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  1. Senior RA, Hill JK, Benedick S, Edwards DP
    Glob Chang Biol, 2018 03;24(3):1267-1278.
    PMID: 29052295 DOI: 10.1111/gcb.13914
    Tropical rainforests are subject to extensive degradation by commercial selective logging. Despite pervasive changes to forest structure, selectively logged forests represent vital refugia for global biodiversity. The ability of these forests to buffer temperature-sensitive species from climate warming will be an important determinant of their future conservation value, although this topic remains largely unexplored. Thermal buffering potential is broadly determined by: (i) the difference between the "macroclimate" (climate at a local scale, m to ha) and the "microclimate" (climate at a fine-scale, mm to m, that is distinct from the macroclimate); (ii) thermal stability of microclimates (e.g. variation in daily temperatures); and (iii) the availability of microclimates to organisms. We compared these metrics in undisturbed primary forest and intensively logged forest on Borneo, using thermal images to capture cool microclimates on the surface of the forest floor, and information from dataloggers placed inside deadwood, tree holes and leaf litter. Although major differences in forest structure remained 9-12 years after repeated selective logging, we found that logging activity had very little effect on thermal buffering, in terms of macroclimate and microclimate temperatures, and the overall availability of microclimates. For 1°C warming in the macroclimate, temperature inside deadwood, tree holes and leaf litter warmed slightly more in primary forest than in logged forest, but the effect amounted to <0.1°C difference between forest types. We therefore conclude that selectively logged forests are similar to primary forests in their potential for thermal buffering, and subsequent ability to retain temperature-sensitive species under climate change. Selectively logged forests can play a crucial role in the long-term maintenance of global biodiversity.
  2. Edwards DP, Woodcock P, Edwards FA, Larsen TH, Hsu WW, Benedick S, et al.
    Ecol Appl, 2012 Mar;22(2):561-71.
    PMID: 22611854 DOI: 10.1890/11-1362.1
    A key driver of rain forest degradation is rampant commercial logging. Reduced-impact logging (RIL) techniques dramatically reduce residual damage to vegetation and soils, and they enhance the long-term economic viability of timber operations when compared to conventionally managed logging enterprises. Consequently, the application of RIL is increasing across the tropics, yet our knowledge of the potential for RIL also to reduce the negative impacts of logging on biodiversity is minimal. We compare the impacts of RIL on birds, leaf-litter ants, and dung beetles during a second logging rotation in Sabah, Borneo, with the impacts of conventional logging (CL) as well as with primary (unlogged) forest. Our study took place 1-8 years after the cessation of logging. The species richness and composition of RIL vs. CL forests were very similar for each taxonomic group. Both RIL and CL differed significantly from unlogged forests in terms of bird and ant species composition (although both retained a large number of the species found in unlogged forests), whereas the composition of dung beetle communities did not differ significantly among forest types. Our results show little difference in biodiversity between RIL and CL over the short-term. However, biodiversity benefits from RIL may accrue over longer time periods after the cessation of logging. We highlight a severe lack of studies investigating this possibility. Moreover, if RIL increases the economic value of selectively logged forests (e.g., via REDD+, a United Nations program: Reducing Emissions from Deforestation and Forest Degradation in Developing Countries), it could help prevent them from being converted to agricultural plantations, which results in a tremendous loss of biodiversity.
  3. Magrach A, Senior RA, Rogers A, Nurdin D, Benedick S, Laurance WF, et al.
    Proc Biol Sci, 2016 Mar 16;283(1826):20153008.
    PMID: 26936241 DOI: 10.1098/rspb.2015.3008
    Selective logging is one of the major drivers of tropical forest degradation, causing important shifts in species composition. Whether such changes modify interactions between species and the networks in which they are embedded remain fundamental questions to assess the 'health' and ecosystem functionality of logged forests. We focus on interactions between lianas and their tree hosts within primary and selectively logged forests in the biodiversity hotspot of Malaysian Borneo. We found that lianas were more abundant, had higher species richness, and different species compositions in logged than in primary forests. Logged forests showed heavier liana loads disparately affecting slow-growing tree species, which could exacerbate the loss of timber value and carbon storage already associated with logging. Moreover, simulation scenarios of host tree local species loss indicated that logging might decrease the robustness of liana-tree interaction networks if heavily infested trees (i.e. the most connected ones) were more likely to disappear. This effect is partially mitigated in the short term by the colonization of host trees by a greater diversity of liana species within logged forests, yet this might not compensate for the loss of preferred tree hosts in the long term. As a consequence, species interaction networks may show a lagged response to disturbance, which may trigger sudden collapses in species richness and ecosystem function in response to additional disturbances, representing a new type of 'extinction debt'.
  4. Messina S, Edwards DP, AbdElgawad H, Beemster GTS, Tomassi S, Benedick S, et al.
    J Anim Ecol, 2020 10;89(10):2222-2234.
    PMID: 32535926 DOI: 10.1111/1365-2656.13280
    Selective logging is the dominant form of human disturbance in tropical forests, driving changes in the abundance of vertebrate and invertebrate populations relative to undisturbed old-growth forests. A key unresolved question is understanding which physiological mechanisms underlie different responses of species and functional groups to selective logging. Regulation of oxidative status is thought to be one major physiological mechanism underlying the capability of species to cope with environmental changes. Using a correlational cross-sectional approach, we compared a number of oxidative status markers among 15 understorey bird species in unlogged and selectively logged forest in Borneo in relation to their feeding guild. We then tested how variation of markers between forest types was associated with that in population abundance. Birds living in logged forests had a higher activity of the antioxidant enzyme superoxide dismutase and a different regulation of the glutathione cycle compared to conspecific birds in unlogged forest. However, neither oxidative damage nor oxidized glutathione differed between forest types. We also found that omnivores and insectivores differed significantly in all markers related to the key cellular antioxidant glutathione irrespective of the forest type. Species with higher levels of certain antioxidant markers in a given type of forest were less abundant in that forest type compared to the other. Our results suggest that there was little long-term effect of logging (last logging rotation occurred ~15 years prior to the study) on the oxidative status of understorey bird species. However, it is unclear if this was owing to plasticity or evolutionary change. Our correlative results also point to a potential negative association between some antioxidants and population abundance irrespective of the forest type.
  5. Brant HL, Ewers RM, Vythilingam I, Drakeley C, Benedick S, Mumford JD
    Malar J, 2016 07 19;15(1):370.
    PMID: 27430261 DOI: 10.1186/s12936-016-1416-1
    BACKGROUND: Malaria cases caused by Plasmodium knowlesi, a simian parasite naturally found in long-tailed and pig-tailed macaques, are increasing rapidly in Sabah, Malaysia. One hypothesis is that this increase is associated with changes in land use. A study was carried out to identify the anopheline vectors present in different forest types and to observe the human landing behaviour of mosquitoes.

    METHODS: Mosquito collections were carried out using human landing catches at ground and canopy levels in the Tawau Division of Sabah. Collections were conducted along an anthropogenic disturbance gradient (primary forest, lightly logged virgin jungle reserve and salvage logged forest) between 18:00 and 22:00 h.

    RESULTS: Anopheles balabacensis, a vector of P. knowlesi, was the predominant species in all collection areas, accounting for 70 % of the total catch, with a peak landing time of 18:30-20:00 h. Anopheles balabacensis had a preference for landing on humans at ground level compared to the canopy (p 

  6. Messina S, Edwards DP, Van Houtte N, Tomassi S, Benedick S, Eens M, et al.
    Int J Parasitol, 2022 Jan;52(1):87-96.
    PMID: 34450133 DOI: 10.1016/j.ijpara.2021.07.003
    Tropical forest degradation affects host-parasite interactions, determining the probability of animals acquiring an infection. The activation of an immune response to fight off infections requires energy and other resources such as antioxidants which may be redirected from growth and reproduction. A key question is how selective logging-the most common form of tropical forest degradation-impacts the prevalence of avian haemosporidian infection and its correlated physiological responses (nutritional and oxidative status markers). We investigated the prevalence of Plasmodium, Haemoproteus, and Leucocytozoon parasites in 14 understorey bird species in lowland, logged and unlogged, old-growth forests of Borneo. Prevalences of infections were similar between selectively logged and unlogged forests. To explore nutritional and oxidative status effects of haemosporidian infections, we examined associations between infections and plasma proteins, plasma triglycerides, and multiple blood-based markers of oxidative status, testing for an impact of selective logging on those markers. Birds infected with Plasmodium showed higher levels of plasma proteins and non-enzymatic antioxidant capacity, and lower levels of plasma triglycerides and glutathione, compared with haemosporidian-free individuals. Conversely, birds infected with Haemoproteus showed no changes in nutritional or physiological markers compared with uninfected individuals. These results indicate higher metabolic and physiological costs of controlling Plasmodium infection, compared with Haemoproteus, possibly due to higher pathogenicity of Plasmodium. Selectively logged forests had no effect on the responses of birds to infection, suggesting that the environmental conditions of degraded forests do not appear to induce any appreciable physiological demands in parasitised birds.
  7. Robin Lim AH, Sam LM, Gobilik J, Ador K, Choon JLN, Majampan J, et al.
    Trop Life Sci Res, 2022 Sep;33(3):61-83.
    PMID: 36545058 DOI: 10.21315/tlsr2022.33.3.5
    The chemical properties of honey depend on the source of collection to packaging, but little is known about honey in Sabah. The aim of this study was to distinguish between the physicochemical properties and mineral content of 76 honey samples from local sources and supermarkets in Sabah, which were from contract beekeepers, unknown sources and branded honey. Raw honey was collected from contract beekeepers, while honey from unknown source was obtained from street vendors and wet markets, while branded honey was purchased from local supermarkets. The chemical parameters of the honey were assessed using established methods, while the mineral content of the honey was determined using inductively coupled plasma optical emission spectroscopy (ICP-OES). Significant differences were found in several parameters measured in honey from different sources, with principal component analysis (PCA) showing clear separation between the measured parameters, yielding five factors that accounted for up to 72.25% of the total explained variance. Honey from contract beekeepers showed significant differences and higher mineral content (Ca, Cu, Fe, K, Mg, Na and Zn) compared to honey from unknown source and branded honey. Potassium was the most important element in the study with an average of 2.65 g/kg and 629.4 mg/kg for sources from contract beekeepers and branded honey, respectively. The honey from the contract beekeepers was of better quality due to its high mineral content. The results suggest that honey from contract beekeepers could be a good choice when it comes to high mineral content.
  8. Garg KM, Chattopadhyay B, Cros E, Tomassi S, Benedick S, Edwards DP, et al.
    Mol Biol Evol, 2022 Jan 07;39(1).
    PMID: 34893875 DOI: 10.1093/molbev/msab340
    Island biogeography is one of the most powerful subdisciplines of ecology: its mathematical predictions that island size and distance to mainland determine diversity have withstood the test of time. A key question is whether these predictions follow at a population-genomic level. Using rigorous ancient-DNA protocols, we retrieved approximately 1,000 genomic markers from approximately 100 historic specimens of two Southeast Asian songbird complexes from across the Sunda Shelf archipelago collected 1893-1957. We show that the genetic affinities of populations on small shelf islands defy the predictions of geographic distance and appear governed by Earth-historic factors including the position of terrestrial barriers (paleo-rivers) and persistence of corridors (Quaternary land bridges). Our analyses suggest that classic island-biogeographic predictors may not hold well for population-genomic dynamics on the thousands of shelf islands across the globe, which are exposed to dynamic changes in land distribution during Quaternary climate change.
  9. Hill JK, Gray MA, Khen CV, Benedick S, Tawatao N, Hamer KC
    Philos Trans R Soc Lond B Biol Sci, 2011 Nov 27;366(1582):3265-76.
    PMID: 22006967 DOI: 10.1098/rstb.2011.0050
    Large areas of tropical forest now exist as remnants scattered across agricultural landscapes, and so understanding the impacts of forest fragmentation is important for biodiversity conservation. We examined species richness and nestedness among tropical forest remnants in birds (meta-analysis of published studies) and insects (field data for fruit-feeding Lepidoptera (butterflies and moths) and ants). Species-area relationships were evident in all four taxa, and avian and insect assemblages in remnants typically were nested subsets of those in larger areas. Avian carnivores and nectarivores and predatory ants were more nested than other guilds, implying that the sequential loss of species was more predictable in these groups, and that fragmentation alters the trophic organization of communities. For butterflies, the ordering of fragments to achieve maximum nestedness was by fragment area, suggesting that differences among fragments were driven mainly by extinction. In contrast for moths, maximum nestedness was achieved by ordering species by wing length; species with longer wings (implying better dispersal) were more likely to occur at all sites, including low diversity sites, suggesting that differences among fragments were driven more strongly by colonization. Although all four taxa exhibited high levels of nestedness, patterns of species turnover were also idiosyncratic, and thus even species-poor sites contributed to landscape-scale biodiversity, particularly for insects.
  10. Edwards FA, Edwards DP, Larsen TH, Hsu WW, Benedick S, Chung A, et al.
    Anim. Conserv., 2014 Apr;17(2):163-173.
    PMID: 25821399
    Forests in Southeast Asia are rapidly being logged and converted to oil palm. These changes in land-use are known to affect species diversity but consequences for the functional diversity of species assemblages are poorly understood. Environmental filtering of species with similar traits could lead to disproportionate reductions in trait diversity in degraded habitats. Here, we focus on dung beetles, which play a key role in ecosystem processes such as nutrient recycling and seed dispersal. We use morphological and behavioural traits to calculate a variety of functional diversity measures across a gradient of disturbance from primary forest through intensively logged forest to oil palm. Logging caused significant shifts in community composition but had very little effect on functional diversity, even after a repeated timber harvest. These data provide evidence for functional redundancy of dung beetles within primary forest and emphasize the high value of logged forests as refugia for biodiversity. In contrast, conversion of forest to oil palm greatly reduced taxonomic and functional diversity, with a marked decrease in the abundance of nocturnal foragers, a higher proportion of species with small body sizes and the complete loss of telecoprid species (dung-rollers), all indicating a decrease in the functional capacity of dung beetles within plantations. These changes also highlight the vulnerability of community functioning within logged forests in the event of further environmental degradation.
  11. Madrid RS, Sychra O, Benedick S, Edwards DP, Efeykin BD, Fandrem M, et al.
    Int J Parasitol Parasites Wildl, 2020 Dec;13:231-247.
    PMID: 33294362 DOI: 10.1016/j.ijppaw.2020.10.011
    The tropical rainforests of Sundaland are a global biodiversity hotspot increasingly threatened by human activities. While parasitic insects are an important component of the ecosystem, their diversity and parasite-host relations are poorly understood in the tropics. We investigated parasites of passerine birds, the chewing lice of the speciose genus MyrsideaWaterston, 1915 (Phthiraptera: Menoponidae) in a natural rainforest community of Malaysian Borneo. Based on morphology, we registered 10 species of lice from 14 bird species of six different host families. This indicated a high degree of host specificity and that the complexity of the system could be underestimated with the potential for cryptic lineages/species to be present. We tested the species boundaries by combining morphological, genetic and host speciation diversity. The phylogenetic relationships of lice were investigated by analyzing the partial mitochondrial cytochrome oxidase I (COI) and the nuclear elongation factor alpha (EF-1α) genes sequences of the species. This revealed a monophyletic group of Myrsidea lineages from seven hosts of the avian family Pycnonotidae, one host of Timaliidae and one host of Pellorneidae. However, species delimitation methods supported the species boundaries hypothesized by morphological studies and confirmed that four species of Myrsidea are not single host specific. Cophylogenetic analysis by both distance-based test ParaFit and event-based method Jane confirmed overall congruence between the phylogenies of Myrsidea and their hosts. In total we recorded three cospeciation events for 14 host-parasite associations. However only one host-parasite link (M. carmenae and their hosts Terpsiphone affinis and Hypothymis azurea) was significant after the multiple testing correction in ParaFit. Four new species are described: Myrsidea carmenaesp.n. ex Hypothymis azurea and Terpsiphone affinis, Myrsidea franciscaesp.n. ex Rhipidura javanica, Myrsidea ramonisp.n. ex Copsychus malabaricus stricklandii, and Myrsidea victoriaesp.n. ex. Turdinus sepiarius.
  12. Cros E, Chattopadhyay B, Garg KM, Ng NSR, Tomassi S, Benedick S, et al.
    Mol Ecol, 2020 07;29(14):2692-2706.
    PMID: 32542783 DOI: 10.1111/mec.15509
    Quaternary climate oscillations are a well-known driver of animal diversification, but their effects are most well studied in areas where glaciations lead to habitat fragmentation. In large areas of the planet, however, glaciations have had the opposite effect, but here their impacts are much less well understood. This is especially true in Southeast Asia, where cyclical changes in land distribution have generated enormous land expansions during glacial periods. In this study, we selected a panel of five songbird species complexes covering a range of ecological specificities to investigate the effects Quaternary land bridges have had on the connectivity of Southeast Asian forest biota. Specifically, we combined morphological and bioacoustic analysis with an arsenal of population genomic and modelling approaches applied to thousands of genome-wide DNA markers across a total of more than 100 individuals. Our analyses show that species dependent on forest understorey exhibit deep differentiation between Borneo and western Sundaland, with no evidence of gene flow during the land bridges accompanying the last 1-2 ice ages. In contrast, dispersive canopy species and habitat generalists have experienced more recent gene flow. Our results argue that there remains much cryptic species-level diversity to be discovered in Southeast Asia even in well-known animal groups such as birds, especially in nondispersive forest understorey inhabitants. We also demonstrate that Quaternary land bridges have not been equally suitable conduits of gene flow for all species complexes and that life history is a major factor in predicting relative population divergence time across Quaternary climate fluctuations.
  13. Cros E, Ng EYX, Oh RRY, Tang Q, Benedick S, Edwards DP, et al.
    Evol Appl, 2020 May;13(5):1026-1036.
    PMID: 32431750 DOI: 10.1111/eva.12918
    Habitat fragmentation is a major extinction driver. Despite dramatically increasing fragmentation across the globe, its specific impacts on population connectivity across species with differing life histories remain difficult to characterize, let alone quantify. Here, we investigate patterns of population connectivity in six songbird species from Singapore, a highly fragmented tropical rainforest island. Using massive panels of genome-wide single nucleotide polymorphisms across dozens of samples per species, we examined population genetic diversity, inbreeding, gene flow and connectivity among species along a spectrum of ecological specificities. We found a higher resilience to habitat fragmentation in edge-tolerant and forest-canopy species as compared to forest-dependent understorey insectivores. The latter exhibited levels of genetic diversity up to three times lower in Singapore than in populations from contiguous forest elsewhere. Using dense genomic and geographic sampling, we identified individual barriers such as reservoirs that effectively minimize gene flow in sensitive understorey birds, revealing that terrestrial forest species may exhibit levels of sensitivity to fragmentation far greater than previously expected. This study provides a blueprint for conservation genomics at small scales with a view to identifying preferred locations for habitat corridors, flagging candidate populations for restocking with translocated individuals and improving the design of future reserves.
  14. Edwards DP, Magrach A, Woodcock P, Ji Y, Lim NT-, Edwards FA, et al.
    Ecol Appl, 2014;24(8):2029-49.
    PMID: 29185670 DOI: 10.1890/14-0010.1
    Strong global demand for tropical timber and agricultural products has driven large-scale logging and subsequent conversion of tropical forests. Given that the majority of tropical landscapes have been or will likely be logged, the protection of biodiversity within tropical forests thus depends on whether species can persist in these economically exploited lands, and if species cannot persist, whether we can protect enough primary forest from logging and conversion. However, our knowledge of the impact of logging and conversion on biodiversity is limited to a few taxa, often sampled in different locations with complex land-use histories, hampering attempts to plan cost-effective conservation strategies and to draw conclusions across taxa. Spanning a land-use gradient of primary forest, once- and twice-logged forests, and oil palm plantations, we used traditional sampling and DNA metabarcoding to compile an extensive data set in Sabah, Malaysian Borneo for nine vertebrate and invertebrate taxa to quantify the biological impacts of logging and oil palm, develop cost-effective methods of protecting biodiversity, and examine whether there is congruence in response among taxa. Logged forests retained high species richness, including, on average, 70% of species found in primary forest. In contrast, conversion to oil palm dramatically reduces species richness, with significantly fewer primary-forest species than found on logged forest transects for seven taxa. Using a systematic conservation planning analysis, we show that efficient protection of primary-forest species is achieved with land portfolios that include a large proportion of logged-forest plots. Protecting logged forests is thus a cost-effective method of protecting an ecologically and taxonomically diverse range of species, particularly when conservation budgets are limited. Six indicator groups (birds, leaf-litter ants, beetles, aerial hymenopterans, flies, and true bugs) proved to be consistently good predictors of the response of the other taxa to logging and oil palm. Our results confidently establish the high conservation value of logged forests and the low value of oil palm. Cross-taxon congruence in responses to disturbance also suggests that the practice of focusing on key indicator taxa yields important information of general biodiversity in studies of logging and oil palm.
  15. Ji Y, Ashton L, Pedley SM, Edwards DP, Tang Y, Nakamura A, et al.
    Ecol Lett, 2013 Oct;16(10):1245-57.
    PMID: 23910579 DOI: 10.1111/ele.12162
    To manage and conserve biodiversity, one must know what is being lost, where, and why, as well as which remedies are likely to be most effective. Metabarcoding technology can characterise the species compositions of mass samples of eukaryotes or of environmental DNA. Here, we validate metabarcoding by testing it against three high-quality standard data sets that were collected in Malaysia (tropical), China (subtropical) and the United Kingdom (temperate) and that comprised 55,813 arthropod and bird specimens identified to species level with the expenditure of 2,505 person-hours of taxonomic expertise. The metabarcode and standard data sets exhibit statistically correlated alpha- and beta-diversities, and the two data sets produce similar policy conclusions for two conservation applications: restoration ecology and systematic conservation planning. Compared with standard biodiversity data sets, metabarcoded samples are taxonomically more comprehensive, many times quicker to produce, less reliant on taxonomic expertise and auditable by third parties, which is essential for dispute resolution.
  16. Ewers RM, Boyle MJ, Gleave RA, Plowman NS, Benedick S, Bernard H, et al.
    Nat Commun, 2015 Apr 13;6:6836.
    PMID: 25865801 DOI: 10.1038/ncomms7836
    Invertebrates are dominant species in primary tropical rainforests, where their abundance and diversity contributes to the functioning and resilience of these globally important ecosystems. However, more than one-third of tropical forests have been logged, with dramatic impacts on rainforest biodiversity that may disrupt key ecosystem processes. We find that the contribution of invertebrates to three ecosystem processes operating at three trophic levels (litter decomposition, seed predation and removal, and invertebrate predation) is reduced by up to one-half following logging. These changes are associated with decreased abundance of key functional groups of termites, ants, beetles and earthworms, and an increase in the abundance of small mammals, amphibians and insectivorous birds in logged relative to primary forest. Our results suggest that ecosystem processes themselves have considerable resilience to logging, but the consistent decline of invertebrate functional importance is indicative of a human-induced shift in how these ecological processes operate in tropical rainforests.
  17. Hudson LN, Newbold T, Contu S, Hill SL, Lysenko I, De Palma A, et al.
    Ecol Evol, 2017 Jan;7(1):145-188.
    PMID: 28070282 DOI: 10.1002/ece3.2579
    The PREDICTS project-Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (www.predicts.org.uk)-has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.
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