The large gap between described and estimated species is referred to as the Linnean shortfall in conservation biology or, specifically for fungi, fungal dark matter. My group studies fungi, which are largely neglected in biodiversity monitoring programs compared to plants and animals—due to their cryptic nature, bias to large fruitbodies (which means microfungi, making out the majority of fungi, are ignored), and a lack of resources and personnel. The fungal kingdom is estimated at 2.5 million species but only 145,000 species have been formally described. Some of this dark matter has been detected through high-throughput sequencing while some is estimated based on modeling studies.
My group focuses on community ecology. I initiated a project focusing on an obligate multitrophic symbiosis of bats, parasitic bat-associated flies, and parasitic fly-associated fungi that we will develop into a worldwide project as anew model system to ask community ecology questions in similar complex multi-species systems. We will use a multidisciplinary approach to describe new diversity in multiple kingdoms (fungi, flies, bats), test whether their diversity patterns follow the latitudinal gradient hypothesis, unravel patterns of host specificity at multiple levels and across ecosystems, build a global multitrophic traits database, and analyze how biotic and abiotic factors affect parasitism across different trophic levels. The following specific questions are asked: (1) What is the diversity in these obligate interaction networks? (2) How is parasitism at different trophic levels affected by biotic and abiotic stresses? (3) Is host health related to infection status and if yes, how? And finally: (4) What is the risk for dark extinctions if one partner is threatened?
Objective 1: Describe and analyze the diversity of the three levels of interactions, increase specimen and DNA-sequence data for global systematics research.
Parasites have evolved as often as, if not more often than, other types of organisms; they alter food webs either indirectly (by enhancing transmission rate and altering life-history traits of hosts) or directly (by changing the food chain length, number of links, and energy flows). Possibly as many as 75% of food web links involve a parasitic partner. Parasitism of parasites (or hyperparasitism) is common in nature but only few examples of such obligate multitrophic host–parasite–parasite networks have been well studied. The study system proposed here involves bats, their blood-sucking ectoparasitic flies, and fungal ectoparasites of the flies. This is an exciting system because (1) it can be found around the world, (2) standard sampling techniques can be used to allow for statistically significant comparisons among locations and regions, (3) there is great potential to involve other partners (e.g., bat-and bat roost-associated viruses), and (4) it has only been explored descriptively, with a lot of questions remaining.
Distributions of macro-organisms typically follow a latitudinal gradient; their diversity is negatively linked to increasing latitude, known as the latitudinal gradient hypothesis. In contrast, distributions of microorganisms such as fungi, which produce propagules that are microscopic in size, are often perceived as cosmopolitan. However, lack of data from understudied regions –such as tropical regions and most of the African continent– has not allowed for testing of this hypothesis when it comes to bat flies and fungi. Recent studies based on environmental DNA, although plagued by lack of comparative data from tropical versus temperate regions, found that fungal diversity in some ecological guilds may follow a reverse latitudinal gradient.
Recently, an integrative taxonomy approach has been proposed—this is the delimitation and subsequent formal description of new species based on multiple, independent lines of evidence including morphology, geometric morphometrics, molecular phylogenetics, sequence-based species delimitation methods, and geography. While bats are the second-most diverse group of mammals, new species remain undiscovered in understudied areas of the world. Bat-associated parasitic flies and fly-associated parasitic microfungi both are poorly studied groups. Based on preliminary phylogenetic study, at least a dozen bat flies from tropical America await formal description. And I and my students have described more than half of bat fly-associated microfungi currently known, with many more estimated to remain undiscovered to date. A global-in-scale, standardized sampling approach will allow to describe the multitrophic diversity captured in these networks.
Objective 2: Evaluate the sensitivity of obligate multitrophic networks to disturbance and climate change
Bats respond to habitat modifications in different ways, including behaviorally, physiologically, and functionally. Responses are highly species and assemblage specific. However, how their associated parasites respond remains poorly understood. Habitat disturbance also affects the abundance of parasitic flies on bats, although based on the available data the direction of this correlation is species-specific. If bat flies are affected by habitat disturbance, then their associated fungi are expected to be affected as well. Elevated population densities of bat flies increase opportunities for transmission of fungal propagules. Preliminary data on the influence of climate factors on parasitism of both bats by flies and flies by fungi are ambiguous and geographically biased. A community ecology approach has never before been applied to any multitrophic symbiosis system and our proposed research will reveal for the first time how multiple levels of interactions respond to biotic and abiotic stresses. Our global-in-scale, standardized sampling approach will involve repeated monitoring in selected sites to evaluate the effect of abiotic factors over time.
Previous work has shown that bat host behavior and sociality affect parasitism (at a single trophic level). Hence, we will also study the most important biotic factors relevant to bats: their roosting behavior, roost switching behavior, cluster density, and grooming behavior. Bats vary greatly in their roosting requirements and social structure. Some bat species have highly specialized roosting needs while others may be more generalist. Roosts include foliage (ephemeral), tree cavities, cliffs, mines, and caves (permanent). It was shown that the intensity and prevalence of bat flies on bats increase with increasing roost permanence, but these results were done on a geographically limited dataset (only including specimens from Venezuela). The effect of roosting behavior on parasitism by bat flies on a larger geographic scale and on parasitism of bat flies by fungi has never before been studied.
Philopatry has been defined as faithfulness to the natal group or site and it is a behavior particularly associated with bats, due to a combination of their longevity (and thus cumulative site knowledge) and gregarious nature (and resultant information sharing). However, many bat roosts are ephemeral in structure, forcing regular relocation. “Roost-switching” is the behavior of relocating from one roosting place to another, hypothesized to control ectoparasite load. Cave-dwelling bats have different population dynamics compared to tree-roosting bats, due to the fact that caves present stable features affording high degrees of philopatry. Caves also pose stable environments for bat flies (it is safer to deposit larvae in caves than in ephemeral roosts). Finally, caves present opportunities to study bat behaviors that may affect parasitism: cluster density and grooming. Cluster density has been shown to affect parasitism but data are patchy. For example, Myotis myotis has higher parasite intensity when roosting in clusters than when roosting alone. Cluster size also has thermodynamic impact on the roost, the colony, individual members, and likely their ectoparasites. Host grooming is considered to be the main cause of ectoparasite mortality in general, but bat flies have adaptations that make them resistant to grooming (combs for attachment, highly mobile). How grooming affects parasitism across trophic levels, in which direction, and whether patterns are similar across bat species has not yet been studied.
Objective 3: Host health in relation to infection and host conservation through the detection of infectious agents in its associated parasites.
We will first assess host health due to infection both in bats (primary hosts) and bat-associated flies (secondary hosts). This will be done by analyzing nutrient stress in bats based on blood samples and in bat flies based on hemolymph samples. Second, we will test a non-invasive approach to testing whether bats are host to infectious agents. Bats are important hosts of many diseases and pathogens. Surveillance studies are often invasive, including collection of bat voucher specimens, blood sampling, wing punching, etc. We propose to use hematophagous (blood-sucking) bat flies as a non-invasive alternative. We will use both bats and bat flies for the detection of pathogens using molecular methods to evaluate the efficacy of this proposed method. We will also test correlations that may exist between the presence of infectious agents in bat flies and infection with parasitic fungi. The detection of pathogens in bat blood and ectoparasitic flies raises concerns for them being respectively reservoirs and carriers for various pathogens some of which may be relevant for humans or have zoonotic potential. Our global sampling strategy will allow for robust comparison of pathogens across locations and regions.
Objective 4: What is the extinction risk of the other partners of the obligate multitrophic symbiosis if one partner goes extinct?
The Scottian shortfall was recently described to quantify the lack of IUCN Red List assessments in a given organismal group. While for bats this shortfall is very small (the vast majority of bats having received a Red List assessment), it is huge for both bat flies and microfungi. Based on our standardized monitoring schemas, we will make Red List assessments for species in these understudied groups. However, conservation assessments do not take interactions into consideration. Assessments are made species by species individually. But in a world driven by interactions (many parasitic) there is an urgent need to evaluate interactions in conservation assessments. For example, a species with Least Concern [LC] status may be driven to extinction very quickly if its host has disappeared. We will perform a literature review to quantify the frequency of unique (one to one) host–parasite relationships for all mammals and link this information to the respective Red List status of both host and parasite. We will take this exercise further by performing another literature review quantifying unique host–parasite relationships for all bat-associated parasites and their parasites. If a host goes extinct, its uniquely associated parasites will also inevitably go extinct, as well as the parasites uniquely associated to those. This is a trickle-down effect (which I will term “dark cascades”) that is currently not considered in conservation practices.
This objective will (1) improve knowledge of the importance of obligate multitrophic symbioses, (2) result in the very first IUCN Red List assessments for bat flies and Laboulbeniales microfungi, both highly understudied organismal groups with currently not a single assessment on the IUCN Red List, and (3) involve the potential identification of areas for designation as Alliance for Zero Extinction (AZE) sites. AZE aims to prevent extinctions by identifying and safeguarding key sites as the last remaining refuge of one or more Endangered or Critically Endangered species. All AZE sites adhere to three criteria: endangerment (must contain at least one Endangered [EN] or Critically Endangered [CR] species), irreplaceability (should be the only area where an EN or CR species occurs, or contain >95% of the known population of the EN or CR species), and discreteness (character of habitats, biological communities, and/or management issues in the site must have more in common with each other than with those in adjacent areas). The data from this project will allow answering the question of how organisms involved in obligate multitrophic symbioses could be protected.
