitat associations of a thermally constrained species, the silver-spotted skipper butterfly, in response to climate warming. Journal of Animal Ecology, 75, 247-256.
Wilson RJ, Gutierrez D, Gutierrez J, Martinez D, Agudo R, Monserrat VJ (2005). Changes to the elevational limits and extent of species ranges associated with climate change. ECOL LETT, 8(11), 1138-1146.
Burke S, Pullin AS, Wilson RJ, Thomas CD (2005). Selection for discontinuous life-history traits along a continuous thermal gradient in the butterfly Aricia agestis. ECOL ENTOMOL, 30, 613-619.
Davies ZG, Wilson, R.J. Brereton, T.M. Thomas, C.D. (2005). The re-expansion and improving status of the silver-spotted skipper butterfly (Hesperia comma) in Britain: a metapopulation success story. Biological Conservation, 124, 189-198.
Cabeza M, Araújo MB, Wilson RJ, Thomas CD, Cowley MJR, Moilanen A (2004). Combining probabilities of occurrence with spatial reserve design.
Journal of Applied Ecology,
41(2), 252-262.
Abstract:
Combining probabilities of occurrence with spatial reserve design
1. There is a great concern about the loss of biodiversity that calls for more nature protection. Unfortunately, the funding available for conservation is limited, and often a compromise is needed between nature protection and economic interests. Reserve selection algorithms are optimization techniques that concentrate on identifying a set of reserves that represents biodiversity efficiently. Simple approaches to reserve selection use presence-absence data assuming that if a species occurs in a selected reserve, it will persist there indefinitely. 2. A refinement of this technique is the selection of reserves according to the local probabilities of occurrence of the given species. These can be estimated from habitat models fitted by empirical modelling techniques. However, local probabilities of occurrence are not static, and are influenced by the changing threats to biodiversity in and around the reserves. 3. The effects of landscape change can be minimized when compact reserves are favoured. Compact reserves that represent all species with a given target probability of occurrence can be achieved by combining the probability approach with spatial reserve design. 4. In this study we brought together two reserve selection approaches that implicitly deal with biodiversity persistence, by combining habitat models and spatial reserve design in a single algorithm. We applied the combined algorithm to a data set of 26 species of butterflies from north Wales. 5. For the particular case study addressed in this paper, clustered reserve networks could be identified at no or a small increase in cost. 6. A new, backwards, heuristic algorithm performed better and more consistently than the regular forwards heuristic approach. 7. Synthesis and applications. The reserve selection approach presented considers habitat quality (via probabilities of occurrence) and the spatial configuration of the reserves during the selection process. Emphasis on reserve networks that include high-quality sites in an aggregated manner increases the potential for long-term persistence of species in the reserve network.
Abstract.
RJWilson, Fox R, Roy DB, Thomas CD (2004). Spatial patterns in species distributions reveal biodiversity change. Nature, 432(7015), 393-396.
RJWilson, Baker JS, Ellis S, Lineham ME (2002). Large-scale patterns of distribution and persistence at the range margins of a butterfly. Ecology, 83(12), 3357-3368.
Thomas CD, Wilson RJ, Lewis OT (2002). Short-term studies underestimate 30-generation changes in a butterfly metapopulation.
Proc Biol Sci,
269(1491), 563-569.
Abstract:
Short-term studies underestimate 30-generation changes in a butterfly metapopulation.
Most studies of rare and endangered species are based on work carried out within one generation, or over one to a few generations of the study organism. We report the results of a study that spans 30 generations (years) of the entire natural range of a butterfly race that is endemic to 35 km(2) of north Wales, UK. Short-term studies (surveys in single years and dynamics over 4 years) of this system led to the prediction that the regional distribution would be quite stable, and that colonization and extinction dynamics would be relatively unimportant. However, a longer-term study revealed unexpectedly high levels of population turnover (local extinction and colonization), affecting 18 out of the 20 patches that were occupied at any time during the period. Modelling the system (using the 'incidence function model' (IFM) for metapopulations) also showed higher levels of colonization and extinction with increasing duration of the study. The longer-term dynamics observed in this system can be compared, at a metapopulation level, with the increased levels of variation observed with increasing time that have been observed in single populations. Long-term changes may arise from local changes in the environment that make individual patches more or less suitable for the butterfly, or from unusual colonization or extinction events that take metapopulations into alternative states. One implication is that metapopulation and population viability analyses based on studies that cover only a few animal or plant generations may underestimate extinction threats.
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Author URL.
Cowley MJR, Thomas CD, Roy DB, Wilson RJ, León-Cortés JL, Gutiérrez D, Bulman CR, Quinn RM, Moss D, Gaston KJ (2001). Density-distribution relationships in British butterflies I: the effect of mobility and spatial scale. Journal of Animal Ecology, 70, 410-425.
Cowley MJR, Thomas CD, Wilson RJ, Leon-Cortes JL, Gutierrez D, Bulman CR (2001). Density-distribution relationships in British butterflies. II. An assessment of mechanisms. JOURNAL OF ANIMAL ECOLOGY, 70(3), 426-441.
Thomas CD, Bodsworth EJ, Simmons AD, RJWilson (2001). Ecological and evolutionary processes at expanding range margins. Nature, 411(6837), 577-581.
Gutiérrez D, León-Cortés JL, Menendez R, Wilson RJ, Cowley MJR, Thomas CD (2001). Metapopulations of four lepidpteran herbivores on a single host plant Lotus corniculatus. Ecology, 82, 1371-1386.
Cowley MJR, Wilson RJ, León-Cortés JL, Gutiérrez D, Bulman CR, Thomas CD (2000). Habitat-based statistical models for predicting the spatial distribution of butterflies and day-flying moths in a fragmented landscape. Journal of Applied Ecology, 37, 60-72.
Lewis OT, Wilson RJ, Harper MC (1998). Endemic butterflies on Grande Comore: habitat preferences and conservation priorities. Biological Conservation, 85, 113-121.
Chapters
Wilson RJ, Gutierrez D (2011). Effects of Climate Change on the Elevational Limits of Species Ranges. In Beever EA, Belant JL (Eds.) Ecological Consequences of Climate Change: Mechanisms, Conservation, and Management, CRC Press, Taylor & Francis Group.
Wilson RJ, Roy DB (2009). Butterfly population structure and dynamics. In Settele J, Shreeve T, Konvicka M, Dyck HV (Eds.) Ecology of Butterflies in Europe, Cambridge: Cambridge University Press, 81-96.
Wilson RJ, Davies ZG, Thomas CD (2007). Insects and climate change: processes, patterns and implications for conservation. In Stewart AJA, New TR, Lewis OT (Eds.) Insect Conservation Biology. Proceedings of the Royal Entomological Society's 22nd Symposium, CABI Publishing, 245-279.
Wilson RJ, Thomas CD (2002). Dispersal and the spatial dynamics of butterfly populations. In Bullock J, Kenward R, Hails R (Eds.) Dispersal Ecology, Blackwell Scientific Publishers, 257-278.
Taneyhill DE, Mallet JB, Wynne IR, Burke S, Pullin AS, Wilson RJ, Butlin RK, Hatcher MJ, Shorrocks B, Thomas CD, et al (2002). Estimating gene flow in endemic butterfly races: the effect of metapopulation dynamics. In Hails RS, Beringer JE, Godfray HCJ (Eds.) Genes in the Environment, Blackwell Scientific Publishers, 3-25.
Publications by year
In Press
Laing LV, Viana J, Dempster EL, Trznadel M, Trunkfield LA, Uren Webster TM, van Aerle R, Paull GC, Wilson RJ, Mill J, et al (In Press). Bisphenol a causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio).
Epigenetics,
11(7), 526-538.
Abstract:
Bisphenol a causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio).
Bisphenol a (BPA) is a commercially important high production chemical widely used in epoxy resins and polycarbonate plastics, and is ubiquitous in the environment. Previous studies demonstrated that BPA activates estrogenic signaling pathways associated with adverse effects on reproduction in vertebrates and that exposure can induce epigenetic changes. We aimed to investigate the reproductive effects of BPA in a fish model and to document its mechanisms of toxicity. We exposed breeding groups of zebrafish (Danio rerio) to 0.01, 0.1, and 1 mg/L BPA for 15 d. We observed a significant increase in egg production, together with a reduced rate of fertilization in fish exposed to 1 mg/L BPA, associated with significant alterations in the transcription of genes involved in reproductive function and epigenetic processes in both liver and gonad tissue at concentrations representing hotspots of environmental contamination (0.1 mg/L) and above. of note, we observed reduced expression of DNA methyltransferase 1 (dnmt1) at environmentally relevant concentrations of BPA, along with a significant reduction in global DNA methylation, in testes and ovaries following exposure to 1 mg/L BPA. Our findings demonstrate that BPA disrupts reproductive processes in zebrafish, likely via estrogenic mechanisms, and that environmentally relevant concentrations of BPA are associated with altered transcription of key enzymes involved in DNA methylation maintenance. These findings provide evidence of the mechanisms of action of BPA in a model vertebrate and advocate for its reduction in the environment.
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Mosedale JR, Abernethy KE, Smart RE, Wilson RJ, Maclean IMD (In Press). Climate change impacts and adaptive strategies: lessons from the grapevine.
Glob Chang Biol,
22(11), 3814-3828.
Abstract:
Climate change impacts and adaptive strategies: lessons from the grapevine.
The cultivation of grapevines for winemaking, known as viticulture, is widely cited as a climate-sensitive agricultural system that has been used as an indicator of both historic and contemporary climate change. Numerous studies have questioned the viability of major viticulture regions under future climate projections. We review the methods used to study the impacts of climate change on viticulture in the light of what is known about the effects of climate and weather on the yields and quality of vineyard harvests. Many potential impacts of climate change on viticulture, particularly those associated with a change in climate variability or seasonal weather patterns, are rarely captured. Key biophysical characteristics of viticulture are often unaccounted for, including the variability of grapevine phenology and the exploitation of microclimatic niches that permit successful cultivation under suboptimal macroclimatic conditions. We consider how these same biophysical characteristics permit a variety of strategies by which viticulture can adapt to changing climatic conditions. The ability to realize these strategies, however, is affected by uneven exposure to risks across the winemaking sector, and the evolving capacity for decision-making within and across organizational boundaries. The role grape provenance plays in shaping perceptions of wine value and quality illustrates how conflicts of interest influence decisions about adaptive strategies within the industry. We conclude by considering what lessons can be taken from viticulture for studies of climate change impacts and the capacity for adaptation in other agricultural and natural systems.
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Maclean IMD, Suggitt AJ, Wilson RJ, Duffy JP, Bennie JJ (In Press). Fine-scale climate change: modelling spatial variation in biologically meaningful rates of warming.
Glob Chang Biol,
23(1), 256-268.
Abstract:
Fine-scale climate change: modelling spatial variation in biologically meaningful rates of warming.
The existence of fine-grain climate heterogeneity has prompted suggestions that species may be able to survive future climate change in pockets of suitable microclimate, termed 'microrefugia'. However, evidence for microrefugia is hindered by lack of understanding of how rates of warming vary across a landscape. Here, we present a model that is applied to provide fine-grained, multidecadal estimates of temperature change based on the underlying physical processes that influence microclimate. Weather station and remotely derived environmental data were used to construct physical variables that capture the effects of terrain, sea surface temperatures, altitude and surface albedo on local temperatures, which were then calibrated statistically to derive gridded estimates of temperature. We apply the model to the Lizard Peninsula, United Kingdom, to provide accurate (mean error = 1.21 °C; RMS error = 1.63 °C) hourly estimates of temperature at a resolution of 100 m for the period 1977-2014. We show that rates of warming vary across a landscape primarily due to long-term trends in weather conditions. Total warming varied from 0.87 to 1.16 °C, with the slowest rates of warming evident on north-east-facing slopes. This variation contributed to substantial spatial heterogeneity in trends in bioclimatic variables: for example, the change in the length of the frost-free season varied from +11 to -54 days and the increase in annual growing degree-days from 51 to 267 °C days. Spatial variation in warming was caused primarily by a decrease in daytime cloud cover with a resulting increase in received solar radiation, and secondarily by a decrease in the strength of westerly winds, which has amplified the effects on temperature of solar radiation on west-facing slopes. We emphasize the importance of multidecadal trends in weather conditions in determining spatial variation in rates of warming, suggesting that locations experiencing least warming may not remain consistent under future climate change.
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2017
Hamston TJ, Wilson RJ, de Vere N, Rich TCG, Stevens JR, Cresswell JE (2017). Breeding system and spatial isolation from congeners strongly constrain seed set in an insect-pollinated apomictic tree: Sorbus subcuneata (Rosaceae).
Sci Rep,
7Abstract:
Breeding system and spatial isolation from congeners strongly constrain seed set in an insect-pollinated apomictic tree: Sorbus subcuneata (Rosaceae).
In plants, apomixis results in the production of clonal offspring via seed and can provide reproductive assurance for isolated individuals. However, many apomicts require pollination to develop functional endosperm for successful seed set (pseudogamy) and therefore risk pollination-limitation, particularly in self-incompatible species that require heterospecific pollen. We used microsatellite paternity analysis and hand pollinations to investigate pollen-limitation in Sorbus subcuneata, a threatened endemic tree that co-occurs with its congener, S. admonitor. We confirmed that S. subcuneata is an obligate pseudogamous apomict, but open-pollinated flowers rarely produced seed (flower-to-seed conversion
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Zografou K, Wilson RJ, Halley JM, Tzirkalli E, Kati V (2017). How are arthopod communities structured and why are they so diverse? Answers from Mediterranean mountains using hierarchical additive partitioning.
Biodiversity and Conservation,
26(6), 1333-1351.
Abstract:
How are arthopod communities structured and why are they so diverse? Answers from Mediterranean mountains using hierarchical additive partitioning
© 2017, Springer Science+Business Media Dordrecht. Mountains are complex ecosystems supporting a great variety of taxa. Here, we explored the diversity patterns of arthropods in two mountains, pinpointing the spatial scale that accounts most for overall diversity variation, using an additive partitioning framework. Butterflies and Orthoptera were sampled in Rodopi (2012) and Grammos (2013) mountains. Diversity was partitioned into five hierarchical levels (mountain, elevational zone, habitat, transect and plot). We compared the estimated diversity values for each level to the respective permuted values expected by chance, for all species, as well as for species identified as “rare” or “common”. At broader spatial levels, the variation in total diversity was attributed to the beta diversity component: mountains accounted for 20.94 and 26.25% of butterfly and Orthoptera diversity, and elevational zones accounted for 28.94 and 35.87% respectively. At finer spatial scales, beta diversity was higher than expected by chance in terms of the Shannon index. The type of habitat was found to play a significant role only for rare orthopterans. Finally, common species were recognized for shaping overall species diversity. We highlight the importance of the spatial levels of elevation zone and then mountain position in conservation planning, due to the greater beta diversity recorded at this scale as compared to habitat or more finite scales. Monitoring programs might need to adapt different strategies with respect to the focal organisms, and consider patterns of common rather than rare species that found to drive the patterns of the entire community.
Abstract.
Donaldson L, Wilson RJ, Maclean IMD (2017). Old concepts, new challenges: adapting landscape-scale conservation to the twenty-first century.
Biodiversity and Conservation,
26(3), 527-552.
Abstract:
Old concepts, new challenges: adapting landscape-scale conservation to the twenty-first century
� 2016, the Author(s). Landscape-scale approaches to conservation stem largely from the classic ideas of reserve design: encouraging bigger and more sites, enhancing connectivity among sites, and improving habitat quality. Trade-offs are imposed between these four strategies by the limited resources and opportunities available for conservation programmes, including the establishment and management of protected areas, and wildlife-friendly farming and forestry. Although debate regarding trade-offs between the size, number, connectivity and quality of protected areas was prevalent in the 1970–1990s, the implications of the same trade-offs for ongoing conservation responses to threats from accelerating environmental change have rarely been addressed. Here, we reassess the implications of reserve design theory for landscape-scale conservation, and present a blueprint to help practitioners to prioritise among the four strategies. We consider the new perspectives placed on landscape-scale conservation programmes by twenty-first century pressures including climate change, invasive species and the need to marry food security with biodiversity conservation. A framework of the situations under which available theory and evidence recommend that each of the four strategies be prioritized is provided, seeking to increase the clarity required for urgent conservation decision-making.
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2016
Gutierrez D, Vila R, Wilson RJ (2016). Asymmetric constraints on limits to species ranges influence consumer-resource richness over an environmental gradient.
Global Ecology and Biogeography: a journal of macroecologyAbstract:
Asymmetric constraints on limits to species ranges influence consumer-resource richness over an environmental gradient
ABSTRACT
Aim There is little consensus about the relative roles of biotic versus abiotic factors in setting limits to species distributions or in generating geographical patterns of species richness. However, despite the probable importance of host availability in governing the distribution and diversity of consumers, few studies have simultaneously tested the effects of resource distribution and diversity on consumer ranges and richness patterns.
Location
Sierra de Guadarrama, central Spain.
Methods
We examined the effects of biotic resources, consumer attributes and climate on the ranges and species richness patterns of 43 specialist
butterflies at 40 sites over a 1800-m elevational gradient. Evidence for resource use was based on comprehensive field records of oviposition and larval feeding on host plants.
Results
We show that limitation by either biotic interactions with resources (the distributions and parts eaten of the larval host plants) or intrinsic dispersal ability was stronger at upper than lower elevational range limits for butterflies. Both resource and consumer richness followed a unimodal, humped pattern over the elevational gradient, but host plant richness peaked 300 m lower than butterfly richness. In addition, whereas changes in butterfly species richness were roughly symmetrical around peak richness over the gradient studied, the host plants showed markedly lower species richness at high elevations (> 1750 m). Butterfly species richness increased with host plant resource diversity and relative humidity, with a steeper response to host plant richness in cooler sites (at higher elevations).
Main conclusions
The results demonstrate the role of bottom-up control by resource availability in limiting consumer distributions and richness. Importantly, resource limitation had increasing relevance towards the coolest parts of environmental gradients and those poorest in resource species, with potential consequences for ecological responses to environmental change.
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Fitzgerald JA, Jameson HM, Fowler VHD, Bond GL, Bickley LK, Webster TMU, Bury NR, Wilson RJ, Santos EM (2016). Hypoxia Suppressed Copper Toxicity during Early Development in Zebrafish Embryos in a Process Mediated by the Activation of the HIF Signaling Pathway.
Environ Sci Technol,
50(8), 4502-4512.
Abstract:
Hypoxia Suppressed Copper Toxicity during Early Development in Zebrafish Embryos in a Process Mediated by the Activation of the HIF Signaling Pathway.
Hypoxia is a global and increasingly important stressor in aquatic ecosystems, with major impacts on biodiversity worldwide. Hypoxic waters are often contaminated with a wide range of chemicals but little is known about the interactions between these stressors. We investigated the effects of hypoxia on the responses of zebrafish (Danio rerio) embryos to copper, a widespread aquatic contaminant. We showed that during continuous exposures copper toxicity was reduced by over 2-fold under hypoxia compared to normoxia. When exposures were conducted during 24 h windows, hypoxia reduced copper toxicity during early development and increased its toxicity in hatched larvae. To investigate the role of the hypoxia signaling pathway on the suppression of copper toxicity during early development, we stabilized the hypoxia inducible factor (HIF) pathway under normoxia using a prolyl-4-hydroxylase inhibitor, dimethyloxalylglycine (DMOG) and demonstrated that HIF activation results in a strong reduction in copper toxicity. We also established that the reduction in copper toxicity during early development was independent of copper uptake, while after hatching, copper uptake was increased under hypoxia, corresponding to an increase in copper toxicity. These findings change our understanding of the current and future impacts of worldwide oxygen depletion on fish communities challenged by anthropogenic toxicants.
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Donaldson L, Woodhead AJ, Wilson RJ, Maclean IM (2016). Subsistence use of papyrus is compatible with wetland bird conservation.
Biological Conservation,
201, 414-422.
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2015
Suggitt AJ, Jones RT, Caseldine CJ, Huntley B, Stewart JR, Brooks SJ, Brown E, Fletcher D, Gillingham PK, Larwood J, et al (2015). A meta-database of Holocene sediment cores for England.
Vegetation History and Archaeobotany,
24(6), 743-747.
Abstract:
A meta-database of Holocene sediment cores for England
© 2015, Springer-Verlag Berlin Heidelberg. Extracting sediment cores for palaeoecological and archaeological investigations has occurred extensively across England since the early 20th century. Surprisingly, there has been comparatively little collation of these valuable publications and potential sources of data; for example, a search on the European Pollen Database (1st Aug 2014 edition) found just 118 core sites for the whole of Great Britain. Here, using a combination of systematic meta-searching and knowledge of the unpublished (‘grey’) literature, we have assembled a meta-database of some 763 sediment cores for palaeoecological records, documented across 273 scientific studies. The majority of these ( > 90 %) were sediment cores upon which pollen analyses had been performed, but other types of evidence, such as plant macrofossil and faunal records were also identified. We are making this meta-database publicly available, in the hope that it will assist further investigations into Holocene vegetation history, palaeoecology, geoarchaeology and environmental change.
Abstract.
Suggitt AJ, Jones RT, Caseldine CJ, Huntley B, Stewart JR, Brooks SJ, Brown E, Fletcher D, Gillingham PK, Larwood J, et al (2015). A reply to ‘A meta-database of Holocene sediment cores for England: missing data’ (Tooley 2015). Vegetation History and Archaeobotany
Mosedale J, Wilson RJ, Maclean IMD (2015). Climate Change and Crop Exposure to Adverse Weather: Changes to Frost Risk and Grapevine Flowering Conditions.
PLOS ONE,
10(10).
Abstract:
Climate Change and Crop Exposure to Adverse Weather: Changes to Frost Risk and Grapevine Flowering Conditions
The cultivation of grapevines in the UK and many other cool climate regions is expected to benefit from the higher growing season temperatures predicted under future climate scenarios. Yet the effects of climate change on the risk of adverse weather conditions or events at key stages of crop development are not always captured by aggregated measures of seasonal or yearly climates, or by downscaling techniques that assume climate variability will remain unchanged under future scenarios. Using fine resolution projections of future climate scenarios for south-west England and grapevine phenology models we explore how risks to cool-climate vineyard harvests vary under future climate conditions. Results indicate that the risk of adverse conditions during flowering declines under all future climate scenarios. In contrast, the risk of late spring frosts increases under many future climate projections due to advancement in the timing of budbreak. Estimates of frost risk, however, were highly sensitive to the choice of phenology model, and future frost exposure declined when budbreak was calculated using models that included a winter chill requirement for dormancy break. The lack of robust phenological models is a major source of uncertainty concerning the impacts of future climate change on the development of cool-climate viticulture in historically marginal climatic regions.
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Nieto-Sanchez S, Gutierrez D, Wilson RJ (2015). Long-term change and spatial variation in butterfly communities over an elevation gradient: driven by climate, buffered by habitat.
Diversity and Distributions: a journal of conservation biogeographyAbstract:
Long-term change and spatial variation in butterfly communities over an elevation gradient: driven by climate, buffered by habitat.
(A) Abstract
(B) Aim
Efforts to adapt conservation to climate change are hampered by a scarcity of studies of community-level ecological responses. We examined temporal (40 years) and spatial (1700 m elevation gradient) variation in butterfly communities, aiming to test whether the composition of communities in terms of species’ thermal envelopes tracked regional warming, and whether local habitat influenced community responses to climate variation.
(B) Location
Sierra de Guadarrama (central Spain).
(B) Methods
Butterfly assemblages were sampled at sites between 550 m and 2250 m elevation, in 1967-1973 and 2006-2012. Changes in community composition over time and space were evaluated using the community temperature index, or CTI, which reflects for local assemblages the balance between species whose geographic ranges occupy regions of low versus high temperatures. We used multiple regressions and an information-theoretic approach to test: 1) whether relationships of CTI with elevation or temperature remained consistent after an estimated 1.78 °C regional warming; and 2) how spatial variation in CTI was related to air temperature and land cover.
(B) Results
CTI decreased consistently with increasing elevation, and increased after 40 years of warming, as communities were increasingly composed by species with warmer geographic ranges. Long-term CTI change represented a c. 160 m uphill shift in community thermal composition, whereas isotherms shifted 307 m upwards. In 2006-2012, CTI was influenced positively by temperature, and negatively by forest and meadow cover.
(B) Main Conclusions
Variation in community composition over space and time suggested a role of climate in structuring butterfly assemblages. Despite this, changing spatial patterns of community composition (CTI) did not appear to keep pace with climate change. In addition, lower values of CTI recorded for sites with greater forest and meadow/pasture cover suggested a role for local habitat in buffering the effects of climate change on community composition.
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Suggitt AJ, Wilson RJ, August TA, Fox R, Isaac NJB, Macgregor NA, Morecroft MD, Maclean IMD (2015). Microclimate affects landscape level persistence in the British Lepidoptera.
Journal of Insect Conservation,
19(2), 237-253.
Abstract:
Microclimate affects landscape level persistence in the British Lepidoptera
© 2014, Springer International Publishing Switzerland. Microclimate has been known to drive variation in the distribution and abundance of insects for some time. Until recently however, quantification of microclimatic effects has been limited by computing constraints and the availability of fine-scale biological data. Here, we tested fine-scale patterns of persistence/extinction in butterflies and moths against two computed indices of microclimate derived from Digital Elevation Models: a summer solar index, representing fine-scale variation in temperature, and a topographic wetness index, representing fine-scale variation in moisture availability. We found evidence of microclimate effects on persistence in each of four 20 × 20 km British landscapes selected for study (the Brecks, the Broads, Dartmoor, and Exmoor). Broadly, local extinctions occurred more frequently in areas with higher minimum or maximum solar radiation input, while responses to wetness varied with landscape context. This negative response. to solar radiation is consistent with a response to climatic warming, wherein grid squares with particularly high minimum or maximum insolation values provided an increasingly adverse microclimate as the climate warmed. The variable response to wetness in different landscapes may have reflected spatially variable trends in precipitation. We suggest that locations in the landscape featuring cooler minimum and/or maximum temperatures could act as refugia from climatic warming, and may therefore have a valuable role in adapting conservation to climatic change.
Abstract.
Maclean IMD, Hopkins JJ, Bennie J, Lawson CR, Wilson RJ (2015). Microclimates buffer the responses of plant communities to climate change.
Global Ecology and Biogeography,
24(11), 1340-1350.
Abstract:
Microclimates buffer the responses of plant communities to climate change
© 2015 John Wiley. &. Sons Ltd. Aim: Despite predictions of high extinction risk resulting from climate change, range expansions have been documented more frequently than range retractions, prompting suggestions that species can endure climatic changes by persisting in cool or damp microclimates. We test whether such 'microrefugia' exist. Location: the United Kingdom. Methods: We examine fine-scale changes in the plant communities of a coastal grassland over a 30-year period in which spring temperatures increased by 1.4°C. We look at whether changes in community composition and local colonizations and extinctions are related to microclimatic conditions. Results: Our findings suggest that while community reassembly was consistent with warming, changes were smaller on cooler, north-facing slopes. Closer inspection of the patterns of species turnover revealed that species with low temperature requirements were able to persist on cooler slopes, while those with high moisture requirements suffered similar decreases in occupancy across all microclimates. Main conclusions: Our results suggest that cooler slopes may act as microrefugia, buffering the effects on plant communities of increases in temperature by delaying extinctions of species with low temperature requirements.
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Wilson RJ, Bennie J, Lawson CR, Pearson D, Ortúzar-Ugarte G, Gutiérrez D (2015). Population turnover, habitat use and microclimate at the contracting range margin of a butterfly.
Journal of Insect Conservation,
19(2), 205-216.
Abstract:
Population turnover, habitat use and microclimate at the contracting range margin of a butterfly
© 2014, Springer International Publishing Switzerland. Climate change is expected to drive patterns of extinction and colonisation that are correlated with geographic gradients in the climate, such as latitude and elevation. However, local population dynamics also depend on the fine-scale effects of vegetation and topography on resource availability and microclimate. Understanding how this fine-scale variation influences population survival in the face of changing climatic favourability could provide clues for adapting conservation to climate change. Here, we document a long-term decline of the butterfly Parnassius apollo in the Sierra de Guadarrama mountain range in central Spain, and examine recent population turnover and habitat use by the species to make inferences about its ecology and conservation. A decline since the 1960s throughout the elevation range suggests a regional deterioration in favourability for the species. Since 2006, local habitat quality has been the main correlate of population persistence, with populations that persisted from 2006 to 2012 associated with high availability of larval host plants. At a finer resolution, the larval distribution in a network of suitable habitat in 2011 and 2012 was most closely related to bare ground cover. Thus, although slope, aspect and elevation lead to considerable variation in microhabitat temperatures during the perio d of P. apollo larval development, vegetation structure appears to have been the most critical factor for local habitat use and population persistence. The results show that site selection and management retain key roles in conservation despite the broad-scale effects of environmental change.
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Hodgson JA, Bennie JJ, Dale G, Longley N, Wilson RJ, Thomas CD (2015). Predicting microscale shifts in the distribution of the butterfly Plebejus argus at the northern edge of its range.
Ecography,
38(10), 998-1005.
Abstract:
Predicting microscale shifts in the distribution of the butterfly Plebejus argus at the northern edge of its range
© 2015 Nordic Society Oikos. Species are often observed to occur in restricted patches of particularly warm microclimate at their high latitude/altitude geographic range margin. In these areas, global warming is expected to cause small-scale expansion of the occupied area, but most previous studies of range expansion have used very coarse scale data. Using high resolution microclimate models together with detailed field surveys, we tested whether the butterfly Plebejus argus, occurring on limestone grassland in north Wales, was responding as might be expected due to climate change in the last 30-40 yr. The abundance of adult Plebejus argus at 100 m resolution in 2011 was strongly affected by elevation and near-ground temperatures in May. A statistical model including microclimate, fitted to 2011 data, was successful (67% correct) at hindcasting the occurrence of Plebejus argus in 1983 when the average May air temperature was 1.4°C cooler. However, the model was less accurate at hindcasting occurrences in 1972 (50% correct). Given the distribution of micro-sites in this landscape, we predict that further warming of approximately 1°C would make the majority of sites highly microclimatically suitable for this species. There are a growing number of long-term studies of range change, and investigations into the mechanisms driving them, but still surprisingly few that explicitly make and test predictions with independent data. Our tests are a valuable example of how accurate predictions of distribution change can be, but also of the inevitable uncertainties. Improved understanding of how well models predict will be very important to plan robust climate change adaptation measures.
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Gillingham PK, Bradbury RB, Roy DB, Anderson BJ, Baxter JM, Bourn NAD, Crick HQP, Findon RA, Fox R, Franco A, et al (2015). The effectiveness of protected areas in the conservation of species with changing geographical ranges.
Biological Journal of the Linnean Society,
115(3), 707-717.
Abstract:
The effectiveness of protected areas in the conservation of species with changing geographical ranges
© 2015 the Linnean Society of London. A cornerstone of conservation is the designation and management of protected areas (PAs): locations often under conservation management containing species of conservation concern, where some development and other detrimental influences are prevented or mitigated. However, the value of PAs for conserving biodiversity in the long term has been questioned given that species are changing their distributions in response to climatic change. There is a concern that PAs may become climatically unsuitable for those species that they were designated to protect, and may not be located appropriately to receive newly-colonizing species for which the climate is improving. In the present study, we analyze fine-scale distribution data from detailed resurveys of seven butterfly and 11 bird species in Great Britain aiming to examine any effect of PA designation in preventing extinctions and promoting colonizations. We found a positive effect of PA designation on species' persistence at trailing-edge warm range margins, although with a decreased magnitude at higher latitudes and altitudes. In addition, colonizations by range expanding species were more likely to occur on PAs even after altitude and latitude were taken into account. PAs will therefore remain an important strategy for conservation. The potential for PA management to mitigate the effects of climatic change for retracting species deserves further investigation.
Abstract.
Zografou K, Adamidis GC, Grill A, Kati V, Wilson RJ, Halley JM (2015). Who flies first? - habitat-specific phenological shifts of butterflies and orthopterans in the light of climate change: a case study from the south-east Mediterranean.
Ecological Entomology,
40(5), 562-574.
Abstract:
Who flies first? - habitat-specific phenological shifts of butterflies and orthopterans in the light of climate change: a case study from the south-east Mediterranean
© 2015 the Royal Entomological Society. 1. Insects undergo phenological change at different rates, showing no consistent trend between habitats, time periods, species or groups. Understanding how and why this variability occurs is crucial. 2. Phenological patterns of butterflies and Orthoptera were analysed using a novel approach of standardised major axis (SMA) analysis. It was investigated whether: (i) phenology (the mean date and duration of flight) of butterflies and Orthoptera changed from one survey (1998 and 1999 respectively) to another (2011), (ii) the rate at which phenology changed differed between taxa and (iii) phenological change was significantly different across habitat types (agriculture fields, grasslands, and forests). Using the 2011 dataset, we investigated relationships between habitat-specific variables and species phenology. 3. For both groups, late-emerging species had an advanced onset on the second survey while the duration showed no consistent trend for butterflies and did not change for Orthoptera. Although the rate at which phenology changed was consistent between the two groups, at the habitat level, a longer duration of flight period emerged for butterflies in agriculture fields while Orthoptera showed no differentiation in flight duration between habitats. We found an earlier emergence of butterflies in grasslands compared to forests, attributed to habitat-specific temperature, whereas spatial variation in humidity had a significantly lower effect on butterflies' phenology in grasslands compared to forests. A gradual delay of butterfly appearances as the canopy cover increased was also found. 4. The utility of SMA analysis was demonstrated in phenological studies and evidence was detected that both habitat type and habitat-specific variables refine species' phenological responses.
Abstract.
2014
Lawson CR, Bennie JJ, Thomas CD, Hodgson JA, Wilson RJ (2014). Active Management of Protected Areas Enhances Metapopulation Expansion Under Climate Change.
Conservation Letters,
7(2), 111-118.
Abstract:
Active Management of Protected Areas Enhances Metapopulation Expansion Under Climate Change
There is a need to adapt biodiversity conservation to climate change, but few empirical studies are available to guide decision-making. Existing networks of protected areas (PAs) have been preferentially colonized during species' range expansions, but this could be due to their original habitat quality and/or to ongoing management activity. Here, we examine how PA status and active conservation management have influenced the range expansion of a butterfly Hesperia comma through fragmented landscapes. PAs under active conservation management were over three times more likely to be colonized than unprotected, unmanaged sites of the same basic vegetation type. Conservation action also increased the survival rate of existing populations inside and outside of PAs. We conclude that PAs facilitate range expansions by preventing habitat degradation and encouraging active conservation that improves habitat quality, and that conservation interventions on nondesignated sites also have a role to play in adapting conservation to climate change. © 2013 the Authors. Conservation Letters published by Wiley Periodicals, Inc.
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Gutiérrez D, Wilson RJ (2014). Climate conditions and resource availability drive return elevational migrations in a single-brooded insect.
Oecologia,
175(3), 861-873.
Abstract:
Climate conditions and resource availability drive return elevational migrations in a single-brooded insect.
Seasonal elevational migrations have important implications for life-history evolution and ecological responses to environmental change. However, for most species, particularly invertebrates, evidence is still scarce for the existence of such migrations, as well as for the potential causes. We tested the extent to which seasonal abundance patterns in central Spain for overwintering (breeding) and summer (non-breeding) individuals of the butterfly Gonepteryx rhamni were consistent with three hypotheses explaining elevational migration: resource limitation (host plant and flower availability), physiological constraints of weather (maximum temperatures) and habitat limitation (forest cover for overwintering). For overwintering adults, abundance was positively associated with host plant density during two intensive survey seasons (2007-2008), and the elevational distribution was relatively stable over a 7-year period (2006-2012). The elevational distribution of summer adults was highly variable, apparently related both to temperature and habitat type. Sites occupied by adults in the summer were on average 3 °C cooler than their breeding sites, and abundance showed negative associations with summer temperature, and positive associations with forest cover and host plant density in 2007 and 2008. The results suggest that the extent of uphill migration in summer could be driven by different factors, depending on the year, and are mostly consistent with the physiological constraint and habitat limitation hypotheses. In contrast, the patterns for overwintering adults suggest that downhill migration can be explained by resource availability. Climate change could generate bottlenecks in the populations of elevational migrant species by constraining the area of specific seasonal habitat networks or by reducing the proximity of environments used at different times of year.
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Voskamp A, Rode EJ, Coudrat CNZ, Wirdateti, Abinawanto, Wilson RJ, Nekaris KAI (2014). Modelling the habitat use and distribution of the threatened Javan slow loris Nycticebus javanicus.
Endangered Species Research,
23(3), 277-286.
Abstract:
Modelling the habitat use and distribution of the threatened Javan slow loris Nycticebus javanicus
© Inter-Research 2014. The Javan slow loris Nycticebus javanicus is threatened by habitat decline and is classified as Critically Endangered on the IUCN Red List. Information on its distribution and habitat preferences is still lacking, and so far the distribution of the Javan slow loris has only been quantified via ecological niche modelling based on museum specimens and remotely derived environmental layers. We aimed to refine the modelled predictions and to verify the distribution of the Javan slow loris by collecting up-to-date occurrence data, which are fundamental for conservation and management of the species. Furthermore, we identify variables that predict its presence and give recommendations for future survey sites and conservation actions. From April to June 2012 we collected data on species presence, habitat preferences and levels of disturbance at priority sites throughout Java. We present a map of the predicted distribution of N. javanicus based on a maxi mum entropy model. We investigated habitat preferences using R (v. 2.14.1). During the study we sighted 52 lorises in 9 out of 14 investigated areas. The amount of bamboo in a forest had a positive effect on the encounter rates. Furthermore, we made 86% of sightings in forest plantations and agricultural areas located outside protected areas, with the majority located in areas with measured high levels of disturbance. We suggest that further ecological studies are needed to understand if and why densities may be higher in anthropogenically disturbed areas.
Abstract.
Wilson RJ, Bennie J, Lawson CR, Pearson D, Ortúzar-Ugarte G, Gutiérrez D (2014). Population turnover, habitat use and microclimate at the contracting range margin of a butterfly.
Journal of Insect ConservationAbstract:
Population turnover, habitat use and microclimate at the contracting range margin of a butterfly
Climate change is expected to drive patterns of extinction and colonisation that are correlated with geographic gradients in the climate, such as latitude and elevation. However, local population dynamics also depend on the fine-scale effects of vegetation and topography on resource availability and microclimate. Understanding how this fine-scale variation influences population survival in the face of changing climatic favourability could provide clues for adapting conservation to climate change. Here, we document a long-term decline of the butterfly Parnassius apollo in the Sierra de Guadarrama mountain range in central Spain, and examine recent population turnover and habitat use by the species to make inferences about its ecology and conservation. A decline since the 1960s throughout the elevation range suggests a regional deterioration in favourability for the species. Since 2006, local habitat quality has been the main correlate of population persistence, with populations that persisted from 2006 to 2012 associated with high availability of larval host plants. At a finer resolution, the larval distribution in a network of suitable habitat in 2011 and 2012 was most closely related to bare ground cover. Thus, although slope, aspect and elevation lead to considerable variation in microhabitat temperatures during the period of P. apollo larval development, vegetation structure appears to have been the most critical factor for local habitat use and population persistence. The results show that site selection and management retain key roles in conservation despite the broad-scale effects of environmental change.
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Lawson CR, Hodgson JA, Wilson RJ, Richards SA (2014). Prevalence, thresholds and the performance of presence-absence models.
Methods in Ecology and Evolution,
5(1), 54-64.
Abstract:
Prevalence, thresholds and the performance of presence-absence models
Summary: the use of species distribution models to understand and predict species' distributions necessitates tests of fit to empirical data. Numerous performance metrics have been proposed, many of which require continuous occurrence probabilities to be converted to binary 'present or absent' predictions using threshold transformations. It is widely accepted that both continuous and binary performance metrics should be independent of prevalence (the proportion of locations that are occupied). However, because these metrics have been mostly assessed on a case-specific basis, there are few general guidelines for measuring performance. Here, we develop a conceptual framework for classifying performance metrics, based on whether they are sensitive to prevalence, and whether they require binary predictions. We use this framework to investigate how these performance metric properties influence the predictions made by the models they select. A literature survey reveals that binary metrics are widely employed and that prevalence-independent metrics are used more frequently than prevalence-dependent metrics. However, we show that prevalence-dependent metrics are essential to assess the numerical accuracy of model predictions and are more useful in applications that require occupancy estimates. Furthermore, we demonstrate that in comparison with continuous metrics, binary metrics often select models that have reduced ability to separate presences from absences, make predictions which over- or underestimate occupancy and give misleading estimates of uncertainty. Importantly, models selected using binary metrics will often be of reduced practical use even when applied to ecological problems that require binary decision-making. We suggest that SDM performance should be assessed using prevalence-dependent performance metrics whenever the absolute values of occurrence predictions are important and that continuous metrics should be used instead of binary metrics whenever possible. We thus recommend the wider application of prevalence-dependent continuous metrics, particularly likelihood-based metrics such as Akaike's Information Criterion (AIC), to assess the performance of presence-absence models. © 2013 British Ecological Society.
Abstract.
Bennie J, Wilson RJ, Maclean IMD, Suggitt AJ (2014). Seeing the woods for the trees - when is microclimate important in species distribution models?.
Global Change Biology,
20(9), 2699-2700.
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Zografou K, Kati V, Grill A, Wilson RJ, Tzirkalli E, Pamperis LN, Halley JM (2014). Signals of climate change in butterfly communities in a Mediterranean protected area.
PLoS One,
9(1).
Abstract:
Signals of climate change in butterfly communities in a Mediterranean protected area.
The European protected-area network will cease to be efficient for biodiversity conservation, particularly in the Mediterranean region, if species are driven out of protected areas by climate warming. Yet, no empirical evidence of how climate change influences ecological communities in Mediterranean nature reserves really exists. Here, we examine long-term (1998-2011/2012) and short-term (2011-2012) changes in the butterfly fauna of Dadia National Park (Greece) by revisiting 21 and 18 transects in 2011 and 2012 respectively, that were initially surveyed in 1998. We evaluate the temperature trend for the study area for a 22-year-period (1990-2012) in which all three butterfly surveys are included. We also assess changes in community composition and species richness in butterfly communities using information on (a) species' elevational distributions in Greece and (b) Community Temperature Index (calculated from the average temperature of species' geographical ranges in Europe, weighted by species' abundance per transect and year). Despite the protected status of Dadia NP and the subsequent stability of land use regimes, we found a marked change in butterfly community composition over a 13 year period, concomitant with an increase of annual average temperature of 0.95°C. Our analysis gave no evidence of significant year-to-year (2011-2012) variability in butterfly community composition, suggesting that the community composition change we recorded is likely the consequence of long-term environmental change, such as climate warming. We observe an increased abundance of low-elevation species whereas species mainly occurring at higher elevations in the region declined. The Community Temperature Index was found to increase in all habitats except agricultural areas. If equivalent changes occur in other protected areas and taxonomic groups across Mediterranean Europe, new conservation options and approaches for increasing species' resilience may have to be devised.
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Lawson CR, Bennie J, Hodgson JA, Thomas CD, Wilson RJ (2014). Topographic microclimates drive microhabitat associations at the range margin of a butterfly.
Ecography,
37(8), 732-740.
Abstract:
Topographic microclimates drive microhabitat associations at the range margin of a butterfly
The habitat associations of individuals underpin the dynamics of species distributions. Broad-scale gradients in climate can alter habitat associations across species' geographic ranges, but topographic heterogeneity creates local microclimates which could generate variation in habitat use at finer spatial scales. We examined the selection of microhabitats for egg-laying by populations of a thermally-constrained butterfly, the skipper Hesperia comma, across 16 sites with different regional temperatures and topographic microclimates. Using models of thermal microclimate, we examined how the association between eggs and warm bare ground microhabitats varied with ambient temperature, and predicted bare ground associations in 287 existing H. comma populations, to investigate the relative impacts of regional temperatures and topographic microclimates on microhabitat use. Eggs were most strongly associated with bare ground in relatively cool sites, indicating climate-driven changes in microhabitat use. The majority of temperature variation between study sites was attributable to topographic microclimates rather than regional temperature differences, such that changes in microhabitat associations occurred principally between north- and south-facing slopes within the same region. Predicted microhabitat associations across the UK distribution of H. comma showed that, due to the large temperature differences generated by topography, most of the between-population variation in microhabitat use occurs locally within 5 km grid squares, with a smaller proportion occurring at a regional level between 5 km squares. Our findings show how microclimatic variation generated by topography alters the habitat associations of populations at fine spatial scales, suggesting that microclimate-driven changes in habitat suitability could shape species' distribution dynamics and their responses to environmental change. © 2014 the Authors. Ecography published by Nordic Society Oikos.
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2013
Gutiérrez D, Harcourt J, Díez SB, Gutiérrez Illán J, Wilson RJ (2013). Models of presence-absence estimate abundance as well as (or even better than) models of abundance: the case of the butterfly Parnassius apollo.
Landscape Ecology,
28(3), 401-413.
Abstract:
Models of presence-absence estimate abundance as well as (or even better than) models of abundance: the case of the butterfly Parnassius apollo
Models relating species distribution records to environmental variables are increasingly applied to biodiversity conservation. Such techniques could be valuable to predict the distribution, abundance or habitat requirements of species that are rare or otherwise difficult to survey. However, despite widely-documented positive intraspecific relationships between occupancy and abundance, few studies have demonstrated convincing associations between models of habitat suitability based on species occurrence, and observed measures of habitat quality such as abundance. Here we compared models based on field-derived abundance and distribution (presence-absence) data for a rare mountain butterfly in 2006-2008. Both model types selected consistent effects of environmental variables, which corresponded to known ecological associations of the species, suggesting that abundance and distribution may be a function of similar factors. However, the models based on occurrence data identified stronger effects of a smaller number of environmental variables, indicating less uncertainty in the factors controlling distribution. Furthermore, cross-validation of the models using observed abundance data from different years, or averaged across years, suggested a marginally stronger ability of models based on occurrence data to predict observed abundance. The results suggest that, for some species, distribution models could be efficient tools for estimating habitat quality in conservation planning or management, when information on abundance or habitat requirements is costly or impractical to obtain. © 2013 Springer Science+Business Media Dordrecht.
Abstract.
Bennie J, Hodgson JA, Lawson CR, Holloway CTR, Roy DB, Brereton T, Thomas CD, Wilson RJ (2013). Range expansion through fragmented landscapes under a variable climate.
Ecol Lett,
16(7), 921-929.
Abstract:
Range expansion through fragmented landscapes under a variable climate.
Ecological responses to climate change may depend on complex patterns of variability in weather and local microclimate that overlay global increases in mean temperature. Here, we show that high-resolution temporal and spatial variability in temperature drives the dynamics of range expansion for an exemplar species, the butterfly Hesperia comma. Using fine-resolution (5 m) models of vegetation surface microclimate, we estimate the thermal suitability of 906 habitat patches at the species' range margin for 27 years. Population and metapopulation models that incorporate this dynamic microclimate surface improve predictions of observed annual changes to population density and patch occupancy dynamics during the species' range expansion from 1982 to 2009. Our findings reveal how fine-scale, short-term environmental variability drives rates and patterns of range expansion through spatially localised, intermittent episodes of expansion and contraction. Incorporating dynamic microclimates can thus improve models of species range shifts at spatial and temporal scales relevant to conservation interventions.
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2012
Maclean IMD, Bennie JJ, Scott AJ, Wilson RJ (2012). A high-resolution model of soil and surface water conditions.
Ecological Modelling,
237-238, 109-119.
Abstract:
A high-resolution model of soil and surface water conditions
Soil moisture and surface water conditions are key determinants of plant community composition and ecosystem function, and predicting such conditions is an important step in understanding the ecological consequences of environmental change. Typically, hydrological models that use real landscape features do not simulate water conditions at the fine spatial and temporal scales that are meaningful to many plant species and ecological processes. We present a hydrological model that simulates daily soil moisture and surface water conditions at a spatial resolution of 1m×1m. The model is applied to 16km 2 of the Lizard Peninsula, UK. The model is kept computationally efficient by combining a simple lumped parameter basin approach with the distributed hydrological effects of basin topography. We also model the complex flows occurring between small basins. Code for running the model using R statistical software is provided as supplementary material. As inputs, the model uses widely available daily weather variables, 1m×1m resolution digital elevation data (LiDAR) and some simple vegetation and soil characteristics identifiable from aerial photographs. Our results indicate that when inter-basin water exchanges and the distributed effects of topography within each basin are not accounted for, the model performs less well than just assuming average conditions in time or space. However, modelling inter-basin water flow also substantially increases computer run-time. The full model is capable of correctly simulating a broad range of hydrological and soil moisture conditions, providing accurate predictions for areas that range from permanently wet through to permanently dry, as well as for ephemeral wetlands with highly variable water levels. We discuss some potential ecological applications of the model, for example in guiding conservation management. © 2012 Elsevier B.V.
Abstract.
Illán JG, Gutiérrez D, Díez SB, Wilson RJ (2012). Elevational trends in butterfly phenology: Implications for species responses to climate change.
Ecological Entomology,
37(2), 134-144.
Abstract:
Elevational trends in butterfly phenology: Implications for species responses to climate change
Impacts of global change on the distribution, abundance, and phenology of species have been widely documented. In particular, recent climate change has led to widespread changes in animal and plant seasonality, leading to debate about its potential to cause phenological mismatches among interacting taxa. In mountainous regions, populations of many species show pronounced phenological gradients over short geographic distances, presenting the opportunity to test for effects of climate on phenology, independent of variation in confounding fac tors such as photoperiod. Here we show for 32 butterfly species sampled for five years over a 1700 m gradient (560-2260 m) in a Mediterranean mountain range that, on average, annual flight period is delayed with elevation by 15-22 days per kilometre. Species mainly occurring at low elevations in the region, and to some extent those flying earlier in the year, showed phenological delays of 23-36 days per kilometre, whereas the flight periods of species that occupy high elevations, or fly in late summer, were consistently more synchronised over the elevation gradient. Elevational patterns in phenology appear to reflect a narrowing phenological window of opportunity for larval and adult butterfly activity of high elevation and late-flying species. Here, we speculate as to the causes of these patterns, and the consequences for our ability to predict species responses to climate change. Our results raise questions about the use of space-time substitutions in predicting phenological responses to climate change, since traits relating to flight period and environmental associations may influence the capacity of species to adapt to changing climates. © 2012 the Authors. Ecological Entomology © 2012 the Royal Entomological Society.
Abstract.
Lawson CR, Bennie JJ, Thomas CD, Hodgson JA, Wilson RJ (2012). Local and landscape management of an expanding range margin under climate change.
Journal of Applied Ecology,
49(3), 552-561.
Abstract:
Local and landscape management of an expanding range margin under climate change
1.There is a pressing need to understand how to facilitate species' range shifts under climate change. However, few empirical studies are available to inform decision-making, particularly at fine spatial and temporal resolutions. 2.We present a case study of a thermally constrained habitat specialist, the silver-spotted skipper butterfly Hesperia comma, at its expanding range margin in south-eastern Britain. Using data from 724 habitat patches over a 9-year interval (2000-2009), we examined local and landscape determinants of colonization, survival and population density. We then predicted probabilities of colonization and survival for habitat patches under the observed 1982 and 2009 distributions to investigate how the factors limiting range expansions change through space and time. 3.Between 2000 and 2009, Hesperia comma continued to expand its range in Britain, but the 67 recorded colonization events were offset by 48 local extinctions. Extinctions were strongly linked to climate, occurring predominantly in cooler regions and on shaded north-facing slopes. 4.Population density and probability of survival were closely related to conditions within a site, whereas probability of colonization was largely determined by functional connectivity. Survival probability was also influenced by connectivity, suggesting that immigration helped to support extinction-prone populations (a 'rescue effect'). 5.Patch occupancy beyond the range margin was primarily constrained by colonization, but close to the expanding front, population survival became the key limiting factor. This pattern was conserved during range expansion, altering management priorities at individual sites. 6.Synthesis and applications. Previous studies on facilitating range shifts have stressed the need to increase landscape-scale connectivity to remove constraints on colonization, and our data substantiate this advice. However, we show that enhancing population survival can also help to facilitate range expansions, because populations at leading range edges face high extinction risk. Population survival can be improved directly through local management actions, such as enlarging patch size and increasing habitat quality, or indirectly by improving connectivity. Thus, local management can secure vulnerable populations at the range edge and provide larger and more stable migrant sources for future expansion and deserves consideration when facilitating range shifts under climate change. © 2012 the Authors. Journal of Applied Ecology © 2012 British Ecological Society.
Abstract.
Thomas CD, Gillingham PK, Bradbury RB, Roy DB, Anderson BJ, Baxter JM, Bourne NAD, Crick HQP, Findon RA, Fox R, et al (2012). Protected areas facilitate species' range expansions.
Proceedings of the National Academy of Sciences of the United States of America,
109(35), 14063-14068.
Abstract:
Protected areas facilitate species' range expansions
The benefits of protected areas (PAs) for biodiversity have been questioned in the context of climate change because PAs are static, whereas the distributions of species are dynamic. Current PAs may, however, continue to be important if they provide suitable locations for species to colonize at their leading-edge range boundaries, thereby enabling spread into new regions. Here, we present an empirical assessment of the role of PAs as targets for colonization during recent range expansions. Records from intensive surveys revealed that seven bird and butterfly species have colonized PAs 4.2 (median) times more frequently than expected from the availability of PAs in the landscapes colonized. Records of an additional 256 invertebrate species with less-intensive surveys supported these findings and showed that 98% of species are disproportionately associated with PAs in newly colonized parts of their ranges. Although colonizing species favor PAs in general, species vary greatly in their reliance on PAs, reflecting differences in the dependence of individual species on particular habitats and other conditions that are available only in PAs. These findings highlight the importance of current PAs for facilitating range expansions and show that a small subset of the landscape receives a high proportion of colonizations by range-expanding species.
Abstract.
2011
Wilson RJ, Roy DB (2011). Butterflies reset the calendar. Nature Climate Change, 1(2), 101-102.
Wilson RJ, Gutierrez D (2011). Effects of Climate Change on the Elevational Limits of Species Ranges. In Beever EA, Belant JL (Eds.) Ecological Consequences of Climate Change: Mechanisms, Conservation, and Management, CRC Press, Taylor & Francis Group.
Maclean IMD, Wilson RJ, Hassall M (2011). Predicting changes in the abundance of African wetland birds by incorporating abundance-occupancy relationships into habitat association models. Diversity and Distributions, 17, 480-490.
Maclean IMD, Wilson RJ (2011). Recent ecological responses to climate change support predictions of high extinction risk. Proceedings of the National Academy of Sciences, 108, 12337-12342.
Wilson RJ, Maclean IMD (2011). Recent evidence for the climate change threat to Lepidoptera and other insects. Journal of Insect Conservation, 15(1-2), 259-268.
2010
Illán JG, Gutiérrez D, Wilson RJ (2010). Fine-scale determinants of butterfly species richness and composition in a mountain region.
Journal of Biogeography,
37(9), 1706-1720.
Abstract:
Fine-scale determinants of butterfly species richness and composition in a mountain region
Aim: Global patterns of species richness are often considered to depend primarily on climate. We aimed to determine how topography and land cover affect species richness and composition at finer scales. Location: Sierra de Guadarrama (central Iberian Peninsula). Methods: We sampled the butterfly fauna of 180 locations (89 in 2004, 91 in 2005) at 600-2300 m elevation in a region of 10800 km 2. We recorded environmental variables at 100-m resolution using GIS, and derived generalized linear models for species density (number of species per unit area) and expected richness (number of species standardized to number of individua ls) based on variables of topoclimate (elevation and insolation) or land cover (vegetation type, geology and hydrology), or both (combined). We evaluated the models against independent data from the alternative study year. We also tested for differences in species composition among sites and years using constrained ordination (canonical correspondence analysis), and used variation partitioning analyses to quantify the independent and combined roles of topoclimate and land cover. Results: Topoclimatic, land cover and combined models were significantly related to observed species density and expected richness. Topoclimatic and combined models outperformed models based on land cover variables, showing a humped elevational diversity gradient. Both topoclimate and land cover made significant contributions to models of species composition. Main conclusions: Topoclimatic factors may dominate species richness patterns in regions with pronounced elevational gradients, as long as large areas of natural habitat remain. In contrast, both topoclimate and land cover may have important effects on species composition. Biodiversity conservation in mountainous regions therefore requires protection and management of natural habitats over a wide range of topoclimatic conditions, which may assist in facilitating range shifts and alleviating declines in species richness related to climate change. © 2010 Blackwell Publishing Ltd.
Abstract.
Wilson RJ, Davies ZG, Thomas CD (2010). Linking habitat use to range expansion rates in fragmented landscapes: a metapopulation approach. Ecography, 33, 73-82.
Illán JG, Gutiérrez D, Wilson RJ (2010). The contributions of topoclimate and land cover to species distributions and abundance: Fine-resolution tests for a mountain butterfly fauna.
Global Ecology and Biogeography,
19(2), 159-173.
Abstract:
The contributions of topoclimate and land cover to species distributions and abundance: Fine-resolution tests for a mountain butterfly fauna
Aim: Models relating species distributions to climate or habitat are widely used to predict the effects of global change on biodiversity. Most such approaches assume that climate governs coarse-scale species ranges, whereas habitat limits fine-scale distributions. We tested the influence of topoclimate and land cover on butterfly distributions and abundance in a mountain range, where climate may vary as markedly at a fine scale as land cover. Location: Sierra de Guadarrama (Spain, southern Europe). Methods: We sampled the butterfly fauna of 180 locations (89 in 2004, 91 in 2005) in a 10,800 km 2. region, and derived generalized linear models (GLMs) for species occurrence and abundance based on topoclimatic (elevation and insolation) or habitat (land cover, geology and hydrology) variables sampled at 100-m resolution using GIS. Models for each year were tested against independent data from the alternate year, using the area under the receiver operating characteristic curve (AUC) (distribution) or Spearman's rank correlation coefficient (r s ) (abundance). Results: in independent model tests, 74% of occurrence models achieved AUCs of. >. 0.7, and 85% of abundance models were significantly related to observed abundance. Topoclimatic models outperformed models based purely on land cover in 72% of occurrence models and 66% of abundance models. Including both types of variables often explained most variation in model calibration, but did not significantly improve model cross-validation relative to topoclimatic models. Hierarchical partitioning analysis confirmed the overriding effect of topoclimatic factors on species distributions, with the exception of several species for which the importance of land cover was confirmed. Main conclusions: Topoclimatic factors may dominate fine-resolution species distributions in mountain ranges where climate conditions vary markedly over short distances and large areas of natural habitat remain. Climate change is likely to be a key driver of species distributions in such systems and could have important effects on biodiversity. However, continued habitat protection may be vital to facilitate range shifts in resp onse to climate change. © 2010 Blackwell Publishing Ltd.
Abstract.
2009
Wilson RJ, Roy DB (2009). Butterfly population structure and dynamics. In Settele J, Shreeve T, Konvicka M, Dyck HV (Eds.) Ecology of Butterflies in Europe, Cambridge: Cambridge University Press, 81-96.
Ashton S, Gutierrez D, Wilson RJ (2009). Effects of temperature and elevation on habitat use by a rare mountain butterfly: implications for species responses to climate change. ECOL ENTOMOL
Wilson RJ, Davies ZG, Thomas CD (2009). Modelling the effect of habitat fragmentation on range expansion in a butterfly. P ROY SOC LOND B BIO
2008
Merrill RM, Gutiérrez, D. Lewis, O.T. Gutiérrez, J. Diez SB, Wilson RJ (2008). Combined effects of climate and biotic interactions on the elevational range of a phytophagous insect. Journal of Animal Ecology, 77, 145-155.
Thomas CD, Bulman CR, Wilson RJ (2008). Where within a geographical range do species survive best? a matter of scale. Insect Conservation & Diversity, 1, 2-8.
2007
Wilson RJ, Gutiérrez, D. Gutiérrez, J. Monserrat, V.J. (2007). An elevational shift in butterfly species richness and composition accompanying recent climate change. Global Change Biology, 13, 1873-1887.
Wilson RJ, Davies ZG, Thomas CD (2007). Insects and climate change: processes, patterns and implications for conservation. In Stewart AJA, New TR, Lewis OT (Eds.) Insect Conservation Biology. Proceedings of the Royal Entomological Society's 22nd Symposium, CABI Publishing, 245-279.
Dormann CF, McPherson JM, Araujo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, et al (2007). Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. ECOGRAPHY, 30, 609-628.
Bulman CR, Wilson RJ, Holt AR, Early RI, Galvez Bravo L, Warren MS, Thomas CD (2007). Minimum viable metapopulation size, extinction debt and the conservation of a declining species.
ECOL APPL,
17, 1460-1473.
Abstract:
Minimum viable metapopulation size, extinction debt and the conservation of a declining species.
A key question facing conservation biologists is whether declines in species' distributions are keeping pace with landscape change, or whether current distributions overestimate probabilities of future persistence. We use metapopulations of the marsh fritillary butterfly Euphydryas aurinia in the United Kingdom as a model system to test for extinction debt in a declining species. We derive parameters for a metapopulation model (incidence function model, IFM) using information from a 625-km2 landscape where habitat patch occupancy, colonization, and extinction rates for E. aurinia depend on patch connectivity, area, and quality. We then show that habitat networks in six extant metapopulations in 16-km2 squares were larger, had longer modeled persistence times (using IFM), and higher metapopulation capacity (λM) than six extinct metapopulations. However, there was a >99% chance that one or more of the six extant metapopulations would go extinct in 100 years in the absence of further habitat loss. For 11 out of 12 networks, minimum areas of habitat needed for 95% persistence of metapopulation simulations after 100 years ranged from 80 to 142 ha (∼5–9% of land area), depending on the spatial location of habitat. The area of habitat exceeded the estimated minimum viable metapopulation size (MVM) in only two of the six extant metapopulations, and even then by only 20%. The remaining four extant networks were expected to suffer extinction in 15–126 years. MVM was consistently estimated as ∼5% of land area based on a sensitivity analysis of IFM parameters and was reduced only marginally (to ∼4%) by modeling the potential impact of long-distance colonization over wider landscapes. The results suggest a widespread extinction debt among extant metapopulations of a declining species, necessitating conservation management or reserve designation even in apparent strongholds. For threatened species, metapopulation modeling is a potential means to identify landscapes near to extinction thresholds, to which conservation measures can be targeted for the best chance of success.
Abstract.
2006
Davies ZG, Wilson, R.J. Coles, S. Thomas, C.D. (2006). Changing habitat associations of a thermally constrained species, the silver-spotted skipper butterfly, in response to climate warming. Journal of Animal Ecology, 75, 247-256.
2005
Wilson RJ, Gutierrez D, Gutierrez J, Martinez D, Agudo R, Monserrat VJ (2005). Changes to the elevational limits and extent of species ranges associated with climate change. ECOL LETT, 8(11), 1138-1146.
Burke S, Pullin AS, Wilson RJ, Thomas CD (2005). Selection for discontinuous life-history traits along a continuous thermal gradient in the butterfly Aricia agestis. ECOL ENTOMOL, 30, 613-619.
Davies ZG, Wilson, R.J. Brereton, T.M. Thomas, C.D. (2005). The re-expansion and improving status of the silver-spotted skipper butterfly (Hesperia comma) in Britain: a metapopulation success story. Biological Conservation, 124, 189-198.
2004
Cabeza M, Araújo MB, Wilson RJ, Thomas CD, Cowley MJR, Moilanen A (2004). Combining probabilities of occurrence with spatial reserve design.
Journal of Applied Ecology,
41(2), 252-262.
Abstract:
Combining probabilities of occurrence with spatial reserve design
1. There is a great concern about the loss of biodiversity that calls for more nature protection. Unfortunately, the funding available for conservation is limited, and often a compromise is needed between nature protection and economic interests. Reserve selection algorithms are optimization techniques that concentrate on identifying a set of reserves that represents biodiversity efficiently. Simple approaches to reserve selection use presence-absence data assuming that if a species occurs in a selected reserve, it will persist there indefinitely. 2. A refinement of this technique is the selection of reserves according to the local probabilities of occurrence of the given species. These can be estimated from habitat models fitted by empirical modelling techniques. However, local probabilities of occurrence are not static, and are influenced by the changing threats to biodiversity in and around the reserves. 3. The effects of landscape change can be minimized when compact reserves are favoured. Compact reserves that represent all species with a given target probability of occurrence can be achieved by combining the probability approach with spatial reserve design. 4. In this study we brought together two reserve selection approaches that implicitly deal with biodiversity persistence, by combining habitat models and spatial reserve design in a single algorithm. We applied the combined algorithm to a data set of 26 species of butterflies from north Wales. 5. For the particular case study addressed in this paper, clustered reserve networks could be identified at no or a small increase in cost. 6. A new, backwards, heuristic algorithm performed better and more consistently than the regular forwards heuristic approach. 7. Synthesis and applications. The reserve selection approach presented considers habitat quality (via probabilities of occurrence) and the spatial configuration of the reserves during the selection process. Emphasis on reserve networks that include high-quality sites in an aggregated manner increases the potential for long-term persistence of species in the reserve network.
Abstract.
RJWilson, Fox R, Roy DB, Thomas CD (2004). Spatial patterns in species distributions reveal biodiversity change. Nature, 432(7015), 393-396.
2002
Wilson RJ, Thomas CD (2002). Dispersal and the spatial dynamics of butterfly populations. In Bullock J, Kenward R, Hails R (Eds.) Dispersal Ecology, Blackwell Scientific Publishers, 257-278.
Taneyhill DE, Mallet JB, Wynne IR, Burke S, Pullin AS, Wilson RJ, Butlin RK, Hatcher MJ, Shorrocks B, Thomas CD, et al (2002). Estimating gene flow in endemic butterfly races: the effect of metapopulation dynamics. In Hails RS, Beringer JE, Godfray HCJ (Eds.) Genes in the Environment, Blackwell Scientific Publishers, 3-25.
RJWilson, Baker JS, Ellis S, Lineham ME (2002). Large-scale patterns of distribution and persistence at the range margins of a butterfly. Ecology, 83(12), 3357-3368.
Thomas CD, Wilson RJ, Lewis OT (2002). Short-term studies underestimate 30-generation changes in a butterfly metapopulation.
Proc Biol Sci,
269(1491), 563-569.
Abstract:
Short-term studies underestimate 30-generation changes in a butterfly metapopulation.
Most studies of rare and endangered species are based on work carried out within one generation, or over one to a few generations of the study organism. We report the results of a study that spans 30 generations (years) of the entire natural range of a butterfly race that is endemic to 35 km(2) of north Wales, UK. Short-term studies (surveys in single years and dynamics over 4 years) of this system led to the prediction that the regional distribution would be quite stable, and that colonization and extinction dynamics would be relatively unimportant. However, a longer-term study revealed unexpectedly high levels of population turnover (local extinction and colonization), affecting 18 out of the 20 patches that were occupied at any time during the period. Modelling the system (using the 'incidence function model' (IFM) for metapopulations) also showed higher levels of colonization and extinction with increasing duration of the study. The longer-term dynamics observed in this system can be compared, at a metapopulation level, with the increased levels of variation observed with increasing time that have been observed in single populations. Long-term changes may arise from local changes in the environment that make individual patches more or less suitable for the butterfly, or from unusual colonization or extinction events that take metapopulations into alternative states. One implication is that metapopulation and population viability analyses based on studies that cover only a few animal or plant generations may underestimate extinction threats.
Abstract.
Author URL.
2001
Cowley MJR, Thomas CD, Roy DB, Wilson RJ, León-Cortés JL, Gutiérrez D, Bulman CR, Quinn RM, Moss D, Gaston KJ (2001). Density-distribution relationships in British butterflies I: the effect of mobility and spatial scale. Journal of Animal Ecology, 70, 410-425.
Cowley MJR, Thomas CD, Wilson RJ, Leon-Cortes JL, Gutierrez D, Bulman CR (2001). Density-distribution relationships in British butterflies. II. An assessment of mechanisms. JOURNAL OF ANIMAL ECOLOGY, 70(3), 426-441.
Thomas CD, Bodsworth EJ, Simmons AD, RJWilson (2001). Ecological and evolutionary processes at expanding range margins. Nature, 411(6837), 577-581.
Gutiérrez D, León-Cortés JL, Menendez R, Wilson RJ, Cowley MJR, Thomas CD (2001). Metapopulations of four lepidpteran herbivores on a single host plant Lotus corniculatus. Ecology, 82, 1371-1386.
2000
Cowley MJR, Wilson RJ, León-Cortés JL, Gutiérrez D, Bulman CR, Thomas CD (2000). Habitat-based statistical models for predicting the spatial distribution of butterflies and day-flying moths in a fragmented landscape. Journal of Applied Ecology, 37, 60-72.
1998
Lewis OT, Wilson RJ, Harper MC (1998). Endemic butterflies on Grande Comore: habitat preferences and conservation priorities. Biological Conservation, 85, 113-121.
