2024 Julie S Denslow &amp; Peter Ashton Prizes for the outstanding articles published in <i>Biotropica</i>

Every year, Biotropica's Editorial Board selects outstanding 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. 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 2024 recipients, whose articles appeared in the 2023 issues. Margarita Lampo Margarita Lampo, Señaris, C., González, K., & Ballestas, O. (2023). Smaller size of harlequin toads from populations long exposed to the fungal disease chytridiomycosis. Biotropica, 55, 699–705. https://doi.org/10.1111/btp.13220 Harlequin toads are renowned for their vivid colors and their hand-signaling behavior, reminiscent of mimes (Figure 1). Despite their uniqueness, they are among the most threatened groups of amphibians. Most species succumbed to chytridiomycosis, a fungal disease that decimated amphibian populations worldwide in the 1980s and 1990s. The Rancho Grande harlequin toad (Atelopus cruciger) is one of the few species that reappeared, but its range shrank from 17,000 to 80 km2. Despite efforts to locate these frogs in their former territories in the northern mountains of Venezuela, only two populations, both at low elevations, are currently known. Understanding how post-epidemic populations persist in the presence of the fungus—which remains deadly to harlequin toads—has been the central focus of our team's long-term research and monitoring program. We began visiting the streams where the Rancho Grande harlequin toad lives shortly after its reappearance in 2003, following its disappearance in 1986. For nearly 8 years, Celsi Señaris, Onil Ballestas, Katiuska González, occasional volunteers, and I collected monthly data on body size, weight, infection status, and habitat use of each toad in these post-epidemic populations (Figure 2a). Celsi, who managed the herpetological collection for many years at the Museo de Historia Natural La Salle (MHNLS), noticed that the frogs we were observing in the field appeared to be smaller than those in the collection (Figure 2b). This observation prompted us to examine nearly 700 frogs collected before their disappearance in 1986 (i.e., pre-epidemic times) from this and three other herpetological collections. Our findings supported Celsi's hunch: Males in persisting populations were 7% smaller, and females were 15% smaller than their pre-epidemic counterparts. This information we started piecing together the complex puzzle of how these harlequin toads persist despite the presence of the lethal fungus. Why are post-epidemic harlequin toads smaller than pre-epidemic ones? Growth and reproduction in amphibians tend to be mutually exclusive: You either grow or breed, but there is not enough energy to do both simultaneously. Frogs that grow larger delay reproduction, which can carry benefits, as larger females produce more eggs. However, life in the wild is a gamble. For harlequin toads, contracting the fungus is a death sentence, and the risk intensifies over time. In this evolutionary “game,” reproducing early rather than late becomes the best bet, a strategy that will be favored by nature's master croupier, natural selection. Yet, not all players can hold winning cards. Since metabolic rates decrease with altitude, we hypothesize that harlequin toads at higher elevations may struggle to reach the minimum size required to reproduce before the first breeding season is over, forcing them to wait until the second. As a result, the “early-breeding strategy” may only be viable for toads living in lower elevations. How do smaller and precocious toads enhance the persistence of populations infected with the fungus? Shifts in a species' life history can affect the population's ability to withstand and recover from disturbances. If turnover rates are high, the loss of animals can be rapidly compensated by the recruitment of new individuals. Capture–recapture studies and mathematical modeling carried out by our team suggest that rapid recruitment of juveniles is the key to the persistence of the Rancho Grande harlequin toad, as it offsets the losses caused by fungal infection. Advancing the breeding schedule one season will necessarily shorten the generation time and increase the population turnover rates, enhancing resilience to ecological perturbations, such as diseases. Harlequin toads will need more than just our knowledge to secure their future. With only two remaining subpopulations, confined to a shrinking range and under constant threat from a deadly fungus, the Rancho Grande harlequin toad is teetering on the edge of extinction. The possibility of losing this species forever is not just a statistic for us—it is personal. In 2022, with a mix of hope and urgency, our team at the Centro de Reproducción e Investigación para Arlequines (CRIA) launched an ex situ program. Our goal was clear: safeguard the species' gene pool and bring these remarkable toads back to their historical range (Figure 2c). So far, we have successfully produced over 500 harlequin toads in captivity, and now, after years of dedicated effort, we are gearing up to release around 200 juveniles and adults in early 2025. The ultimate vision? To see thriving populations of harlequin toads that no longer rely on human intervention. We dream of the day when the vibrant yellow and black patterns of these toads once again light up the streams of the Venezuelan mountains, as they did before. Mauro Rivas-Ferreiro Mauro Rivas-Ferreiro, Skarha, S. M., Rakotonasolo, F., Suz, L. M., & Dentinger, B. T. M. (2023). DNA-based fungal diversity in Madagascar and arrival of the ectomycorrhizal fungi to the island. Biotropica, 55, 954–968. https://doi.org/10.1111/btp.13245 The study of fungal diversity in Madagascar has a long but fragmented history, with most of the early research dating back to the colonial period (until the late 1940s). During that time, tropical mycology in the colonies primarily focused on crop pathogens, and very few fungal specimens were collected or preserved in public collections. It was not until the 1990s that a series of opportunistic field surveys began to document the diversity of certain genera, such as Marasmius, Cantharellus, and Russula. These surveys facilitated the description of new species and underscored Madagascar's unique yet vastly underexplored fungal diversity, which remains under constant threat. Our project began in February 2012, when Dr. Bryn Dentinger, then Senior Researcher in Mycology at the Royal Botanic Gardens Kew, conducted fieldwork in Madagascar with the help of Dr. Franck Rakotonasolo. Bryn was looking to explore the fungal diversity in the island, so he collected both fungal sporocarps (mushrooms) and roots from trees known to form ectomycorrhizal symbioses with fungi, so he could account for both the aboveground and belowground diversity of fungi. A second expedition followed in November of the same year, this time collecting only sporocarps. In March 2014, he returned with Dr. Paul Cannon and Dr. Laura M. Suz, also from RBG Kew, to collect both sporocarps and ectomycorrhizal roots. Finally, during her MSc field trip module in February 2017, Shannon Skarha also went to Madagascar and collected roots from both endemic and non-native ectomycorrhizal trees. By 2020, I had joined the MSc program at RBG Kew and was keen to work on ectomycorrhizal fungi. I contacted Laura and she invited me to work with all the genetic and ecological data accumulated over the years by all of these researchers. I gladly took on the opportunity to work with tropical fungi, particularly because after my MSc I wanted to pursue a PhD in mycology; a year later, I did start my PhD journey, which allowed me to continue working on this Malagasy fungi project until it was published. Our initial goal with this study was to place Malagasy fungi within the broader context of global fungal diversity. For that, we compiled several different genetic datasets and compared them with our Malagasy data. Remarkably, our opportunistic surveys accounted for 10% of the known fungal diversity of Madagascar. We also found out that the pattern of endemicity shown in Malagasy plants and animals seems to hold true for fungi as well, with around 60% of all fungal species and 81% of the ectomycorrhizal species being only ever found in Madagascar, nowhere else in the world. Building on these findings, we sought to test the hypothesis of a Gondwanan origin of ectomycorrhizal symbiosis in Madagascar. We focused on three ectomycorrhizal families—Amanitaceae, Boletaceae, and Russulaceae—and used a molecular dating approach to assess their arrival on the island. While the results varied, our analyses suggested that all Malagasy ectomycorrhizal species arrived via long-distance dispersal, well after the separation of the India–Madagascar landmass (88 million years ago). Almost a year after our study was published in BIOTROPICA, I had the opportunity to conduct my own fieldwork in Madagascar. With the support of the Bentham–Moxon Trust and the Emily Holmes Memorial Scholarships, I was able to conduct fieldwork in Madagascar with my now PhD supervisor Laura M. Suz, with Malagasy mycologist Anna B. Ralaiveloarisoa, along with Spanish mycologists Rodrigo Márquez-Sanz, Ibai Olariaga, and Sergio Pérez-Gorjón. During the 2 weeks of fieldwork, we collected close to 700 fungal sporocarps, as well as 120 root samples. This massive amount of data will help us to not only describe new fungal species but also start understanding patterns of distribution, evolution, and diversity of the Funga of Madagascar. Additionally, these data will refine the findings from our previous study and may reveal patterns of endemism in other fungal guilds, such as saprotrophic fungi. Madagascar's fungal diversity is under increasing threat from deforestation, fires, and large-scale mining operations. Time is critical if we are to document and conserve this unique mycobiota. Sustained funding and support for taxonomic research on the island are essential to achieving this goal before these species—and the ecosystems they support—are lost (Figures 3-5).

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Publication Details

Journal
Biotropica
Published
2024-11-01
DOI
https://doi.org/10.1111/btp.13396
Primary Topic
Metabolomics and Mass Spectrometry Studies
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article
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0.00
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article

2024 Julie S Denslow & Peter Ashton Prizes for the outstanding articles published in Biotropica

Jennifer S. Powers
Biotropica
Metabolomics and Mass Spectrometry Studies
article

2024 Julie S Denslow & Peter Ashton Prizes for the outstanding articles published in Biotropica

Jennifer S. Powers
article en

Abstract

Every year, Biotropica's Editorial Board selects outstanding 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. 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 2024 recipients, whose articles appeared in the 2023 issues. Margarita Lampo Margarita Lampo, Señaris, C., González, K., & Ballestas, O. (2023). Smaller size of harlequin toads from populations long exposed to the fungal disease chytridiomycosis. Biotropica, 55, 699–705. https://doi.org/10.1111/btp.13220 Harlequin toads are renowned for their vivid colors and their hand-signaling behavior, reminiscent of mimes (Figure 1). Despite their uniqueness, they are among the most threatened groups of amphibians. Most species succumbed to chytridiomycosis, a fungal disease that decimated amphibian populations worldwide in the 1980s and 1990s. The Rancho Grande harlequin toad (Atelopus cruciger) is one of the few species that reappeared, but its range shrank from 17,000 to 80 km2. Despite efforts to locate these frogs in their former territories in the northern mountains of Venezuela, only two populations, both at low elevations, are currently known. Understanding how post-epidemic populations persist in the presence of the fungus—which remains deadly to harlequin toads—has been the central focus of our team's long-term research and monitoring program. We began visiting the streams where the Rancho Grande harlequin toad lives shortly after its reappearance in 2003, following its disappearance in 1986. For nearly 8 years, Celsi Señaris, Onil Ballestas, Katiuska González, occasional volunteers, and I collected monthly data on body size, weight, infection status, and habitat use of each toad in these post-epidemic populations (Figure 2a). Celsi, who managed the herpetological collection for many years at the Museo de Historia Natural La Salle (MHNLS), noticed that the frogs we were observing in the field appeared to be smaller than those in the collection (Figure 2b). This observation prompted us to examine nearly 700 frogs collected before their disappearance in 1986 (i.e., pre-epidemic times) from this and three other herpetological collections. Our findings supported Celsi's hunch: Males in persisting populations were 7% smaller, and females were 15% smaller than their pre-epidemic counterparts. This information we started piecing together the complex puzzle of how these harlequin toads persist despite the presence of the lethal fungus. Why are post-epidemic harlequin toads smaller than pre-epidemic ones? Growth and reproduction in amphibians tend to be mutually exclusive: You either grow or breed, but there is not enough energy to do both simultaneously. Frogs that grow larger delay reproduction, which can carry benefits, as larger females produce more eggs. However, life in the wild is a gamble. For harlequin toads, contracting the fungus is a death sentence, and the risk intensifies over time. In this evolutionary “game,” reproducing early rather than late becomes the best bet, a strategy that will be favored by nature's master croupier, natural selection. Yet, not all players can hold winning cards. Since metabolic rates decrease with altitude, we hypothesize that harlequin toads at higher elevations may struggle to reach the minimum size required to reproduce before the first breeding season is over, forcing them to wait until the second. As a result, the “early-breeding strategy” may only be viable for toads living in lower elevations. How do smaller and precocious toads enhance the persistence of populations infected with the fungus? Shifts in a species' life history can affect the population's ability to withstand and recover from disturbances. If turnover rates are high, the loss of animals can be rapidly compensated by the recruitment of new individuals. Capture–recapture studies and mathematical modeling carried out by our team suggest that rapid recruitment of juveniles is the key to the persistence of the Rancho Grande harlequin toad, as it offsets the losses caused by fungal infection. Advancing the breeding schedule one season will necessarily shorten the generation time and increase the population turnover rates, enhancing resilience to ecological perturbations, such as diseases. Harlequin toads will need more than just our knowledge to secure their future. With only two remaining subpopulations, confined to a shrinking range and under constant threat from a deadly fungus, the Rancho Grande harlequin toad is teetering on the edge of extinction. The possibility of losing this species forever is not just a statistic for us—it is personal. In 2022, with a mix of hope and urgency, our team at the Centro de Reproducción e Investigación para Arlequines (CRIA) launched an ex situ program. Our goal was clear: safeguard the species' gene pool and bring these remarkable toads back to their historical range (Figure 2c). So far, we have successfully produced over 500 harlequin toads in captivity, and now, after years of dedicated effort, we are gearing up to release around 200 juveniles and adults in early 2025. The ultimate vision? To see thriving populations of harlequin toads that no longer rely on human intervention. We dream of the day when the vibrant yellow and black patterns of these toads once again light up the streams of the Venezuelan mountains, as they did before. Mauro Rivas-Ferreiro Mauro Rivas-Ferreiro, Skarha, S. M., Rakotonasolo, F., Suz, L. M., & Dentinger, B. T. M. (2023). DNA-based fungal diversity in Madagascar and arrival of the ectomycorrhizal fungi to the island. Biotropica, 55, 954–968. https://doi.org/10.1111/btp.13245 The study of fungal diversity in Madagascar has a long but fragmented history, with most of the early research dating back to the colonial period (until the late 1940s). During that time, tropical mycology in the colonies primarily focused on crop pathogens, and very few fungal specimens were collected or preserved in public collections. It was not until the 1990s that a series of opportunistic field surveys began to document the diversity of certain genera, such as Marasmius, Cantharellus, and Russula. These surveys facilitated the description of new species and underscored Madagascar's unique yet vastly underexplored fungal diversity, which remains under constant threat. Our project began in February 2012, when Dr. Bryn Dentinger, then Senior Researcher in Mycology at the Royal Botanic Gardens Kew, conducted fieldwork in Madagascar with the help of Dr. Franck Rakotonasolo. Bryn was looking to explore the fungal diversity in the island, so he collected both fungal sporocarps (mushrooms) and roots from trees known to form ectomycorrhizal symbioses with fungi, so he could account for both the aboveground and belowground diversity of fungi. A second expedition followed in November of the same year, this time collecting only sporocarps. In March 2014, he returned with Dr. Paul Cannon and Dr. Laura M. Suz, also from RBG Kew, to collect both sporocarps and ectomycorrhizal roots. Finally, during her MSc field trip module in February 2017, Shannon Skarha also went to Madagascar and collected roots from both endemic and non-native ectomycorrhizal trees. By 2020, I had joined the MSc program at RBG Kew and was keen to work on ectomycorrhizal fungi. I contacted Laura and she invited me to work with all the genetic and ecological data accumulated over the years by all of these researchers. I gladly took on the opportunity to work with tropical fungi, particularly because after my MSc I wanted to pursue a PhD in mycology; a year later, I did start my PhD journey, which allowed me to continue working on this Malagasy fungi project until it was published. Our initial goal with this study was to place Malagasy fungi within the broader context of global fungal diversity. For that, we compiled several different genetic datasets and compared them with our Malagasy data. Remarkably, our opportunistic surveys accounted for 10% of the known fungal diversity of Madagascar. We also found out that the pattern of endemicity shown in Malagasy plants and animals seems to hold true for fungi as well, with around 60% of all fungal species and 81% of the ectomycorrhizal species being only ever found in Madagascar, nowhere else in the world. Building on these findings, we sought to test the hypothesis of a Gondwanan origin of ectomycorrhizal symbiosis in Madagascar. We focused on three ectomycorrhizal families—Amanitaceae, Boletaceae, and Russulaceae—and used a molecular dating approach to assess their arrival on the island. While the results varied, our analyses suggested that all Malagasy ectomycorrhizal species arrived via long-distance dispersal, well after the separation of the India–Madagascar landmass (88 million years ago). Almost a year after our study was published in BIOTROPICA, I had the opportunity to conduct my own fieldwork in Madagascar. With the support of the Bentham–Moxon Trust and the Emily Holmes Memorial Scholarships, I was able to conduct fieldwork in Madagascar with my now PhD supervisor Laura M. Suz, with Malagasy mycologist Anna B. Ralaiveloarisoa, along with Spanish mycologists Rodrigo Márquez-Sanz, Ibai Olariaga, and Sergio Pérez-Gorjón. During the 2 weeks of fieldwork, we collected close to 700 fungal sporocarps, as well as 120 root samples. This massive amount of data will help us to not only describe new fungal species but also start understanding patterns of distribution, evolution, and diversity of the Funga of Madagascar. Additionally, these data will refine the findings from our previous study and may reveal patterns of endemism in other fungal guilds, such as saprotrophic fungi. Madagascar's fungal diversity is under increasing threat from deforestation, fires, and large-scale mining operations. Time is critical if we are to document and conserve this unique mycobiota. Sustained funding and support for taxonomic research on the island are essential to achieving this goal before these species—and the ecosystems they support—are lost (Figures 3-5).

BiotropicaVol. 56(6)
University of Minnesota (US)
Openalex Percentile: Top 82%
Metabolomics and Mass Spectrometry Studies
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