Biodiversity Data Journal :
Data Paper (Biosciences)
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Corresponding author: Winifred F Frick (wfrick@batcon.org)
Academic editor: Miguel Camacho Sanchez
Received: 09 Mar 2022 | Accepted: 10 May 2022 | Published: 19 May 2022
© 2022 Jon Flanders, Winifred Frick, Julius Nziza, Olivier Nsengimana, Prince Kaleme, Marie Claire Dusabe, Innocent Ndikubwimana, Innocent Twizeyimana, Sospeter Kibiwot, Pierre Ntihemuka, Tina Cheng, Richard Muvunyi, Paul Webala
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Flanders J, Frick WF, Nziza J, Nsengimana O, Kaleme P, Dusabe MC, Ndikubwimana I, Twizeyimana I, Kibiwot S, Ntihemuka P, Cheng TL, Muvunyi R, Webala P (2022) Rediscovery of the critically endangered Hill`s horseshoe bat (Rhinolophus hilli) and other new records of bat species in Rwanda. Biodiversity Data Journal 10: e83546. https://doi.org/10.3897/BDJ.10.e83546
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For forty years, there has been growing uncertainty about whether Hill's horseshoe bat (Rhinolophus hilli) still persists in Nyungwe National Park, Rwanda. Only known from one small area within the National Park, R. hilli is listed as Critically Endangered by the International Union for the Conservation of Nature (IUCN), based on its extremely small geographic range and presumed low number of mature individuals. Here, we present and describe bat species occurrence data contributed to the Global Biodiversity Information Facility (GBIF) that we collected as part of a long-term collaborative project to rediscover this lost species. This data paper describes the survey methods and findings resulting from cave roost surveys, capture surveys, and acoustic sampling of bat echolocation activity in Nyungwe National Park and surrounding areas in south-western Rwanda from 2013-2020 and their conservation relevance.
We report the discovery of an extant population of Hill's horseshoe bat (Rhinolophus hilli) in Nyungwe National Park, Rwanda, 40 years since the last reported observation of the species in 1981. We also report the first record of Lander's horseshoe bat (Rhinolophus landeri) in Nyungwe National Park and the first record of the Damara woolly bat (Kerivoula argentata) in Rwanda. The dataset contributed to GBIF and described in this paper includes 278 occurrence records from 10 bat species of five families detected at 71 locations in or near Nyungwe National Park, Rwanda. We include a description of the morphological descriptions of R. hilli and present the first acoustic echolocation signatures and phylogenetic information for this species.
Afromontane rainforest, Albertine Rift, Nyungwe National Park, Rwanda
Nyungwe National Park in south-western Rwanda is one of the most biologically important montane rainforests in central Africa. The Park protects 1,019 km2 of montane rainforest, which is home to a diversity of wildlife species, including many species endemic to the Albertine Rift region of Africa (
First described by
Results of this work contribute to the overall knowledge of the biodiversity of the region and provide specific information to guide protective measures to save a critically-endangered bat from global extinction. Nyungwe National Park is one of the most biologically important montane rainforests in Central Africa. Documentation of the diversity of bat species occurring in the Park aids national Rwandan conservation efforts, which must balance competing interests. Since decades passed without any reported observation of R. hilli, uncertainty over its continued persistence impeded implementation of species-specific management actions, including safeguarding critical habitat for the species against encroachment or disturbance. Rediscovery of R. hilli and documenting new records of Rhinolophus landeri and Kerivoula argentata reinforces the universal value of Rwanda's committed stewardship of Nyungwe National Park as a global biodiversity hotspot.
By recording the first echolocation signature for R. hilli, we provide a beneficial tool for conservation managers to conduct cost-effective monitoring that provides information for conservation planning. The on-going acoustic monitoring conducted by Nyungwe National Park staff continues to identify the core range of the species within the Park, which greatly improves knowledge about critical habitat needs of the species. Furthermore, by contributing the echolocation signature to the ChiroVox global acoustic call database (
Bat surveys were conducted in Nyungwe National Park in south-western Rwanda and in a few locations near the park boundary. Sampling locations within Nyungwe National Park were primarily caves and forest trails. Surveys for bats were conducted within the Uwinka region of Nyungwe and in similar habitats in the Park to determine the presence of an extant population of R. hilli and document all bat species encountered.
Surveys were conducted in four phases: Initial reconnaissance surveys (2013-2015); reconnaissance for cave suitability by Nyungwe National Park Rangers (2018); a survey expedition with trapping efforts in forest habitats, cave surveys to assess bat use, and acoustic sampling of bat echolocation activity (2019); and on-going acoustic monitoring conducted by Nyungwe National Park Rangers (2019-present). Initial reconnaissance surveys were carried out by a small team (P. Webala and J. Nziza) with the intention of determining if the presence of R. hilli in Nyungwe National Park was readily detectable with minimal survey effort. Surveys were targeted in the Uwinka region of Nyungwe National Park and surrounding areas where bat roosts had been reported. Over the course of two years, 10 sites were surveyed with eight species detected (Fig.
In the cave suitability reconnaissance phase, Nyungwe National Park Rangers identified caves within Nyungwe National Park with features suitable for bat occupancy. We provided Nyungwe National Park Rangers with a pictorial cave survey form to describe the size, type, and location of caves and abandoned mines and to report on any sign of bats using subterranean features. Rangers reported caves encountered during patrols and queried local communities to identify sites. Rangers identified and located a total of ten caves, one abandoned mine, and one building as potential bat roost habitats prior to the planned survey expedition in early 2019 (Fig.
We conducted a 10-day intensive field survey from 13-23 January 2019 that focused on: (1) surveys for bat use at caves identified by Nyungwe Rangers as suitable and likely to be occupied by bats, (2) capture surveys in forested habitats in the Uwinka region and similar surrounding habitats in Nyungwe National Park, and (3) acoustic sampling of bat echolocation activity using SongMeter 4BAT-FS recorders (Wildlife Acoustics, Inc). In total, 17 locations were surveyed, ten within the Nyungwe National Park boundary (Fig.
Bat species encountered in Nyungwe National Park and surrounding areas from 2013-2020, their IUCN Red List Status and the habitat type where observations occurred.
Taxon |
IUCN Red List Status |
Occurrence Habitat |
Hipposideridae |
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Hipposideros caffer |
Least Concern |
Cave/Mine/Forest |
Hipposideros ruber |
Least Concern |
Building |
Nycteridae |
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Nycteris sp. |
Cave/Mine |
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Pteropodidae |
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Epomophorus labiatus |
Least Concern |
Village |
Myonycteris angolensis |
Least Concern |
Cave/Forest |
Rousettus aegyptiacus |
Least Concern |
Cave/Forest |
Stenonycteris lanosus |
Least Concern |
Cave/Forest |
Rhinolophidae |
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Rhinolophus clivosus |
Least Concern |
Mine/Forest |
Rhinolophus hilli 1 |
Critically Endangered |
Forest |
Rhinolophus landeri 2 |
Least Concern |
Cave/Forest |
Vespertilionidae |
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Kerivoula argentata 3 |
Least Concern |
Forest |
Miniopterus sp. |
Forest |
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Neoromicia sp. |
Forest |
1First record since 1981; 2First record in Nyungwe National Park; 3First record in Rwanda.
Notable records of bat species encountered in Nyungwe National Park. A, B Rhinolophus hilli, first observation of this species since 1981; C Rhinolophus landeri, first record of this species in Nyungwe National Park; D Rhinolophus clivosus, congeneric species found in Nyungwe for comparison; E Kerivoula argentata, first record of this species in Rwanda.
Location of acoustic surveys for Rhinolophus hilli conducted from July 2019 to November 2020 in Nyungwe National Park, Rwanda. Locations where R. hilli were detected and frequency in which R. hilli calls were identified (measured by number of positive triggering events/night, inset) are shown.
Survey efforts focused within Nyungwe National Park and surrounding areas in south-western Rwanda. The dataset includes 278 occurrence records from 10 bat species of five families detected at 71 locations in or near Nyungwe National Park.
Cave surveys: We surveyed caves by visually searching with the aid of bright lights all accessible areas for the presence of bats or signs of bat use. We noted the presence of bat guano or wall staining, if present. At sites with areas inaccessible to human observers, we deployed acoustic detectors (SongMeter 4BAT-FS with SMM-U2 ultrasonic microphones, Wildlife Acoustics, Inc.) at entrances for 1-2 nights and used Kaleidoscope Pro (version 5.4.2, Wildlife Acoustics, Inc.) to identify the presence of bat echolocation activity during crepuscular and nocturnal hours. If bats were present during an internal search, we captured bats with hand nets or placed harp traps (details below) at the entrance prior to evening emergence.
Capture surveys in forest habitats: Capture surveys were conducted with harp traps (a 2-bank 4.2 m2 harp trap by Ausbat and the ‘cave-catcher’ 2-bank 0.9 m2 harp trap by Bat Conservation and Management) and use of three to five mist-nets of 2 m, 6 m and 12 m lengths (Avinet). We placed harp traps and mist-nets parallel or perpendicular to forest trails in locations selected to maximise capture probability. Harp traps were deployed from sunset until sunrise. We opened mist-nets at sunset and monitored for approximately 4 hours and then re-opened 1-2 hours before sunrise. We monitored mist-nets continuously while open every 10-15 mins. We held bats individually in clean, cloth bags until processed and then released bats at the location of capture. See ‘Step Description’ for the description of data collected from captured bats.
Acoustic sampling: Nyungwe Park Rangers deployed SongMeter 4BAT-FS acoustic recorders (Wildlife Acoustics, Inc) at locations along forest trails or near cave entrances during multi-day patrols and collected recorders when returning from patrol. The SM4BAT-FS recorders with SMM-U2 microphones were programmed to record in full-spectrum at 384 kilohertz sampling frequency with 12 dB gain and 16 k high filter. All other settings were set to default. The SM4BATs were set to record 30 minutes before sunset to 30 minutes after sunrise and were typically deployed for 3-5 nights at each location. We embedded geo-location coordinates on all files using the GPS attachment available from Wildlife Acoustics, Inc. Data were transferred to external hard drives and sent to Bat Conservation International in the USA for processing. See ‘Step Description’ for the description of the processing of acoustic data for species identification of R. hilli.
For a subset of tissue samples, we compared species identification determined from morphological measurements with genetic data using BLASTN. As we were unable to obtain viable DNA from the holotype R. hilli specimen collected in 1981, we inspected both museum samples and compared morphological features with measurements of the two R. hilli caught during our survey. In addition, we compared the sequence data from the two suspected R. hilli samples with sequence data from closely-related species (
Species Identification and Morphometrics: We assessed captured bats for age (juvenile/sub-adult/adult), sex, and reproductive condition (females: non-breeding/pregnant/lactating/post-lactating; males: reproductively active/non-reproductively active as determined by enlarged testes) (
Echolocation Voucher Calls: We recorded voucher echolocation calls upon release for each echolocating bat species using an M500 full-spectrum bat detector (Pettersson Electronics) at a sampling rate of 500 kHz. For constant-frequency (CF) bats (e.g. Rhinolophus spp.), we recorded resting echolocation calls while the bat was in hand. For species using frequency-modulated (FM) echolocation, we recorded echolocation activity in flight immediately upon release while visually following the bat with a light. Hand-recorded bat echolocations were analysed using BatSound v.4.1 (Pettersson Electronics) to determine the following parameters for each pulse: duration (D), maximum frequency (FMAX), minimum frequency (FMIN), peak frequency (PF), and interpulse interval (IPI). We measured these parameters (D, FMAX, FMIN, and IPI) from spectrograms and the peak frequency (PF) from the power spectrum. We removed noise files and filtered the remaining files for constant frequency acoustic signatures (>15 ms call duration) using Kaleidoscope Pro (version 5.4.2, Wildlife Acoustics). Echolocation calls matching those of voucher calls collected from R. hilli (Fig.
DNA Extraction for Species Confirmation: DNA extraction from wing biopsy punches was carried out at CIBIO-InBIO, University of Porto, Portugal, using Qiagen DNeasy kits (Qiagen, Crawley, UK) and stored at -20oC. Mitochondrial cytochrome b (cyt b) gene was amplified by polymerase chain reaction (PCR) using the primers MOLCIT‐F (5′-AATGACAT-GAAAAATCACCGTTGT-3′) (
Due to the age and preservation method, we were unable to obtain viable DNA from the two museum specimens of R. hilli . Instead, to verify species identification, we inspected both specimens and compared morphological features with measurements of the two R. hilli caught during our survey (Table
Morphological measurements from two Rhinolophus hilli captured in 2019 (BCI RW19009, RW19052) compared to those recorded by
Sample Number |
BCI RW19009 |
BCI RW19052 |
ZMUZ 126639 |
MRAC 82006M1 |
Sex |
M |
M |
F |
F |
Age |
Adult |
Adult |
Adult |
Adult |
Mass (grams) |
14.0 |
15.0 |
- |
16.5 |
Forearm length (mm) |
53.35 |
49.75 |
54.3 |
54.2 |
Tail length (mm) |
21.10 |
26.55 |
29.3 |
- |
Hind-foot length (mm) |
8.80 |
9.50 |
12.2 |
- |
Ear length (mm) |
23.25 |
24.33 |
28.5 |
- |
Horseshoe-width (mm) |
13.25 |
14.35 |
- |
- |
Tibia length (mm) |
24.3 |
21.1 |
23.8 |
- |
4th Metacarpal length (mm) |
- |
- |
40.9 |
40.6 |
4th Phalange length (mm) |
- |
- |
10.9 |
10.6 |
Bayesian phylogeny of selected indivduals from the genus Rhinolophus using an alignment of 490 base pairs of mitochondrial gene cytochrome b. Black circles at nodes represent Bayesian posterior probabilities (PP) ≥ 0.95, and grey circles represent PP < 0.95. Tip labels represent major clades and more detailed breakdown of species names for R. maclaudi group. Species used in the phylogenetic analysis, including GenBank accession numbers are outlined in Suppl. material
Nyungwe National Park is the second-largest national park in Rwanda, protecting 1,019 km2 of Afromontane rainforest habitat in the Albertine Rift region of Africa. The Park is recognised for exceptionally high biodiversity with 1,068 recorded plant species, 322 bird species and 75 known mammal species, including 13 primates (
-2.918 and -2.142 Latitude; 28.869 and 29.575 Longitude.
The dataset includes occurrence records from Class Mammalia and Order Chiroptera, including 13 taxonomic records representing 10 genera and five families. Three records were identified to genus with the remaining 10 identified to species.
Rank | Scientific Name | Common Name |
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class | Mammalia | Mammals |
order | Chiroptera | Bats |
family | Rhinolophidae | Horseshoe Bats |
family | Hipposideridae | Roundleaf Bats |
family | Nycteridae | Slit-faced Bats |
family | Pteropodidae | Old World Fruit Bats |
family | Vespertilionidae | Vesper Bats |
2013-05-10 through 2020-11-14
The dataset includes bat species occurrence records resulting from survey efforts in Nyungwe National Park and surrounding areas in south-western Rwanda from 2013 to 2020 (
Column label | Column description |
---|---|
Scientific name | Scientific name (Genus and species) |
Country or Area | Country name where observation occurred |
Coordinates | Lat/Long |
Month and Year | Month and Year when observation occurred |
Basis of record | Method of observation |
Dataset | Name of dataset |
Kingdom | Kingdom |
Phylum | Phylum |
Class | Class |
Order | Order |
Family | Family |
Genus | Genus |
Species | Species |
This work was supported by Daniel Maltz, The Shared Earth Foundation, The Woodtiger Fund, Cullen Geiselman, Mohamed bin Zayed Species Conservation Fund, Wildlife Acoustics, and Bat Conservation International.
We would like to thank the Rwanda Development Board, Nyungwe Management Company, and the Nyungwe Park Rangers for their continued assistance with this project. We would also like to thank Deo Ruhagazi, Providence Uwanyirigira, and Deo Ryumugabe for their assistance during the 2019 expedition, to the authors of Demos et al. 2019 for granting early access to their data, and to David Bloom for assistance with publishing the data on GBIF. Lastly, we are grateful to Martina Schenkel, Emmanuel Gilissen, Dina Dechmann, the Zoological Museum of the University of Zurich, and the Royal Museum for Central Africa for allowing access to, and help collecting information from the preserved specimens of R. hilli.
JF - conceptualisation, investigation, data curation, writing - original draft and reviewing/editing, visualisation, supervision, project administration, funding acquisition
WFF - conceptualisation, investigation, writing - original draft and reviewing/editing, supervision, project administration, funding acquisition
JN - investigation, writing - reviewing and editing
ON - project administration, supervision, writing - reviewing and editing
PK - investigation, writing - reviewing and editing
MCD - investigation, project administration, writing - reviewing and editing
IN - investigation, project administration, supervision, writing - reviewing and editing
IT - investigation, writing - reviewing and editing
SK - investigation, writing - reviewing and editing
PN - project administration, supervision, writing - reviewing and editing
TLC - data curation, writing - reviewing and editing
RM - project administration, writing - reviewing and editing
PW - conceptualisation, investigation, data curation, writing - reviewing/editing, supervision, project administration, funding acquisition
Author contribution statement developed using Contributor Role Taxonomy (CRediT).