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  1. Keith SA, Maynard JA, Edwards AJ, Guest JR, Bauman AG, van Hooidonk R, et al.
    Proc. Biol. Sci., 2016 05 11;283(1830).
    PMID: 27170709 DOI: 10.1098/rspb.2016.0011
    Coral spawning times have been linked to multiple environmental factors; however, to what extent these factors act as generalized cues across multiple species and large spatial scales is unknown. We used a unique dataset of coral spawning from 34 reefs in the Indian and Pacific Oceans to test if month of spawning and peak spawning month in assemblages of Acropora spp. can be predicted by sea surface temperature (SST), photosynthetically available radiation, wind speed, current speed, rainfall or sunset time. Contrary to the classic view that high mean SST initiates coral spawning, we found rapid increases in SST to be the best predictor in both cases (month of spawning: R(2) = 0.73, peak: R(2) = 0.62). Our findings suggest that a rapid increase in SST provides the dominant proximate cue for coral mass spawning over large geographical scales. We hypothesize that coral spawning is ultimately timed to ensure optimal fertilization success.
  2. Boyero L, Pearson RG, Hui C, Gessner MO, Pérez J, Alexandrou MA, et al.
    Proc. Biol. Sci., 2016 Apr 27;283(1829).
    PMID: 27122551 DOI: 10.1098/rspb.2015.2664
    Plant litter breakdown is a key ecological process in terrestrial and freshwater ecosystems. Streams and rivers, in particular, contribute substantially to global carbon fluxes. However, there is little information available on the relative roles of different drivers of plant litter breakdown in fresh waters, particularly at large scales. We present a global-scale study of litter breakdown in streams to compare the roles of biotic, climatic and other environmental factors on breakdown rates. We conducted an experiment in 24 streams encompassing latitudes from 47.8° N to 42.8° S, using litter mixtures of local species differing in quality and phylogenetic diversity (PD), and alder (Alnus glutinosa) to control for variation in litter traits. Our models revealed that breakdown of alder was driven by climate, with some influence of pH, whereas variation in breakdown of litter mixtures was explained mainly by litter quality and PD. Effects of litter quality and PD and stream pH were more positive at higher temperatures, indicating that different mechanisms may operate at different latitudes. These results reflect global variability caused by multiple factors, but unexplained variance points to the need for expanded global-scale comparisons.
  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. Dong SX, Davies SJ, Ashton PS, Bunyavejchewin S, Supardi MN, Kassim AR, et al.
    Proc. Biol. Sci., 2012 Oct 7;279(1744):3923-31.
    PMID: 22833269
    The response of tropical forests to global climate variability and change remains poorly understood. Results from long-term studies of permanent forest plots have reported different, and in some cases opposing trends in tropical forest dynamics. In this study, we examined changes in tree growth rates at four long-term permanent tropical forest research plots in relation to variation in solar radiation, temperature and precipitation. Temporal variation in the stand-level growth rates measured at five-year intervals was found to be positively correlated with variation in incoming solar radiation and negatively related to temporal variation in night-time temperatures. Taken alone, neither solar radiation variability nor the effects of night-time temperatures can account for the observed temporal variation in tree growth rates across sites, but when considered together, these two climate variables account for most of the observed temporal variability in tree growth rates. Further analysis indicates that the stand-level response is primarily driven by the responses of smaller-sized trees (less than 20 cm in diameter). The combined temperature and radiation responses identified in this study provide a potential explanation for the conflicting patterns in tree growth rates found in previous studies.
  5. Byrnes G, Lim NT, Spence AJ
    Proc. Biol. Sci., 2008 May 7;275(1638):1007-13.
    PMID: 18252673 DOI: 10.1098/rspb.2007.1684
    Arboreal animals negotiate a highly three-dimensional world that is discontinuous on many spatial scales. As the scale of substrate discontinuity increases, many arboreal animals rely on leaping or gliding locomotion between distant supports. In order to successfully move through their habitat, gliding animals must actively modulate both propulsive and aerodynamic forces. Here we examined the take-off and landing kinetics of a free-ranging gliding mammal, the Malayan colugo (Galeopterus variegatus) using a custom-designed three-dimensional accelerometry system. We found that colugos increase the propulsive impulse to affect longer glides. However, we also found that landing forces are negatively associated with glide distance. Landing forces decrease rapidly as glide distance increases from the shortest glides, then level off, suggesting that the ability to reorient the aerodynamic forces prior to landing is an important mechanism to reduce velocity and thus landing forces. This ability to substantially alter the aerodynamic forces acting on the patagial wing in order to reorient the body is a key to the transition between leaping and gliding and allows gliding mammals to travel long distances between trees with reduced risk of injury. Longer glides may increase the access to distributed resources and reduce the exposure to predators in the canopy or on the forest floor.
  6. Feeley KJ, Davies SJ, Ashton PS, Bunyavejchewin S, Nur Supardi MN, Kassim AR, et al.
    Proc. Biol. Sci., 2007 Nov 22;274(1627):2857-64.
    PMID: 17785266
    The responses of tropical forests to global anthropogenic disturbances remain poorly understood. Above-ground woody biomass in some tropical forest plots has increased over the past several decades, potentially reflecting a widespread response to increased resource availability, for example, due to elevated atmospheric CO2 and/or nutrient deposition. However, previous studies of biomass dynamics have not accounted for natural patterns of disturbance and gap phase regeneration, making it difficult to quantify the importance of environmental changes. Using spatially explicit census data from large (50 ha) inventory plots, we investigated the influence of gap phase processes on the biomass dynamics of four 'old-growth' tropical forests (Barro Colorado Island (BCI), Panama; Pasoh and Lambir, Malaysia; and Huai Kha Khaeng (HKK), Thailand). We show that biomass increases were gradual and concentrated in earlier-phase forest patches, while biomass losses were generally of greater magnitude but concentrated in rarer later-phase patches. We then estimate the rate of biomass change at each site independent of gap phase dynamics using reduced major axis regressions and ANCOVA tests. Above-ground woody biomass increased significantly at Pasoh (+0.72% yr(-1)) and decreased at HKK (-0.56% yr(-1)) independent of changes in gap phase but remained stable at both BCI and Lambir. We conclude that gap phase processes play an important role in the biomass dynamics of tropical forests, and that quantifying the role of gap phase processes will help improve our understanding of the factors driving changes in forest biomass as well as their place in the global carbon budget.
  7. Kingston T, Lara MC, Jones G, Akbar Z, Kunz TH, Schneider CJ
    Proc. Biol. Sci., 2001 Jul 7;268(1474):1381-6.
    PMID: 11429138
    We present evidence that a relatively widespread and common bat from South East Asia comprises two morphologically cryptic but acoustically divergent species. A population of the bicoloured leaf-nosed bat (Hipposideros bicolor) from Peninsular Malaysia exhibits a bimodal distribution of echolocation call frequencies, with peaks in the frequency of maximum energy at ca. 131 and 142 kHz. The two phonic types are genetically distinct, with a cytochrome b sequence divergence of just under 7%. We consider the mechanisms by which acoustic divergence in these species might arise. Differences in call frequency are not likely to effect resource partitioning by detectable prey size or functional range. However, ecological segregation may be achieved by differences in microhabitat use; the 131kHz H. bicolor is characterized by significantly longer forearms, lower wing loading, a lower aspect ratio and a more rounded wingtip, features that are associated with greater manoeuvrability in flight that may enable it to forage in more cluttered environments relative to the 142 kHz phonic type. We suggest that acoustic divergence in these species is a consequence of social selection for a clear communication channel, which is mediated by the close link between the acoustic signal and receptor systems imposed by the highly specialized nature of the hipposiderid and rhinolophid echolocation system.
  8. Wills C, Condit R
    Proc. Biol. Sci., 1999 Jul 22;266(1427):1445-52.
    PMID: 10457617
    Quadrat-based analysis of two rainforest plots of area 50 ha, one in Panama (Barro Colorado Island, BCI) and the other in Malaysia (Pasoh), shows that in both plots recruitment is in general negatively correlated with both numbers and biomass of adult trees of the same species in the same quadrat. At BCI, this effect is not significantly influenced by treefall gaps. In both plots, recruitment of individual species is negatively correlated with the numbers of trees of all species in the quadrats, but not with overall biomass. These observations suggest, but do not prove, widespread frequency-dependent effects produced by pathogens and seed-predators that act most effectively in quadrats crowded with trees. Within-species correlations of mortality with numbers or biomass are not found in either plot, indicating that most frequency-dependent mortality takes place before the trees reach 1 cm in diameter. Stochastic effects caused by BCI's more rapid tree turnover may contribute to a larger variance in diversity from quadrat to quadrat at BCI, although they are not sufficient to explain why BCI has fewer than half as many tree species as Pasoh. Finally, in both plots quadrats with low diversity show a significant increase in diversity over time, and this increase is stronger at BCI. This process, like the frequency-dependence, will tend to maintain diversity over time. In general, these non-random forces that should lead to the maintenance of diversity are slightly stronger at BCI, even though the BCI plot is less diverse than the Pasoh plot.
  9. Harrison RD
    Proc. Biol. Sci., 2000 May 7;267(1446):911-5.
    PMID: 10853734
    Figs (Ficus spp.) and their species-specific pollinators, the fig wasps (Agaonidae), have coevolved one of the most intricate interactions found in nature, in which the fig wasps, in return for pollination services, raise their offspring in the fig inflorescence. Fig wasps, however, have very short adult lives and hence are dependent on the near-continuous production of inflorescences to maintain their populations. From January to March 1998 northern Borneo suffered a very severe drought linked to the El Niño-Southern Oscillation event of 1997-1998. This caused a substantial break in the production of inflorescences on dioecious figs and led to the local extinction of their pollinators at Lambir Hills National Park, Sarawak, Malaysia. Most pollinators had not recolonized six months after the drought and, given the high level of endemism and wide extent of the drought, some species may be totally extinct. Cascading effects on vertebrate seed dispersers, for which figs are often regarded as keystone resources, and the tree species dependent on their services are also likely. This has considerable implications for the maintenance of biodiversity under a scenario of climate change and greater climatic extremes.
  10. Xu X, Liu F, Cheng RC, Chen J, Xu X, Zhang Z, et al.
    Proc. Biol. Sci., 2015 Jun 07;282(1808):20142486.
    PMID: 25948684 DOI: 10.1098/rspb.2014.2486
    Living fossils are lineages that have retained plesiomorphic traits through long time periods. It is expected that such lineages have both originated and diversified long ago. Such expectations have recently been challenged in some textbook examples of living fossils, notably in extant cycads and coelacanths. Using a phylogenetic approach, we tested the patterns of the origin and diversification of liphistiid spiders, a clade of spiders considered to be living fossils due to their retention of arachnid plesiomorphies and their exclusive grouping in Mesothelae, an ancient clade sister to all modern spiders. Facilitated by original sampling throughout their Asian range, we here provide the phylogenetic framework necessary for reconstructing liphistiid biogeographic history. All phylogenetic analyses support the monophyly of Liphistiidae and of eight genera. As the fossil evidence supports a Carboniferous Euramerican origin of Mesothelae, our dating analyses postulate a long eastward over-land dispersal towards the Asian origin of Liphistiidae during the Palaeogene (39-58 Ma). Contrary to expectations, diversification within extant liphistiid genera is relatively recent, in the Neogene and Late Palaeogene (4-24 Ma). While no over-water dispersal events are needed to explain their evolutionary history, the history of liphistiid spiders has the potential to play prominently in vicariant biogeographic studies.
  11. Edwards DP, Larsen TH, Docherty TD, Ansell FA, Hsu WW, Derhé MA, et al.
    Proc. Biol. Sci., 2011 Jan 7;278(1702):82-90.
    PMID: 20685713 DOI: 10.1098/rspb.2010.1062
    Southeast Asia is a hotspot of imperiled biodiversity, owing to extensive logging and forest conversion to oil palm agriculture. The degraded forests that remain after multiple rounds of intensive logging are often assumed to be of little conservation value; consequently, there has been no concerted effort to prevent them from being converted to oil palm. However, no study has quantified the biodiversity of repeatedly logged forests. We compare the species richness and composition of birds and dung beetles within unlogged (primary), once-logged and twice-logged forests in Sabah, Borneo. Logging had little effect on the overall richness of birds. Dung beetle richness declined following once-logging but did not decline further after twice-logging. The species composition of bird and dung beetle communities was altered, particularly after the second logging rotation, but globally imperiled bird species (IUCN Red List) did not decline further after twice-logging. Remarkably, over 75 per cent of bird and dung beetle species found in unlogged forest persisted within twice-logged forest. Although twice-logged forests have less biological value than primary and once-logged forests, they clearly provide important habitat for numerous bird and dung beetle species. Preventing these degraded forests from being converted to oil palm should be a priority of policy-makers and conservationists.
  12. Tuck SL, O'Brien MJ, Philipson CD, Saner P, Tanadini M, Dzulkifli D, et al.
    Proc. Biol. Sci., 2016 12 14;283(1844).
    PMID: 27928046
    One of the main environmental threats in the tropics is selective logging, which has degraded large areas of forest. In southeast Asia, enrichment planting with seedlings of the dominant group of dipterocarp tree species aims to accelerate restoration of forest structure and functioning. The role of tree diversity in forest restoration is still unclear, but the 'insurance hypothesis' predicts that in temporally and spatially varying environments planting mixtures may stabilize functioning owing to differences in species traits and ecologies. To test for potential insurance effects, we analyse the patterns of seedling mortality and growth in monoculture and mixture plots over the first decade of the Sabah biodiversity experiment. Our results reveal the species differences required for potential insurance effects including a trade-off in which species with denser wood have lower growth rates but higher survival. This trade-off was consistent over time during the first decade, but growth and mortality varied spatially across our 500 ha experiment with species responding to changing conditions in different ways. Overall, average survival rates were extreme in monocultures than mixtures consistent with a potential insurance effect in which monocultures of poorly surviving species risk recruitment failure, whereas monocultures of species with high survival have rates of self-thinning that are potentially wasteful when seedling stocks are limited. Longer-term monitoring as species interactions strengthen will be needed to more comprehensively test to what degree mixtures of species spread risk and use limited seedling stocks more efficiently to increase diversity and restore ecosystem structure and functioning.
  13. Granados A, Bernard H, Brodie JF
    Proc. Biol. Sci., 2018 02 28;285(1873).
    PMID: 29491176 DOI: 10.1098/rspb.2017.2882
    Animals can have both positive (e.g. via seed dispersal) and negative (e.g. via herbivory) impacts on plants. The net effects of these interactions remain difficult to predict and may be affected by overhunting and habitat disturbance, two widespread threats to tropical forests. Recent studies have documented their separate effects on plant recruitment but our understanding of how defaunation and logging interact to influence tropical tree communities is limited. From 2013 to 2016, we followed the fate of marked tree seedlings (n = 1489) from 81 genera in and outside experimental plots. Our plots differentially excluded small, medium and large-bodied mammal herbivores in logged and unlogged forest in Malaysian Borneo. We assessed the effects of experimental defaunation and logging on taxonomic diversity and plant trait (wood density, specific leaf area, fruit size) composition of seedling communities. Although seedling mortality was highest in the presence of all mammal herbivores (44%), defaunation alone did not alter taxonomic diversity nor plant trait composition. However, herbivores (across all body sizes) significantly reduced mean fruit size across the seedling community over time (95% confidence interval (CI): -0.09 to -0.01), particularly in logged forest (95% CI: -0.12 to -0.003). Our findings suggest that impacts of mammal herbivores on plant communities may be greater in forests with a history of disturbance and could subsequently affect plant functional traits and ecological processes associated with forest regeneration.
  14. Brodie JF, Strimas-Mackey M, Mohd-Azlan J, Granados A, Bernard H, Giordano AJ, et al.
    Proc. Biol. Sci., 2017 01 25;284(1847).
    PMID: 28100818 DOI: 10.1098/rspb.2016.2335
    The responses of lowland tropical communities to climate change will critically influence global biodiversity but remain poorly understood. If species in these systems are unable to tolerate warming, the communities-currently the most diverse on Earth-may become depauperate ('biotic attrition'). In response to temperature changes, animals can adjust their distribution in space or their activity in time, but these two components of the niche are seldom considered together. We assessed the spatio-temporal niches of rainforest mammal species in Borneo across gradients in elevation and temperature. Most species are not predicted to experience changes in spatio-temporal niche availability, even under pessimistic warming scenarios. Responses to temperature are not predictable by phylogeny but do appear to be trait-based, being much more variable in smaller-bodied taxa. General circulation models and weather station data suggest unprecedentedly high midday temperatures later in the century; predicted responses to this warming among small-bodied species range from 9% losses to 6% gains in spatio-temporal niche availability, while larger species have close to 0% predicted change. Body mass may therefore be a key ecological trait influencing the identity of climate change winners and losers. Mammal species composition will probably change in some areas as temperatures rise, but full-scale biotic attrition this century appears unlikely.
  15. Venkataraman VV, Yegian AK, Wallace IJ, Holowka NB, Tacey I, Gurven M, et al.
    Proc. Biol. Sci., 2018 11 07;285(1890).
    PMID: 30404871 DOI: 10.1098/rspb.2018.1492
    The convergent evolution of the human pygmy phenotype in tropical rainforests is widely assumed to reflect adaptation in response to the distinct ecological challenges of this habitat (e.g. high levels of heat and humidity, high pathogen load, low food availability, and dense forest structure), yet few precise adaptive benefits of this phenotype have been proposed. Here, we describe and test a biomechanical model of how the rainforest environment can alter gait kinematics such that short stature is advantageous in dense habitats. We hypothesized that environmental constraints on step length in rainforests alter walking mechanics such that taller individuals are expected to walk more slowly due to their inability to achieve preferred step lengths in the rainforest. We tested predictions from this model with experimental field data from two short-statured populations that regularly forage in the rainforest: the Batek of Peninsular Malaysia and the Tsimane of the Bolivian Amazon. In accordance with model expectations, we found stature-dependent constraints on step length in the rainforest and concomitant reductions in walking speed that are expected to compromise foraging efficiency. These results provide the first evidence that the human pygmy phenotype is beneficial in terms of locomotor performance and highlight the value of applying laboratory-derived biomechanical models to field settings for testing evolutionary hypotheses.
  16. Brock PM, Fornace KM, Grigg MJ, Anstey NM, William T, Cox J, et al.
    Proc. Biol. Sci., 2019 Jan 16;286(1894):20182351.
    PMID: 30963872 DOI: 10.1098/rspb.2018.2351
    The complex transmission ecologies of vector-borne and zoonotic diseases pose challenges to their control, especially in changing landscapes. Human incidence of zoonotic malaria ( Plasmodium knowlesi) is associated with deforestation although mechanisms are unknown. Here, a novel application of a method for predicting disease occurrence that combines machine learning and statistics is used to identify the key spatial scales that define the relationship between zoonotic malaria cases and environmental change. Using data from satellite imagery, a case-control study, and a cross-sectional survey, predictive models of household-level occurrence of P. knowlesi were fitted with 16 variables summarized at 11 spatial scales simultaneously. The method identified a strong and well-defined peak of predictive influence of the proportion of cleared land within 1 km of households on P. knowlesi occurrence. Aspect (1 and 2 km), slope (0.5 km) and canopy regrowth (0.5 km) were important at small scales. By contrast, fragmentation of deforested areas influenced P. knowlesi occurrence probability most strongly at large scales (4 and 5 km). The identification of these spatial scales narrows the field of plausible mechanisms that connect land use change and P. knowlesi, allowing for the refinement of disease occurrence predictions and the design of spatially-targeted interventions.
  17. Jessop TS, Ariefiandy A, Purwandana D, Ciofi C, Imansyah J, Benu YJ, et al.
    Proc. Biol. Sci., 2018 11 14;285(1891).
    PMID: 30429305 DOI: 10.1098/rspb.2018.1829
    Loss of dispersal typifies island biotas, but the selective processes driving this phenomenon remain contentious. This is because selection via, both indirect (e.g. relaxed selection or island syndromes) and direct (e.g. natural selection or spatial sorting) processes may be involved, and no study has yet convincingly distinguished between these alternatives. Here, we combined observational and experimental analyses of an island lizard, the Komodo dragon (Varanus komodoensis, the world's largest lizard), to provide evidence for the actions of multiple processes that could contribute to island dispersal loss. In the Komodo dragon, concordant results from telemetry, simulations, experimental translocations, mark-recapture, and gene flow studies indicated that despite impressive physical and sensory capabilities for long-distance movement, Komodo dragons exhibited near complete dispersal restriction: individuals rarely moved beyond the valleys they were born/captured in. Importantly, lizard site-fidelity was insensitive to common agents of dispersal evolution (i.e. indices of risk for inbreeding, kin and intraspecific competition, and low habitat quality) that consequently reduced survival of resident individuals. We suggest that direct selection restricts movement capacity (e.g. via benefits of spatial philopatry and increased costs of dispersal) alongside use of dispersal-compensating traits (e.g. intraspecific niche partitioning) to constrain dispersal in island species.
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