The ancient Greek philosopher Heraclitus espoused that life is continuously in a state of flux, and this is attested by the ubiquity of temporal changes in environmental conditions such as precipitation and temperature, which are often well characterised by a random process and referred to as temporal environmental stochasticity (TES). TES results in random changes in species’ demographic rates over time, with profound cascading effects on community dynamics and species richness. This is the topic of a new review paper published in Mathematical Biosciences, authored by Tak and Ryan in collaboration with colleagues Jayant Pande from FLAME University, Nadav Shnerb from Bar-Ilan University and James O’Dwyer from the University of Illinois.

In our review, we synthesise studies that have analysed process-based community models to quantitatively examine how TES affects species richness. The simplest community models assume that species interactions are so weak that they can be ignored, such that community dynamics are essentially the sum of independent species dynamics, thus being amenable to mathematical analysis. More complex community models incorporate non-negligible interspecific interactions, which renders them more difficult to analyse. However, techniques from “mean-field theory” can be used to represent the strengths of interspecific interactions as time-averaged constants, such that community dynamics can be represented effectively as the sum of independent species dynamics and analysed.

Our review identified important processes via which TES affects species richness. Firstly, TES increases temporal fluctuations of species populations, such that the variance in species abundance over a particular time period scales quadratically with the initial abundance, in contrast to the linear scaling found in the absence of TES. The greater TES-induced fluctuations tend to promote species extinctions by bringing the abundances of species more frequently to the extinction threshold, thus decreasing species richness. Secondly, in competitive communities, non-linear averaging of TES-induced temporal fluctuations in interspecific competition strength (via Jensen’s inequality) can result in weaker interspecific competition on average, thus increasing species richness. However, this effect only dominates when the temporal correlation of environmental conditions is sufficiently short. If the correlation is too long, then this allows strong selection of the fittest species between infrequent changes in environmental conditions, which decreases species richness.

We end our review by discussing fruitful avenues for further research. These include a greater focus on interspecific interactions other than competition, for example consumption and mutualism. They also include examining eco-evolutionary feedbacks that critically shape the response of a species to TES, which may mitigate the effects of TES. Furthermore, there is much scope to explore how TES affects species richness in spatially explicit settings. Successful exploration of these new avenues requires development of new theory, collection of more community data, and better integration between theory and data.

Fung, T., J. Pande, N. M. Shnerb, J. P. O’Dwyer, R. A. Chisholm. 2023. Processes governing species richness in communities exposed to temporal environmental stochasticity: a review and synthesis of modelling approaches. Mathematical Biosciences 109131

Habitat destruction is one of the greatest threats to biodiversity worldwide, yet the effects of habitat loss and fragmentation on genetic diversity remain unclear. Tak has coauthored a new study published in Biological Conservation that provides new insights on this topic, using mathematical analyses and simulations of population genetic models. The study was led by Qian Tang, who is a Senior Research Fellow from Frank Rheindt’s Avian Evolution Lab at NUS.

The study found that for model bird species with different dispersal abilities, the amount of habitat lost had greater negative effects on population-level genetic diversity than did the degree of habitat fragmentation over timescales of a few hundred years. This was because the amount of habitat lost had the biggest negative impact on population sizes, which led to increases in genetic drift. The loss of genetic diversity manifested itself slowly over several decades, due to genetic drift acting slowly to remove alleles at the population level. This time lag provided a window of opportunity to rebuild populations and reduce the genetic extinction debt. However, loss of genetic diversity occurred more quickly at the subpopulation level due to spatial isolation of individuals and associated inbreeding, which accelerated loss of alleles in subpopulations via genetic drift. Species with higher dispersal abilities were more affected by habitat loss and fragmentation because they were more likely to disperse to areas with unsuitable habitat.  

The study also used modelling to examine a case study of how habitat destruction reduced genetic diversity in populations of malleefowl (Leipoa ocellata) in South Australia. The empirical trends in genetic diversity under different levels of habitat loss and fragmentation broadly matched those found for the model bird species. In addition, the modelling exercise revealed that small sample sizes blurred the effects of habitat loss and fragmentation, suggesting that caution should be taken when interpreting results from empirical studies with sparse sampling.

What are the impacts of tropical deforestation on biodiversity? To assess this, case studies are needed of tropical regions that have both a history of substantial deforestation and reliable biodiversity data. Singapore was almost entirely forested two hundred years ago but today less than 1% of the original primary forest remains today, with an additional ~20% of the landscape covered in lower quality secondary forest. Singapore also has an exceptionally detailed biodiversity record. Many species have gone extinct from Singapore, from the majestic tiger, the last of which was shot in the 1930s, to the humble epiphyte Hoya finlaysonii, which was last seen in 1837.

We compiled a comprehensive dataset of biodiversity in Singapore, comprising more than 50,000 individual records and representing more than 3,000 species and ten major taxonomic groups (mammals, birds, reptiles, amphibians, freshwater fishes, butterflies, bees, phasmids, decapod crustaceans, and plants). We developed novel statistical methods that account for “dark extinctions”, i.e., extinctions of undiscovered species, and estimated that 37% of Singapore’s species have gone extinct over the last two centuries. We extrapolated Singapore’s historical experience to a future scenario for the whole of Southeast Asia and estimated that around 18% of species would be lost regionally by 2100.

Our extinction estimates for both Singapore and future Southeast Asia are a factor of two lower than previous estimates, which we attribute to our improved statistical methods. However, extinctions in Singapore have been concentrated among charismatic species, including large mammals, forest-dependent birds, butterflies, and orchids. Thus, we speculate that if deforestation continues across the region, Southeast Asia may come to resemble a “tropical Europe”, where a large majority of species persist in a human-dominated landscape, but where many of the most charismatic species are absent. We recommend that future tropical conservation efforts focus on charismatic species such as tigers, elephants, rhinoceroses and orangutans, in line with the classic umbrella species approach.

The paper has just been published in PNAS. It represents the culmination of a decade of work by many people to assemble the comprehensive database of Singapore biodiversity records and develop the novel statistical methods needed to account for dark extinctions.

Several news outlets have reported on our work, including Mongabay, the Straits Times (see also this accompanying feature), and 联合早报 (Lianhe Zaobao).

Chisholm, R. A., N. P. Kristensen, F. E. Rheindt, K. Y. Chong, J. S. Ascher, K. K. P. Lim, P. K.
L. Ng, D. C. J. Yeo, R. Meier, H. H. Tan, X. Giam, Y. S. Yeoh, W. W. Seah, L. M. Berman, H. Z. Tan, K. R. Sadanandan, M. Theng, W. F. A. Jusoh, A. Jain, B. Huertas, D. J. X. Tan, A. C. R. Ng, A. Teo, Z. Yiwen, T. J. Y. Cho, and Y. C. K. Sin. 2023. Two centuries of biodiversity discovery and loss in Singapore. Proceedings of the National Academy of Sciences 120:e2309034120

Kong Fanhua, who has been a visiting student in our lab for the past two years, recently successfully defended her PhD at her home institution, East China Normal University, where she is advised by He Fangliang. The title of her thesis was “Effects of the competition–colonisation trade-off on species coexistence in forest plant communities”. During her time in our lab, she successfully published a chapter from thesis on neighbourhood diversity of pioneer versus shade-tolerant trees in Baishanzu Nature Reserve in China (see here). She also has in preparation a manuscript about tree diversity in gaps and non-gaps in the Barro Colorado Island forest in Panama. Congratulations, Fanhua!

Dengue is a mosquito-borne virus that infects hundreds of millions of people every year, mainly in tropical countries. Dengue occurs as four different variants (serotypes) whose frequencies exhibit cyclic behaviour, but the mechanisms underlying these cycles are incompletely understood. A new study in the Bulletin of Mathematical Biology by Tak, Ryan and Hannah Clapham from the School of Public Health sheds new light on this by analysing a mathematical model describing the epidemiology of multiple serotypes of dengue infecting a host population. We found that after infection of a host by one serotype and subsequent recovery, a temporary period of immunity to infection by other serotypes creates a time-lag in between infections and thereby generates asynchronous cycles of the different serotypes. Without such temporary cross-immunity, there can only be synchronous cycles.

We also explored conditions that increase the frequency of the asynchronous cycles, when such cycles occur. The frequency increases with the disease transmission rate because this leads to susceptible hosts being infected at a faster rate and hence more rapid formation of epidemics. Thus, management measures aimed at decreasing the disease transmission rate, such as fogging to eliminate mosquitoes, can reduce the frequency of epidemics. In addition, the frequency of asynchronous cycles increases with the birth rate of the host population, which introduces susceptible newborn individuals into the population at a greater rate and hence results in more rapid formation of epidemics. Thus, countries with higher birth rates are expected to exhibit faster cycling of dengue serotypes.

Fung, T., H. E. Clapham, and R. A. Chisholm. 2023. Temporary cross-immunity as a plausible driver of asynchronous cycles of dengue serotypes. Bulletin of Mathematical Biology 85:124

Tropical forests are biodiversity hotspots with dozens of tree species per hectare. The mechanisms maintaining such high levels of species richness have been studied for many decades. Previous studies have found that an important process is random changes in environmental conditions over time (temporal environmental stochasticity), and that simple parsimonious models that include this process can explain both static and dynamic patterns of tree diversity. In a previous paper led by Tak, we explored in detail how a changing temporal environment affects species diversity in a large-scale community. In a new paper just published in Journal of Ecology, we extended this work to a small-scale community that, in addition to being subject to a temporally varying environment, receives substantial immigration from a larger scale. This is important because tropical forest dynamics are often studied at small scales (e.g., 50 ha plots) where immigration is important.

Our main finding was that immigration substantially dampens the effect of temporal environmental variation on the species richness of an ecological community. We confirmed this with an application to the 50 ha forest plot on Barro Colorado Island, Panama (see figure below). Thus, while a varying environment may have big effects on population fluctuations of individual species, it does not, somewhat surprisingly, have a big effect on species richness. We expect that our findings will generalise to other tropical forest plots, which also typically receive many immigrants dispersed from surrounding areas, and likely many other ecological communities as well.

We reached our conclusions using novel technical methods for partitioning the effects of temporal environmental variation on species richness into components associated with population-level effects and interspecies-competition effects (see figure below).

The paper was a collaboration with Nao Takashina, who spent a few months in our lab in 2016 and is now an Assistant Professor at the University of Tokyo.

Fung, T., N. Takashina, and R. A. Chisholm. 2023. Mechanistic partitioning of species richness in diverse tropical forest tree communities with immigration and temporal environmental stochasticity. Journal of Ecology

Last week, Hisashi Ohtsuki from SOKENDAI (the Graduate University for Advanced Studies) in Japan visited the lab. Hisashi studies evolutionary game theory and has been collaborating with us over the past few years on related problems, resulting in a publication led by Nadiah Kristensen last year. During his visit, Hisashi gave the departmental colloquium, engaged with students and staff in the lab and the department more broadly, and worked on our ongoing collaborative projects.

As part of her PhD research in our lab, Deepthi Chimalakonda conducted six censuses of water birds over four years at 57 wetlands in the Warangal district of Telangana state in India (see map below), with the aim of understanding the forces that structure these bird communities. These wetlands are artificial habitats created by humans for irrigation and other purposes, but they are also valuable habitat for wildlife. Such artificial ecological communities are becoming increasingly common around the world as humans continue to modify natural environments, and it is crucial to understand their potential role in conserving biodiversity.

In her wetland data, Deepthi found that the wetland bird communities were highly dynamic, with substantial turnover in the species present from one census to the next. There was also substantial spatial turnover between neighbouring wetlands, even at distances of just 1 km. These results are consistent with the hypothesis that each wetland’s bird community is at a dynamic equilibrium with bird diversity arising from a balance between immigration and local extinction, as in classic island biogeography. The observed species abundance distributions and species–area relationships were also consistent with this hypothesis. Deepthi’s work has just been published in Diversity and Distributions. Deepthi is currently a post-doctoral research fellow at Nanyang Technology University in Singapore.

Chimalakonda, D. and R. A. Chisholm. 2023. Patterns of species diversity in a network of artificial islands. Diversity and Distributions (in press)

Last week Ryan attended a Gordon Research Conference on predictive ecology, held at Stonehill College just outside of Boston. The conference was motivated by a need for more quantitative predictions in ecology, in order to test our understanding of ecological systems and to aid conservation. Speakers came from a diverse array of disciplines, leading to many creative discussions. Ryan spoke about our lab’s work on testing predictions of mechanistic biodiversity models against data, including our recent experimental paper on intertidal communities. Several speakers discussed the recent success of machine learning at predicting ecological systems—surprisingly, in many cases these predictions are better than those based on traditional mechanistic models. Also of interest was the NEON Ecological Forecast Challenge, which encourages researchers to submit forecasts for a range of variables (e.g., beetle abundance, bird counts, and canopy leaf area) from the National Ecological Observatory Network (NEON), a network of 81 monitoring sites across the United States that began operation in 2019.

What determines the number of species that occur together in a given ecological community? One view is that species richness is driven mainly by characteristics of the local site, such as resource availability and habitat diversity. This is the niche perspective. Another view is that species richness is driven mainly by immigration from a larger region. This is the dispersal perspective. A long-standing goal of ecology is to reconcile these two perspectives. A classic unified theory predicts that dispersal assembly is observed only when immigration to a system is very low, and that niche assembly is observed in most other situations. A novel unified theory, developed by our lab (see here and here), predicts just the opposite: that niche assembly is observed only when immigration is very low, with dispersal assembly prevailing otherwise.

In a paper led by Lynette Loke and just published in Nature, we present the results of an experiment designed to test these two unified theories by systematically varying the rate of immigration and observing the response of species richness. Our focal system was intertidal animal communities on artificial seawalls in Singapore. The communities comprise crustaceans, gastropods, bivalves, tunicates and other creatures (the photo below shows lightning dove shells, Pictocolumbella ocellata). Each experimental unit was a concrete tile overlain by a stainless steel cage with polycarbonate sheet panels, into which we punched variable numbers of holes to allow different immigration rates across treatments.

The results were consistent with the novel unified theory. The number of species was roughly constant, at around five, for low-immigration treatments with one to five holes, but then began to increase substantially with the addition of further holes (see graph below). This implies that roughly five animal species can coexist via niche assembly in these seawall communities in the absence of substantial immigration, but in practical settings the communities will usually be in a dispersal-assembly regime with many more than five species, because natural immigration is higher than even in our highest-immigration experimental treatment. If these results can be generalised to other systems, it would follow that the species diversity we see small-scale ecological communities in the natural world is largely due to dispersal assembly rather than niche assembly.

This project is the most recent in a series of collaborations between Lynette and our lab (see here and here). Lynette is currently a post-doctoral researcher Macquarie University in Sydney. The experimental work for this project involved her going out alone into the field for a few days every fortnight for 12 months and navigating various challenges including pandemic social-distancing restrictions. The journal has also published a Research Briefing about the work.

Loke, L. and R. A. Chisholm. 2023. Unveiling the transition from niche to dispersal assembly in ecology. Nature