2022 Julie S. Denslow & Peter Ashton Prizes for the Outstanding Articles Published in Biotropica

Abstract

Every year Biotropica's Editorial Board selects papers in our journal as the recipients of the Julie S. Denslow and Peter Ashton Prizes, with which we honor the outstanding articles published in our journal in the previous calendar year. Criteria for selecting the papers to receive these awards include clarity of presentation, a strong basis in natural history, well-planned experimental or sampling design, and the novel insights gained into critical processes that influence the structure, functioning, or conservation of tropical systems. This year we were lucky to have a tie for the Ashton Prize, and hence, we celebrate two winners. Below the authors of the award-winning articles describe what motivated their studies and how they hope the work will inspire other researchers; we hope you enjoy these insights into the process that led to their discoveries and ask that you join the Editorial Board of Biotropica and The Association for Tropical Biology and Conservation in congratulating the 2022 recipients, whose articles appeared in the 2021 issues.

Chris Doughty

Doughty, C. E., Cheesman, A. W., Riutta, T., Thomson, E. R., Shenkin, A., Nottingham, A. T., Telford, E. M., Huaraca Huasco, W., Majalap, N., Arn, I. Y., Meir, P., & Malhi, Y. (2021). Predicting tropical tree mortality with leaf spectroscopy. Biotropica, 53, 581–595. https://doi.org/10.1111/btp.12901.

Sometimes science can be tricky. I do not mean complex or difficult, as it often can be. I mean sometimes it is difficult to decide whether or not the whole enterprise is justified. In our case, the difficulty was whether we should deliberately hasten the demise of a small area of Bornean forest (which was destined to be converted to a palm oil plantation) to better understand the mechanism of tropical tree death. Understanding the mechanism of tropical tree death is one of the most pressing questions in tropical forest ecology. However, contributing to the destruction of the forest, which as ecologists, we all love, was indeed tricky.

Prior to our work, the recent large-scale studies had found that tropical forest tree mortality had been increasing, but not uniformly across the globe.¹ We still have very little understanding of what causes tree mortality in the hyper-diverse tropics. Yet, as critical sources of carbon and biodiversity, it is more important than ever to understand what is causing the increase in mortality in tropical forests. In particular, developing remote-sensing techniques to predict possible future mortality would be key to addressing the question at even larger scales. The need to understand and predict tree mortality in tropical forests was clear, but did the ends justify the means?

Our project was informally led by Dr. Terhi Riutta of the University of Exeter, who had been working in Malaysian Borneo trying to understand how logging impacts tropical forest carbon cycling for many years.² This project was also working in the broader SAFE project which studies forest fragmentation.³ Both projects involved working with industrial partners who were modifying or destroying the forest. The logging projects are clearly needed and justified. Around 2015, Terhi learned that one of her long-term carbon cycling plots was to be converted to palm oil in the near future, so the trees were already doomed. We sensed a scientific opportunity.

Studies using girdling, the removal of living bark and phloem from trees to halt the transfer of sugars to below-ground roots, have been critical for understanding key ecosystem properties like how much CO₂ is released from soils due to root and mycorrhizal respiration.⁴ At the time of planning our experiment, there had been several large-scale temperate and boreal girdling studies, but as far as we were aware, no such studies in tropical forests. We also realized that by measuring as many aspects of the forest as possible, we could really begin to get new insight into helping us understand what causes tropical tree death (hydraulic limitations or carbon starvation) and possibly understand the consequences of tree death for soil processes below the ground, and even to detect it from the sky using remote sensing. However, this would mean we would have to kill the trees ourselves and not be dependent on the logging company project partners.

Trees do not scream and they do not feel pain, at least not in the manner of animals. Yet, the act of slicing through the phloem with the goal of killing the trees felt wrong. We knew the science we were doing was important and justified, but was it justified for those old (ish – the plot had been extensively logged before our study) trees? As ecologists, especially remote sensors or modelers, these ethical concerns were fairly new, but obviously, other scientists that use animals as research subjects had been facing such concerns for as long as science has been around.

We were determined to squeeze every last bit of data from the forest we had just committed to death. We cannot verify this, but these may have been the most measured trees in the history of tropical forest ecology. We measured total carbon and water fluxes (using eddy covariance), the release of carbon dioxide from soils and the dying root systems and their fungal partners (using infra-red gas analyzers), calculated net primary productivity and carbon use efficiency, documented changes in non-structural carbohydrates and wood morphology (using tree cores), looked at changes in leaf traits and photosynthesis (using sap flow sensors and monthly tree climbing campaigns), and finally leaf spectroscopy.

The main goal of our article was to understand the impact of forest death on canopy-scale processes and to test whether we can detect those changes using remote sensing (while this study tried to understand the impacts of tree death from the air, our other papers have considered the impacts of tree death on carbon cycling below the ground⁵). We found that leaf photosynthesis was surprisingly robust following the girdling and no evidence for phloem loading control of photosynthesis. Also, we found that the net leaf carbon balance (photosynthesis minus leaf respiration) became worse for leaves just prior to death. The most intriguing finding was our ability to predict tree death with leaf spectroscopy prior to tree death. This is critical as there are several new hyperspectral satellites that will come online over the next few years and there is a possibility of using these new satellites to predict regions that are especially stressed and susceptible to mortality.

When I try to explain what I do to my young kids, I generally stumble through too many details before I give up and say that I'm an Earth doctor. I generally use satellites, field data, and models to understand how tropical forests work and, here in particular, whether they are sick. As “Earth doctors”, tropical forest ecologists have nothing akin to the hippocratic oath and few oversights common to biologists studying vertebrate animals. In this case, I feel like the work was justified and receiving this award further makes me feel that we made the correct decision (Figures 1 and 2).

Samantha Tol

Tol, S. J., Jarvis, J. C., York, P. H., Congdon, B. C., & Coles, R. G. (2021). Mutualistic relationships in marine angiosperms: Enhanced germination of seeds by mega-herbivores. Biotropica, 53, 1535–1545. https://doi.org/10.1111/btp.13001.

Seagrass meadows in the tropics can grow to form lush underwater fields of swaying green leaves, creating a haven for an array of species. From brightly colored small fish, sea stars, and sea cucumbers to large majestic animals such as stingrays, sharks, sea turtles, and dugongs (dugongs are marine herbivorous mammals closely related to manatees, found in coastal waters of the southern hemisphere).

Seagrass habitats are vital for the health of coastlines, estuaries and coral reefs. They provide ecosystem services of sediment stabilization, water filtration and coral disease prevention. They are also vital for the survival of dugongs and an important diet for green sea turtles; both of which are listed on the IUCN (International Union for the Conservation of Nature) Red List of threatened species. The importance of seagrass to these marine mega-herbivores (green sea turtles and dugongs) is well established, yet the importance of marine mega-herbivores to seagrass is less known. This is what I sought to understand.

Before starting my PhD I worked for the Seagrass Ecology Team at James Cook University's TropWATER in Cairns, where we looked into the health of seagrass meadows in the Great Barrier Reef. One way we measured seagrass health was to look at the seed bank of seagrass species. Working with these microscopic seeds led to many a lunchtime discussion about the role dugongs and green sea turtles could play in dispersing seagrass seeds. Is it like the role birds play in spreading plant species in the Wet Tropics Rainforest adjacent to the Great Barrier Reef? We knew these marine mega herbivores consumed large quantities of seagrass daily and had a high chance of incidental ingestion of fruits and seeds. We also knew dugongs and turtles have co-evolved with seagrass over millions of years without the seagrass becoming unpalatable. This suggests a mutualistic relationship could be present. After much discussion, I turned this curiosity into my PhD project and began collecting dugong and green sea turtle feces to search for seagrass seeds.

My supervisor, Rob Coles, and I would venture out to known dugong and green sea turtle foraging grounds in the Great Barrier Reef Marine Park. Once we found where the animals were actively feeding, we would start collecting as many fecal deposits as we could; scooping them from the water's surface with a landing net. To ensure the seeds remained viable, but did not prematurely germinate, we kept the feces cool by storing them in the lab fridge before sorting them through a series of sieves to find the small seeds. Sieving the feces was, unfortunately, a predominately solo affair, due to the overwhelming aroma that the samples produced. Once we collected the seagrass seeds from the marine mega-herbivore feces, we placed them in a germination experiment to compare them to seeds we harvested off the plant. This involved using a microscope daily to observe each individual seed to see if it had begun to germinate.

We suspected the seeds passed by marine mega-herbivores would have a greater germination rate. Our previous research found that more than half of seeds passed through dugong and turtles had a split seed coat, which is known to hasten germination time. However, the results went beyond our expectations. We found the time to germinate was up to 60% faster and the germination success was up to four times greater than seeds collected directly off the plant. We suspect the enhanced germination rate is a combination of manual scarification (the splitting of the seed coat) and the sterilization of the seeds by stomach acid to remove any pathogens which can inhibit development. We hope that our research can assist in seagrass restoration projects in the future by mimicking what these marine mega-herbivores do to the seeds to improve restoration outcomes.

This research will always have a special place in my heart, from the beautiful moments in the field (like when a mother dugong and her calf surfaced right next to my boat), the hilarious memories of people finding out how dugong and green sea turtle feces smell, to the peculiar conversations that would arise due to my ‘unique’ aroma after a busy lab day. But mostly I'm heartened that this research has proved a fundamental ecological service for such important species – dugongs, green sea turtles, and seagrass equally (Figure 3).

Dominic A. Martin

Martin, D. A., Andriafanomezantsoa, R., Dröge, S., Osen, K., Rakotomalala, E., Wurz, A., Andrianarimisa, A., & Kreft, H. (2021). Bird diversity and endemism along a land-use gradient in Madagascar: The conservation value of vanilla agroforests. Biotropica, 53(1), 179–190. https://doi.org/10.1111/btp.12859.

When I first visited vanilla agroforests back in 2016, I was astonished by their diversity, their heterogeneity, and the skills of the people looking after them. Such complex agroforests are often hailed as an opportunity to reconcile production and conservation goals on the same land. Large shade trees provide a habitat for epiphytes, insects, and birds, while cash and subsistence crops may thrive underneath, profiting from ecosystem services like natural pest control. But for vanilla agroforests, the topic was literally unexplored until recently.

The large transdisciplinary “Diversity Turn in Land Use Science” project (@Diversity_Turn on Twitter) set out to change this in the most important global center of vanilla production in northeastern Madagascar. Overall, we were two Postdocs, 12 PhD researchers, and a dozen MSc students with corresponding supervisors based at the University of Göttingen, Germany, as well as at the University of Antananarivo and the Regional University Center of the SAVA Region, both in Madagascar. Together, we studied the drivers and consequences of land-use change in northeastern Madagascar, in particular vanilla production and trade.

Seven of us PhD students worked on ecosystem services and biodiversity within a common study design focusing on vanilla agroforests. These differ in land-use history: Some are established directly inside forests by replacing the natural understory with vanilla orchids. However, the majority of vanilla agroforests are established on fallow land that previously formed part of the shifting cultivation cycle for rice production. To put the vanilla agroforests into the wider land-use context, we additionally sampled the land-use types the agroforests originate from, fallow land, forest fragments, and old-growth forest. Among us PhD researchers, we then shared study design and logistics while focusing on different taxa and services. Being a lifelong birder, I joined efforts with my colleagues Rouvah Andriafanomezantsoa, Saskia Dröge, and Eric Rakotomalala counting birds across all 80 plots.

At first sight, the differences in species richness between land-use types were moderate – only old-growth forest stood out with a median diversity of 12 species on the plot level (neotropical ornithologists are probably rather unimpressed with this number, but for Madagascar it's decent!). During data collection, we already had the impression that endemic species – those only occurring in the country of Madagascar – appeared to be more abundant in forest fragments and old-growth forests compared to other land uses. With this hypothesis in mind, we separated all species depending on their endemism level into non-endemics, species-level endemics, genus-level endemics, subfamily-level endemics, and family-level endemics. The results were striking: family-level endemics only occurred in the old-growth forest, subfamily- and genus-level endemics were strongly overrepresented in old-growth forests and were represented as would be expected by chance alone in forest fragment and forest-derived vanilla agroforests. On open land-use types and fallow-derived vanilla agroforests, endemic species were underrepresented while non-endemics were strongly overrepresented. In sum, this suggested that higher-level endemic species are at particular risk of extinction under ongoing land-use change.

The data analysis in the paper is – admittedly – quite simple, not relying on complex estimates and models. But, I think that really makes the study more elegant; having a clear study design, standardized sampling effort across 80 plots, and the endemism levels as an additional unit of analysis allowed us to tell a coherent and well-supported story of the effect of land-use change on bird diversity in northeast Madagascar. We were able to present these results at the ATBC conference in Antananarivo – which was perfectly timed with our Diversity Turn project-sharing session in the 10 Malagasy study villages in 2019. It was a great honor to publish them in Biotropica. Thanks go to my co-authors and the editors for pushing this article – my first one as a first author.

Our article “Bird diversity and endemism along a land-use gradient in Madagascar: The conservation value of vanilla agroforests” was the start to a series of papers on biodiversity and ecosystem services in the same study design led by my fellow PhD colleagues. More recently, we also published two interdisciplinary synthesis papers bringing together data on seven taxa and multiple ecosystem services. However, if you ask me now what the greatest “legacy” of our project is, I would first highlight our 11 (soon 12!) PhD degrees and how we grew together as a team, how we built lasting friendships, how we all learned from each other over the last 6 years, and how we still ponder about plans for future research. Our WhatsApp chat is still one of the busiest I'm in (Figures 4 and 5).