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29 March 2022

Dozens of unidentified bat species likely live in Asia — and could host new viruses

Study suggests some 40% of horseshoe bats in the region have yet to be formally described.

Smriti Mallapaty

Smriti Mallapaty

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There could be more species of horseshoe bat than previously thought.Credit: Chien Lee/Nature Picture Library

A genomic analysis suggests that there are probably dozens of unknown species of horseshoe bats in southeast Asia1. Horseshoe bats (Rhinolophidae) are considered the reservoir of many zoonotic viruses — which jump from animals to people — including the close relatives of the viruses that caused severe acute respiratory syndrome and COVID-19. Identifying bat species correctly might help pinpoint geographical hotspots with a high risk of zoonotic disease, says Shi Zhengli, a virologist at the Wuhan Institute of Virology in China. “This work is important,” she says. The study was published in Frontiers in Ecology and Evolution on 29 March.Better identification of unknown bat species could also support the search for the origins of SARS-CoV-2 by narrowing down where to look for bats that may harbour close relatives of the virus, says study co-author Alice Hughes, a conservation biologist at the University of Hong Kong. The closest known relatives of SARS-CoV-2 have been found in Rhinolophus affinis bats in Yunnan province, in southwestern China2, and in three species of horseshoe bat in Laos3.Cryptic speciesHughes wanted to better understand the diversity of bats in southeast Asia and find standardized ways of identifying them. So she and her colleagues captured bats in southern China and southeast Asia between 2015 and 2020. They took measurements and photographs of the bats’ wings and noseleaf — “the funky set of tissue around their nose”, as Hughes describes it — and recorded their echolocation calls. They also collected a tiny bit of tissue from the bats’ wings to extract genetic data.To map the bats’ genetic diversity, the team used mitochondrial DNA sequences from 205 of their captured animals, and another 655 sequences from online databases — representing a total of 11 species of Rhinolophidae. As a general rule, the greater the difference between two bats’ genomes, the more likely the animals represent genetically distinct groups, and therefore different species.The researchers found that each of the 11 species were probably actually multiple species, possibly including dozens of hidden species across the whole sample. Hidden, or ‘cryptic’, species are animals that seem to belong to the same species but are actually genetically distinct. For example, the genetic diversity of Rhinolophus sinicus suggests that the group could be six separate species. Overall, they estimated that some 40% of the species in Asia have not been formally described.“It’s a sobering number, but not terribly surprising,” says Nancy Simmons, a curator at the American Museum of Natural History in New York City. Rhinolophid bats are a complex group and there has been only a limited sampling of the animals, she says.However, relying on mitochondrial DNA could mean that the number of hidden species is an overestimate. That is because mitochondrial DNA is inherited only from the mother, so could be missing important genetic information, says Simmons. Still, the study could lead to a burst of research into naming new bat species in the region, she says.Further evidenceThe findings corroborate other genetic research suggesting that there are many cryptic species in southeast Asia, says Charles Francis, a biologist at the Canadian Wildlife Service, Environment and Climate Change Canada, in Ottawa, who studies bats in the region. But, he says, the estimates are based on a small number of samples.Hughes’ team used the morphological and acoustic data to do a more detailed analysis of 190 bats found in southern China and Vietnam and found that it supported their finding that many species had not been identified in those regions. The study makes a strong argument for “the use of multiple lines of evidence when delineating species”, says Simmons.Hughes says her team also found that the flap of tissue just above the bats’ nostrils, called the sella, could be used to identify species without the need for genetic data. Gábor Csorba, a taxonomist at the Hungarian Natural History Museum in Budapest, says this means that hidden species could be identified without doing intrusive morphology studies or expensive DNA analyses.

doi: https://doi.org/10.1038/d41586-022-00776-2

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Our results show that the average diel activity patterns of Ae. aegypti populations in both Miami, FL and in Brownsville, TX were very similar; they both had two peaks, one in the early morning and the other in the evening, and the average host-seeking peaks are between 7:00 and 8:00 and between 19:00 and 20:00 (Fig. 4). Similar observations were previously reported by several investigators3,4,10,11,12 and the bimodal diel activity pattern is the most frequently reported for Ae. aegypti populations worldwide. However, variations between peak activity have been detected between populations. In East Africa, for instance, Trpis et al.3 reported peak activity at 7:00 and at 19:00, whereas McClelland10 reported peak activity two or three hours after sunrise (9:00 or 10:00) and one or two hours before sunset (17:00 or 16:00). Similarly, in the United States, Smith et al.7 observed a bimodal diel activity pattern for Ae. aegypti, but the evening peak was earlier, between 17:00 and 19:00. Despite these variations, the spacing of the peaks is similar in all these studies despite the fact that these studies were conducted in ecologically and climatically diverse locations.The activity patterns observed at site 3 in Brownsville (Fig. 2) and at site 1 in Miami (Fig. 1) were trimodal. In Brownsville, the trimodal activity peaks were between 6:30 and 7:30, 9:30 and 10:30, and 18:30 and 19:30 (Fig. 2), and in Miami the trimodal peaks were between 7:00 and 8:00, 9:00 and 10:00 and between 19:00 and 20:00 (Fig. 1). Interestingly, the timing of the third peak was similar in both Brownsville site 3 and Miami site 1 suggesting similar underlying factors despite geographic distance, different ecology, and different climate. Brownsville, Texas, is in the Lower Rio Grande Alluvial Floodplain ecoregion. The climate is humid subtropical and urbanization has removed most of the indigenous palm trees and floodplain forests vegetation (https://www.epa.gov/sites/default/files/2018-05/documents/brownsvilletx.pdf). Miami is in the Tropical Florida Ecoregion. Similar to Brownsville, Texas, urbanization and agriculture has replaced most of the indigenous Pine Rockland vegetation. Trimodal biting patterns for Ae. aegypti have been observed before in Trinidad by Chadee and Martinez4, but the middle peak was observed at 11:00 which is half an hour to an hour later than what we observed in Miami and Brownsville, respectively (Figs. 1 and 2). While the morning and evening peaks coincide with human outdoor activity, the middle peak occurs during high heat conditions and the factors that lead to this peak or its importance in the epidemiology of Ae. aegypti-borne arboviral diseases are currently not known. The studies by McClelland13 observed multiple activity peaks in an East African population of Ae. aegypti. The significance of the different activity patterns to the epidemiology of Ae. aegypti-borne arboviral diseases are currently unknown and we think they need more investigation especially since Ae. aegypti-borne arboviral infections have been rising in the recent past14,15.We observed that the host-seeking activity peaks were consistent between 5:45 and 7:30 and between 18:00 and 20:45 (Figs. 1 and 2). These observations are important in planning and conducting control operations directed at the adult Ae. aegypti female populations. During the 2016 Zika outbreak, there was no specific information on the host-seeking activity patterns of Ae. aegypti in Miami Dade County and the adulticide treatment implemented as part of an integrated approach targeted the morning activity16. The integrated approach effectively reduced the vector population and interrupted the transmission of the Zika virus; however, it highlighted the need for site-specific information on the diel activity patterns of Ae. aegypti in Miami Dade County in particular and the CONUS in general. There have been sporadic Ae. aegypti-borne arboviral disease outbreaks in Miami Dade County, FL and the city of Brownsville, TX17,18,19,20,21, in the future we will be better prepared to conduct effective adulticide applications with the current knowledge of the diel activity patterns of Ae. aegypti in these areas. Furthermore, we are now better equipped to educate the public on how to minimize exposure to Ae. aegypti-borne arboviral diseases by avoiding outdoor activities during peak biting activity periods.In our studies, we used BG-Sentinel 2 traps and monitored them every hour, twenty-four hours a day over 96 h, a method with some similarities to that used by Smith et al.7. In the past, diel biting activity studies were carried out using human landing catches following the methods primarily established by Haddow22. To our knowledge, only two studies have previously used sampling procedures not based on human landing catches to study the biting activity patterns of Ae. aegypti; the study by Ortega-Lopez et al.6 used mosquito electrocuting traps, and the study by Smith et al.7 used a mechanical rotator mosquito trap. In the present study, the use of BG-Sentinel II traps had the advantage that it was specifically designed to capture female host-seeking Ae. aegypti8,9. In addition, attached BG-Counter devices can keep track of the number of mosquitoes captured per specified unit time and environmental conditions, and store the information in a cloud server. However, the BG-Sentinel 2 traps collected a wide variety of mosquito species, (Table 1), and to keep track of specific species captured each hour, we had to monitor them every hour.Overall, we present data on the diel activity of Ae. aegypti populations in two cities in the southern United States. In both cities the activity patterns were bimodal; there were peaks of activity in the mornings and the evenings. The significance of these observations is that these peaks can be targeted to improve the effectiveness of adulticide treatments aimed at controlling Ae. aegypti adult populations. Using BG-Sentinel 2 traps eliminates individual variations associated with human landing catches and the associated danger of infections from wild mosquitoes especially during ongoing outbreaks. More

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This picture was taken at night in the coastal community of Dakenggu in Yilan County, which is just southeast of Taipei in Taiwan. I’m on the left, working with two other researchers to measure the body size of a red-clawed crab (Chiromantes haematocheir).An old man from the local community told me that years ago, during the breeding season, you could barely cross the road because of all the crabs. He said nobody knows where they all went. They’re an important memory for the local people, and part of the culture here.Habitat loss — especially resulting from the widespread use of concrete — seems to be driving the decline. I’m working with local people to create rocky microhabitats and artificial wetlands for the red-clawed crabs to live in. They’re important scavengers — eating dead animals and other organic matter, breaking it down and playing a key part in the nutrient cycle.Small organisms need our help — they can’t stand up for themselves. But in Taiwan, a lot of people think a coastal villa is more important than a few crabs. Corporations want to build luxury developments in our national parks, and authorities often approve them. I’ve seen so many intact habitats destroyed or covered in concrete.Crabs caught my interest because they were frequent visitors to my dormitory. National Sun Yat-sen University in Kaohsiung sits in a coastal buffer zone between a mountain and the ocean, and land hermit crabs (Coenobita cavipes) have to scurry through it on their way to breed.After watching habitat after habitat destroyed by overdevelopment, I’ve realized that just doing the science is not enough. It doesn’t matter how many papers you publish: you need to connect with people through education and communication. That’s why I decided to do my PhD in social science. And it’s why I believe conservation will be my life’s work.

Nature 603, 962 (2022)
doi: https://doi.org/10.1038/d41586-022-00810-3

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