Two centuries of biodiversity discovery and loss in Singapore.

There is an urgent need for reliable data on the impacts of deforestation on tropical biodiversity. The city-state of Singapore has one of the most detailed biodiversity records in the tropics, dating back to the turn of the 19th century. In 1819, Singapore was almost entirely covered in primary forest, but this has since been largely cleared. We compiled more than 200 y of records for 10 major taxonomic groups in Singapore (>50,000 individual records; >3,000 species), and we estimated extinction rates using recently developed and novel statistical models that account for "dark extinctions," i.e., extinctions of undiscovered species. The estimated overall extinction rate was 37% (95% CI [31 to 42%]). Extrapolating our Singapore observations to a future business-as-usual deforestation scenario for Southeast Asia suggests that 18% (95% CI [16 to 22%]) of species will be lost regionally by 2100. Our extinction estimates for Singapore and Southeast Asia are a factor of two lower than previous estimates that also attempted to account for dark extinctions. However, we caution that particular groups such as large mammals, forest-dependent birds, orchids, and butterflies are disproportionately vulnerable.

Leaf and twig traits predict habitat adaptation and demographic strategies in tropical freshwater swamp forest trees.

Differences in demographic and environmental niches facilitate plant species coexistence in tropical forests. However, the adaptations that enable species to achieve higher demographic rates (e.g. growth or survival) or occupy unique environmental niches (e.g. waterlogged conditions) remain poorly understood. Anatomical traits may better predict plant environmental and demographic strategies because they are direct measurements of structures involved in these adaptations. We collected 18 leaf and twig traits from 29 tree species in a tropical freshwater swamp forest in Singapore. We estimated demographic parameters of the 29 species from growth and survival models, and degree of association toward swamp habitats. We examined pairwise trait-trait, trait-demography and trait-environment links while controlling for phylogeny. Leaf and twig anatomical traits were better predictors of all demographic parameters than other commonly measured leaf and wood traits. Plants with wider vessels had faster growth rates but lower survival rates. Leaf and spongy mesophyll thickness predicted swamp association. These findings demonstrate the utility of anatomical traits as indicators of plant hydraulic strategies and their links to growth-mortality trade-offs and waterlogging stress tolerance that underlie species coexistence mechanisms in tropical forest trees.

Leaf decomposition and flammability are largely decoupled across species in a tropical swamp forest despite sharing some predictive leaf functional traits.

Decomposition and fire are major carbon pathways in many ecosystems, yet potential linkages between these processes are poorly understood. We test whether variability in decomposability and flammability across species are related to each other and to key plant functional traits in tropical swamp forests, where habitat degradation is elevating decomposition and fire regimes. Using senesced and fresh leaves of 22 swamp tree species in Singapore, we conducted an in situ decomposition experiment and a laboratory flammability experiment. We analysed 16 leaf physical and biochemical traits as predictors of decomposability and components of flammability: combustibility, ignitability and sustainability. Decomposability and flammability were largely decoupled across species, despite some shared predictive traits such as specific leaf area (SLA). Physical traits predicted that thicker leaves with a smaller SLA and volume decomposed faster, while various cation concentrations predicted flammability components, particularly ignitability. We show that flammability and decomposability of swamp forest leaves are decoupled because flammability is mostly driven by biochemical traits, while decomposition is driven by physical traits. Our approach identifies species that are slow to decompose and burn (e.g. Calophyllum tetrapterum and Xanthophyllum flavescens), which could be planted to mitigate carbon losses in tropical swamp reforestation.

Downstream resource leakage a necessary condition for the stress-gradient hypothesis in processing chain commensalisms.

The stress-gradient hypothesis (SGH) in ecology predicts that the strength and frequency of positive interspecific interactions, including processing chain commensalisms (PCCs), increase with environmental stress. Although observed in some empirical PCC studies, a recent theoretical study of PCCs using a consumer-resource-type model found that, given the model's assumptions, the SGH never occurs. To investigate if this is a true reflection of PCCs or merely an artefact of the model, in this study, we modified this earlier model formulation by incorporating generalized, monotonically increasing resource uptake functions in place of linear functions, and added a term to represent the spontaneous leakage of the downstream resource to the environment. Mathematical analyses of the model revealed two key insights: 1) the specific algebraic forms of the functional responses of the species in a PCC do not affect the long-term behaviour of the system; 2) the SGH can occur in a facilitative interaction only if the consumer-independent leakage rate of the downstream resource exceeds the consumer-independent input rate. The first insight shows that the outcomes of consumer-resource interactions are robust to details of the functional responses when the functional responses are monotonically increasing, while the second insight shows that the SGH is not a universal feature of positive interactions but instead holds only under a well-defined set of conditions which may vary between PCC interactions and the environmental contexts in which they take place.

Extinction rate of discovered and undiscovered plants in Singapore.

Extinction is a key issue in the assessment of global biodiversity. However, many extinction rate measures do not account for species that went extinct before they could be discovered. The highly developed island city-state of Singapore has one of the best-documented tropical floras in the world. This allowed us to estimate the total rate of floristic extinctions in Singapore since 1822 after accounting for sampling effort and crypto extinctions by collating herbaria records. Our database comprised 34,224 specimens from 2076 native species, of which 464 species (22%) were considered nationally extinct. We assumed that undiscovered species had the same annual per-species extinction rates as discovered species and that no undiscovered species remained extant. With classical and Bayesian algorithms, we estimated that 304 (95% confidence interval, 213-414) and 412 (95% credible interval, 313-534) additional species went extinct before they could be discovered, respectively; corresponding total extinction rate estimates were 32% and 35% (range 30-38%). We detected violations of our 2 assumptions that could cause our extinction estimates, particularly the absolute numbers, to be biased downward. Thus, our estimates should be treated as lower bounds. Our results illustrate the possible magnitudes of plant extirpations that can be expected in the tropics as development continues.

Tasa de Extinción de Plantas Descubiertas y No Descubiertas en Singapur Resumen La extinción es un tema importante para la valoración de la biodiversidad global. Sin embargo, muchas medidas de la tasa de extinción no consideran a las especies que se extinguieron antes de que pudieran ser descubiertas. Singapur, la ciudad-estado isleña altamente desarrollada, tiene una de las floras mejor documentadas del mundo. Esto nos permitió estimar la tasa total de las extinciones florísticas en Singapur desde 1822 después de considerar el esfuerzo de muestreo y las criptoextinciones cuando recopilamos los registros de herbarios. Nuestra base de datos incluyó 34,224 especímenes de unas 2,076 especies nativas, de las cuales 464 especies (22%) estaban consideradas como extintas a nivel nacional. Asumimos que las especies no descubiertas tuvieron la misma tasa anual de extinción por especie que las especies descubiertas y que ninguna especie no descubierta permanecía en existencia. Con algoritmos clásicos y bayesianos, respectivamente, estimamos que 304 (95% IC 213-414) y 412 (95% IC 313-534) especies adicionales se extinguieron antes de que fueran descubiertas; las estimaciones correspondientes de la tasa de extinción total fueron 32% y 35% (rango de 30-38%). Detectamos violaciones en nuestras dos suposiciones que podrían causar que nuestras estimaciones de extinción, particularmente los números absolutos, tuvieran un sesgo hacia abajo. Por lo tanto, nuestras estimaciones deberían ser tratadas como límites inferiores. Nuestros resultados ilustran las magnitudes posibles de las extirpaciones de plantas que pueden esperarse en los trópicos conforme el desarrollo continúa.

Dipteran larvae and microbes facilitate nutrient sequestration in the Nepenthes gracilis pitcher plant host.

The fluid-containing traps of Nepenthes carnivorous pitcher plants (Nepenthaceae) are often inhabited by organisms known as inquilines. Dipteran larvae are key components of such communities and are thought to facilitate pitcher nitrogen sequestration by converting prey protein into inorganic nitrogen, although this has never been demonstrated in Nepenthes Pitcher fluids are also inhabited by microbes, although the relationship(s) between these and the plant is still unclear. In this study, we examined the hypothesis of digestive mutualism between N. gracilis pitchers and both dipteran larvae and fluid microbes. Using dipteran larvae, prey and fluid volumes mimicking in situ pitcher conditions, we conducted in vitro experiments and measured changes in available fluid nitrogen in response to dipteran larvae and microbe presence. We showed that the presence of dipteran larvae resulted in significantly higher and faster releases of ammonium and soluble protein into fluids in artificial pitchers, and that the presence of fluid microbes did likewise for ammonium. We showed also that niche segregation occurs between phorid and culicid larvae, with the former fragmenting prey carcasses and the latter suppressing fluid microbe levels. These results clarify the relationships between several key pitcher-dwelling organisms, and show that pitcher communities facilitate nutrient sequestration in their host.

Mitigating the impact of oil-palm monoculture on freshwater fishes in Southeast Asia.

Anthropogenic land-cover change is driving biodiversity loss worldwide. At the epicenter of this crisis lies Southeast Asia, where biodiversity-rich forests are being converted to oil-palm monocultures. As demand for palm oil increases, there is an urgent need to find strategies that maintain biodiversity in plantations. Previous studies found that retaining forest patches within plantations benefited some terrestrial taxa but not others. However, no study has focused on aquatic taxa such as fishes, despite their importance to human well-being. We assessed the efficacy of forested riparian reserves in conserving freshwater fish biodiversity in oil-palm monoculture by sampling stream fish communities in an oil-palm plantation in Central Kalimantan, Indonesia. Forested riparian reserves maintained preconversion local fish species richness and functional diversity. In contrast, local and total species richness, biomass, and functional diversity declined markedly in streams without riparian reserves. Mechanistically, riparian reserves appeared to increase local species richness by increasing leaf litter cover and maintaining coarse substrate. The loss of fishes specializing in leaf litter and coarse substrate decreased functional diversity and altered community composition in oil-palm plantation streams that lacked riparian reserves. Thus, a land-sharing strategy that incorporates the retention of forested riparian reserves may maintain the ecological integrity of fish communities in oil-palm plantations. We urge policy makers and growers to make retention of riparian reserves in oil-palm plantations standard practice, and we encourage palm-oil purchasers to source only palm oil from plantations that employ this practice.

Trends in the direction of global plant invasion biology research over the past two decades.

Invasive plants are a growing ecological problem worldwide, but biases and patterns within invasive plant research may affect our understanding of invasive plant ecology. In this study, we analyzed 458 invasive plant papers sampled from the two journals dedicated entirely to the field of invasion biology, i.e., Biological Invasions and Neobiota. From these papers, we collected information on geographic coverage, climate, habitat, taxonomic coverage, plant functional type, and research topic to examine trends across a 21-year time period from 1999 to 2020. Our analysis found that invasive plant research was consistently biased toward temperate grassland and forest ecosystems particularly within the Americas, Europe, and Australia, and toward smaller, herbaceous invasive plant species (i.e., forbs, grasses, and shrubs), with an increase in interest in invasive nitrogen-fixing legumes over time. Our analysis also identified "hot" research topics in invasive plant research at specific time periods, such as a peak in the use of genetic analysis methods in 2014-2015 and a more recent focus on plant physiological and functional traits. While current models, concepts, and understanding of plant invasion ecology are still driven by such biases, this has been partially offset by recent increased research in understudied systems, as well as increasing awareness that plant invasion is heavily affected by their growth types, physiological traits, and soil interactions. As the field of invasion biology becomes ever increasingly important over time, focusing invasive plant research on understudied ecosystems and plant groups will allow us to develop a more holistic understanding of the ecology of invasive plants. In particular, given the outsized importance of the tropics to global biodiversity, the threats they face, and the dearth of studies, it is of critical importance that more invasive plant research is conducted within the tropics to develop a more globally representative understanding of invasive plant ecology.

Non-additive biotic interactions improve predictions of tropical tree growth and impact community size structure.

Growth in individual size or biomass is a key demographic component in population models, with wide-ranging applications from quantifying species performance across abiotic or biotic conditions to assessing landscape-level dynamics under global change. In forest ecology, the responses of tree growth to biotic interactions are widely held to be crucial for understanding forest diversity, function, and structure. To date, most studies on plant-plant interactions only examine the additive competitive or facilitative interactions between species pairs; however, there is increasing evidence of non-additive, higher-order interactions (HOIs) impacting species demographic rates. When HOIs are present, the dynamics of a multispecies community cannot be fully understood or accurately predicted solely from pairwise outcomes because of how additional species "interfere" with the direct, pairwise interactions. Such HOIs should be particularly prevalent when species show non-linear functional responses to resource availability and resource-acquisition traits themselves are density dependent. With this in mind, we used data from a tropical secondary forest-a system that fulfills both of these conditions-to build an ontogenetic diameter growth model for individuals across 10 woody-plant species. We allowed both direct and indirect interactions within communities to influence the species-specific growth parameters in a generalized Lotka-Volterra model. Specifically, indirect interactions entered the model as higher-order quadratic terms, i.e., non-additive effects of conspecific and heterospecific neighbor size on the focal individual's growth. For the whole community and for four out of 10 focal species, the model that included HOIs had more statistical support than the model that included only direct interactions, despite the former containing a far greater number of parameters. HOIs had comparable effect sizes to direct interactions, and tended to further reduce the diameter growth rates of most species beyond what direct interactions had already reduced. In a simulation of successional stand dynamics, the inclusion of HOIs led to rank swaps in species' diameter hierarchies, even when community-level size distributions remained qualitatively similar. Our study highlights the implications, and discusses possible mechanisms, of non-additive density dependence in highly diverse and light-competitive tropical forests.

Familiarity with, perceptions of and attitudes toward butterflies of urban park users in megacities across East and Southeast Asia.

Perceptions of, and attitudes toward, wildlife are influenced by exposure to, and direct experiences with, nature. Butterflies are a conspicuous and ubiquitous component of urban nature across megacities that are highly urbanized with little opportunity for human-nature interactions. We evaluated public familiarity with, perceptions of and attitudes toward butterflies across nine megacities in East and Southeast Asia through face-to-face interviews with 1774 urban park users. A total of 79% of respondents had seen butterflies in their cities mostly in urban parks, indicating widespread familiarity with butterflies. Those who had seen butterflies also had higher perceptions of butterflies, whereas greater than 50% of respondents had positive attitudes toward butterflies. Frequent visits to natural places in urban neighbourhoods was associated with (i) sightings of caterpillars, indicating increased familiarity with urban wildlife, and (ii) increased connectedness to nature. We found two significant positive relationships: (i) between connectedness to nature and attitudes toward butterflies and (ii) between connectedness to nature and perceptions of butterflies, firmly linking parks users' thoughts and feelings about butterflies with their view of nature. This suggests that butterflies in urban parks can play a key role in building connectedness to nature and consequently pro-environmental behaviours and support for wildlife conservation among urban residents.

Pollination of Ficus elastica: India rubber re-establishes sexual reproduction in Singapore.

Ficus elastica, otherwise known as India Rubber (although its geographical origins are unclear), was an important source of latex in the early 19th century and was widely cultivated in tropical Asia. Like all figs, F. elastica is dependent on tiny, highly specific wasps for pollination, and detailed studies based out of Singapore in the 1930s suggested that through the loss of its pollinator F. elastica was extinct in the wild. However, around 2005 wild seedlings of F. elastica began appearing in Singapore. We identified the pollinator as Platyscapa clavigera, which was originally described from F. elastica in Bogor in 1885. A visit to Bogor Botanical Gardens revealed that not only was F. elastica being pollinated by P. clavigera in the gardens, but there was clear evidence it had been reproducing naturally there over many decades. Although Singapore has a native fig flora of over 50 species, F. elastica went unpollinated for at least 70 years and probably from the time it was introduced during the 19th century. These observations illustrate the extraordinary specificity of this interaction and, through the fig's ability to wait for its pollinators, demonstrates one way in which such highly specific interactions can be evolutionarily stable.