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Data Paper (Biosciences)
Shrews (Soricidae) of the lowland forests around Kisangani (DR Congo)
expand article infoFrederik Van de Perre, Herwig Leirs, Julien Cigar§, Sylvestre Gambalemoke Mbalitini|, Jean-Claude Mukinzi Itoka, Erik Verheyen#,
‡ Evolutionary Ecology Group, University of Antwerp, Antwerp, Belgium
§ Belgian Biodiversity Platform, Brussels, Belgium
| Centre de Surveillance de la Biodiversité, Kisangani, Democratic Republic of the Congo
¶ Faculté des Sciences, UNIKIS, Kisangani, Democratic Republic of the Congo
# Royal Belgian Institute of Natural Sciences, Brussels, Belgium
Open Access

Abstract

Background

The Congo Basin rainforest is the second largest rainforest in the world and one of the most biodiverse regions on Earth. Nevertheless, the Congo Basin biodiversity remains to be fully mapped, with many species awaiting discovery or official description. In recent years, much effort has been put into research on shrews (Soricidae), particularly in the region around Kisangani (D.R. Congo). Shrews are opportunistic feeders that are able to forage on a large diversity of invertebrate prey and therefore play an important role in the forest ecosystem. Furthermore, as they largely depend on forest habitats and have limited dispersal capacities, shrews form an interesting model group to study biogeographic patterns in the Congo Basin.

New information

This paper collates the efforts on shrew research from the wider region around Kisangani, in the centre of the Congo Basin. Apart from sampling information, the dataset includes morphological measures, DNA sequences and photographs. This dataset is therefore critical in the study of the taxonomy and ecology of Soricidae in the Congo Basin lowland rainforests.

Keywords

pitfall, removal trapping, tropical lowland forest, Democratic Republic Congo, Soricidae

Introduction

The Congo basin rainforest is the second largest in the world and one of the most biodiverse regions on earth (Mittermeier et al. 2003, Lewis 2005). Both the forest and its biodiversity are threatened by forest loss and bushmeat hunting (Malhi et al. 2013). Despite its importance for climate change mitigation and biodiversity conservation, knowledge on the impact of forest loss and degradation and bushmeat hunting on local biodiversity is currently lacking (Gibson et al. 2011, Alroy 2017, Phillips et al. 2017). In fact, the biodiversity of the Congo basin is generally understudied, with several new species being discovered every year (e.g. Colyn et al. 2010, Stanley et al. 2013).

Our knowledge on occurrence, ecology and taxonomy of shrews (Soricidae) in the Congo basin is currently incomplete (Mukinzi et al. 2005, Gambalemoke 2014, Jacquet et al. 2015). Shrews represent critical food web links via their role as predators of small vertebrates and invertebrates and as prey for several vertebrate predators (Churchfield et al. 2004). Apart from their importance in the ecosystem, shrews are also a suitable model taxon for evaluating biogeographic and historical hypotheses (Quérouil et al. 2003). Indeed, the central Congo basin (i.e. the lowland forests south of the Congo river) harbours less terrestrial vertebrate species than the northern part which is due to the smaller habitat area and isolated position of the central Congolian lowland forests (Van de Perre et al. 2019). As richness is limited by habitat area and isolation, this implies that diversity differences amongst Congolian lowland forests are mostly due to forest-associated taxa with limited dispersal capacities, such as shrews.

Therefore, this paper assembles shrew occurrences from three studies in the central Congo Basin (Gambalemoke et al. 2008b, Mukinzi 2014, Van de Perre et al. 2018) and includes the metadata of the captured specimens (morphological measurements, DNA and sampling details) which allows for the advancement of the knowledge on taxonomy and ecology of shrews in the central Congo basin.

General description

Purpose: 

This paper assembles data collected in the framework of the PhD theses of Jean-Claude Mukinzi Itoka, Sylvestre Gambalemoke Mbalitini and Frederik Van de Perre. These three theses were executed at or in collaboration with the University of Kisangani, the University of Antwerp and the Royal Belgian Institute for Natural Sciences. Although the design and purpose of the three studies differ, the sampling design (the method in which shrews were collected) is equal across studies, which justifies the publication of the dataset as a whole.

Project description

Study area description: 

We compiled data from three studies in the region around Kisangani (Gambalemoke et al. 2008b, Mukinzi 2014, Van de Perre et al. 2018). The combined data represent 36 sampling sites in which sampling effort was equal and distributed within 6 localities in the Tshopo Province (Fig. 1 and Table 1). Sampling localities are separated by the Congo River and some of its major tributaries (Tshopo, Lindi, Lomami).

List of sampling sites including locality (and initials of collectors), coordinates, forest type (OG-X: Mixed old-growth forest; OG-M: Monodominant old-growth forest; RF: Regrowth forest; FL: Fallow land; OP: abandoned oil palm plantation), number of trapping sessions, start date of trapping and range of field numbers under which specimens are stored.

Locality

Latitude

Longitude

Site

Forest type

Number of trapping sessions

Start date

Field numbers

Baliko

(SG)

0.6415

26.3639

Baliko_FP

OG-X

1

23/09/2006

BA77-675

0.6415

26.3639

Baliko_FS

RF

1

23/09/2006

0.6415

26.3639

Baliko_JC

FL

1

23/09/2006

Djabir

(JCM, SG)

0.5192

24.1736

Djabir_FP_L1

OG-X

1

13/10/2005

DJ1-567

0.5192

24.1736

Djabir_FP_L2

OG-X

1

13/10/2005

0.5192

24.1736

Djabir_FS

RF

1

13/10/2005

Masako

(JCM, SG)

0.6051

25.2565

Masako_FP

OG-X

1

2/06/2005

R27985-28242

0.6051

25.2565

Masako_FS

RF

1

2/06/2005

0.6051

25.2565

Masako_FS_L1A

RF

1

12/03/2011

CRT3151-3520

0.6051

25.2565

Masako_FS_L1C

RF

1

12/03/2011

0.6051

25.2565

Masako_Gil_L1A

OG-M

1

27/03/2012

MSK1-362

0.6051

25.2565

Masako_Gil_L1C

OG-M

1

27/03/2012

Yangambi

(FVdP)

0.8144

24.4937

Yangambi_BRA1

OG-M

1

12/07/2015

COB2-1390

0.7966

24.4978

Yangambi_GIL3

OG-M

1

8/05/2014

0.8081

24.5281

Yangambi_GIL4

OG-M

1

21/06/2013

0.7894

24.5175

Yangambi_JEU1

RF

1

20/06/2013

0.7949

24.4919

Yangambi_JEU2

RF

1

7/05/2014

0.7967

24.4941

Yangambi_JEU3

RF

1

13/07/2015

0.7931

24.4901

Yangambi_JEU4

RF

1

16/07/2016

0.7921

24.4972

Yangambi_JEU5

RF

1

17/07/2016

0.8135

24.5126

Yangambi_MIX2

OG-X

1

16/07/2016

0.7805

24.5211

Yangambi_MIX3

OG-X

1

20/06/2013

0.8144

24.4931

Yangambi_MIX5

OG-X

1

12/07/2015

0.8026

24.4875

Yangambi_MIX6

OG-X

1

7/05/2014

Yelenge

(JCM)

0.6387

25.0780

Yelenge_FP

OG-X

1

6/03/2005

R27622-27981

0.6387

25.0780

Yelenge_FS

RF

1

6/03/2005

Yoko (JCM)

0.2940

25.2881

Babogombe_FPG_L1

OG-M

5

21/04/2007

LEGM400-3017

0.2940

25.2881

Babogombe_FPG_L2

OG-M

5

22/02/2007

0.2940

25.2881

Babogombe_FP_L1

OG-X

8

14/12/2006

0.2940

25.2881

Babogombe_FP_L2

OG-X

7

14/12/2006

0.2940

25.2881

Babogombe_FP_L3

OG-X

9

21/04/2007

0.2940

25.2881

Babogombe_FS_L1

RF

3

14/12/2006

0.2940

25.2881

Babogombe_FS_L2

RF

3

14/12/2006

0.2940

25.2881

Babogombe_JJ_L1

FL

3

15/12/2006

0.2940

25.2881

Babogombe_JV_L1

FL

3

23/02/2007

0.2940

25.2881

Babogombe_JV_L2

FL

2

15/12/2006

0.3234

25.2539

Kisesa_JJ

FL

8

18/10/2007

0.3234

25.2539

Kisesa_JV

FL

8

18/10/2007

0.3234

25.2539

Kisesa_VPS

OP

8

18/10/2007

Figure 1.  

Sampling localities (dots) in the environs of Kisangani (see Table 1 for additional details). The city of Kisangani (square) is surrounded by a mosaic of agricultural land and regrowth forest (light green), while old-growth forests (dark green) can be found throughout the area. Blue lines represent the Congo River and its tributaries. The map on the left shows the situation of the study area within Africa.

In the study area, forest disturbance is mainly in the form of slash-and-burn agricultural activities, followed by abandonment and secondary succession. Fallow land, the pioneer stage of forest recolonisation, contains dense thickets with few tall trees. Regrowth forests generally are dominated by Musanga cecropioides in the canopy. Old-growth, closed canopy forests represent a range of vegetation, including mixed, semi-deciduous forest, monodominant forest of Gilbertiodendron dewevrei (De Wild.) J. Leonard and monodominant forest of Brachystegia laurentii (De Wild.) Hoyle. In some localities, sampling was also conducted in abandoned oil palm plantations. Apart from Yangambi (Van de Perre et al. 2018), quantitative data on tree composition of each sampling site is lacking.

Following the revised Köppen-Geiger classification (Peel et al. 2007), the climate of the region is Af-type tropical rainforest climate. At the Yangambi meteorological station, the annual precipitation is 1839.5 ± 205.7 mm (1980–2012) and average dry season length is 3.3 ± 1.3 months (a month is dry if it receives less than 100 mm of precipitation). Dry seasons occur in December–February and June-August. Temperatures are high and constant throughout the year, with a minimum of 24.2 ± 0.4°C in July and a maximum of 25.5 ± 0.6°C in March (Doetterl et al. 2015).

Funding: 

F.V.d.P. was supported by a Ph.D. fellowship from the Research Foundation – Flanders and by the Belgian Science Policy Office (COBIMFO Project; Congo Basin integrated monitoring for forest carbon mitigation and biodiversity; contract no. SD/AR/01A).

Sampling methods

Sampling description: 

In all localities, shrews were sampled using the paceline method, which involved placing 20 pitfall traps at 5 m intervals on transects (Nicolas et al. 2003). Pitfall traps consisted of non-baited buckets (10-litre, 30×30×23 cm) that were buried in the ground, with rims even with the ground surface. A plastic drift fence (100 m) was set to increase capture effectiveness by guiding shrews toward traps. Pitfall traps were maintained at their locations for 21 days and were checked daily. Only in Yoko, these pitfall lines were set for multiple sessions at the same location. In all other locations, trapping was only conducted once (Table 1).

Quality control: 

Species were identified based on external morphology and cranio-dental characteristics. In addition, species assignments were confirmed for several specimens of each species by molecular analysis (16s rRNA). Taxonomic nomenclature follows Hutterer (2005). Specimens belonging to problematic species complexes that are in need of revision were provisionally labelled with cheironyms, pending formal description.

Step description: 

Field measurements

Sex and sexual condition were noted for each specimen:

  • Males:
    • testes: abdominal
    • swelling of the epididymis: visible or not
  • Females:
    • vagina: closed or perforated
    • nipples: small or swollen, lactating
    • pregnant: yes or no

Following measurements were taken from those specimens that were completely intact:

  • Weight (in grams)
  • Body length (head - tailbone, in mm)
  • Length of tail (tail length in mm of the point of curvature (anus) until the tip of the tail)
  • Size of the left hind leg (0.1 mm)
  • Size of the left ear (0.1 mm)

Sample collection

Samples of liver, spleen and kidney were stored in 96% alcohol and RNA-later (only kidney). Blood samples were transferred to filter paper. Ectoparasites were preserved in 70% alcohol. Carcasses of specimens were stored at the Laboratory of Ecology and Animal Resource Management (University of Kisangani) and the Zoologisches Forschungsmuseum Alexander Koenig (Bonn). Tissues samples are stored at the Evolutionary Ecology Lab (University of Antwerp) and at the Royal Belgian Institute of Natural Sciences (Brussels). All specimens are stored under their field number.

For the collection in Yangambi, pictures were taken of each specimen's ventral, dorsal and lateral sides.

DNA Barcoding

DNA analysis of 16S-rRNA was conducted for a selection of individuals. For PCR amplification, we used the primer pair 16Sar-L (forward: 5′-CGCCTGTTTATCAAAAACAT-3′, Palumbi et al. 1991) and 16S-Hm (reverse: 5′AGATCACGTAGGACTTTAAT-3′, Quérouil et al. 2001). PCR amplification was performed in 15-µl reaction mixtures that contained 7.5 µl Qiagen Multiplex, 0.2 µM of each primer, 1.5 µl DNA template and 5.4 µl sterile deionised water. The reaction mixtures were preheated at 95°C for 15 min, followed by 42 amplification cycles (95°C for 30 s, 46°C for 90 s and 72°C for 90 s), with a final 10 min extension at 72°C. The samples were purified and sequenced in both directions at VIB Genetic Service Facility (University of Antwerp). Sequences were aligned using the Geneious software (Drummond et al. 2015).

Geographic coverage

Description: 

Lowland forests of the Kisangani, Isangi and Ubundu territories of the Tshopo province (former province Orientale), Democratic Republic of Congo.

Coordinates: 

0°N and 1°N Latitude; 24°E and 27°E Longitude.

Taxonomic coverage

Description: 

All species belong to the family Soricidae, particularly the subfamily Crocidurinae. The dataset contains species from 5 genera: Crocidura (14 species), Paracrocidura (1), Scutisorex (2), Suncus (1) and Sylvisorex (4) (Table 2).

Number of specimens per species caught in each locality.

Species

Djabir

Yoko

Yangambi

Yelenge

Masako

Baliko

Crocidura caliginea Hollister, 1916.

-

-

52

3

14

7

Crocidura crenata Brosset, Dubost & Heim de Balsac, 1965.

-

-

9

5

2

0

Crocidura denti Dollman, 1915.

-

-

104

8

25

11

Crocidura dolichura Peters, 1876.

13

111

8

6

5

0

Crocidura cf. fuscomurina Heuglin, 1865

-

4

-

-

-

-

Crocidura goliath Thomas, 1906.

0

10

-

-

-

-

Crocidura grassei Brosset, Dubost & Heim de Balsac, 1965.

0

26

-

-

-

-

Crocidura latona Hollister, 1916.

21

168

0

1

26

0

Crocidura littoralis Heller, 1910.

27

24

153

44

21

4

Crocidura ludia Hollister, 1916.

4

1013

27

0

34

11

Crocidura cf. maurisca Thomas, 1904

0

1

-

-

-

-

Crocidura cf. muricauda Miller, 1900

-

-

4

0

1

0

Crocidura olivieri Lesson, 1827.

6

173

43

0

11

10

Crocidura yoko sp1

0

64

-

-

-

-

Paracrocidura schoutedeni Heim de Balsac, 1956.

3

47

6

6

33

4

Scutisorex congicus Thomas, 1915.

-

-

4

1

22

6

Scutisorex n.sp.

-

75

-

-

-

-

Suncus cf. remyi Brosset, Dubost & Heim de Balsac, 1965.

-

-

27

0

5

5

Sylvisorex akaibei Mukinzi, Hutterer & Barriere, 2009.

-

-

27

1

0

1

Sylvisorex cf. johnstoni Dobson, 1888.

-

-

12

5

16

14

Sylvisorex nsp1

0

11

-

-

-

-

Sylvisorex cf. ollula Thomas, 1913.

6

275

-

-

-

-

Unidentified specimens

14

15

9

26

8

3

Total

94

2017

485

106

223

76

The dataset contains a number of specimens that likely belong to species new to science. Specimens morphologically resembling known species but found far outside the distribution of the known species have been identified using a cf. statement, others were named using a cheironym.

Crocidura sp1 yoko has easily distinguishable characteristics: small size (4-6 g), brownish on the back, greyish-brown on the belly, brownish tail that is completely glabrous, except from the base which is covered with few small vibrissae, the down side of the tail clear, almost white at the base and around the anus and its small paws are equally light coloured (Fig. 2). Its skull resembles that of Crocidura ludia but is smaller (Mukinzi-Itoka 2014).

Figure 2.  

Dorsal and ventral view of Crocidura sp1 yoko (LEGM458, Mukinzi 2014).

Sylvisorex n.sp. is a small and rare species. Brown greyish on the back and silvery grey on the belly. It has a long tail covered with small hairs that grow longer and are more numerous towards the tip, forming a white brush. The tail is brown-black on top and slightly lighter on the bottom (Fig. 3). The species resembles Crocidura polia Hollister, 1916. However, the new species has little vibrissae on its tail while, in C. polia, half of the tail is covered with vibrissae (Mukinzi 2014).

Figure 3.  

Dorsal and ventral view of body and skull of Sylvisorex n. sp. (LEGM1887, Mukinzi 2014).

Scutisorex n. sp. (description in progress, J. Hulselmans pers. comm.) was found in RF Yoko and its distribution seems to be limited to the forest bloc between the Lomami and Lualaba.

Temporal coverage

Notes: 

8 June 2005 (Yelenge) to 7 August 2014 (Yangambi).

Collection data

Collection name: 
Carcasses of specimens were stored at the Laboratory of Ecology and Animal Resource Management, University of Kisangani. Tissues samples are stored at the University of Antwerp and at the Royal Belgian Institute of Natural Sciences. For the collection of Yangambi, pictures were taken of each specimen's ventral, dorsal and lateral sides.
Specimen preservation method: 
Samples of liver, spleen and kidney were stored in 96% alcohol and RNA-later (only kidney). Blood samples were transferred to filter paper. Ectoparasites were preserved in 70% alcohol. Specimen carcasses were stored in 70% alcohol.

Usage rights

Use license: 
Creative Commons Public Domain Waiver (CC-Zero)

Data resources

Data package title: 
African Mammalia
Number of data sets: 
3
Data set name: 
Specimen list
Data format: 
.csv
Description: 

The data can be downloaded from the online database, African Mammalia. Shrew specimens can be searched through the 'Search' or 'Taxa' tab.

Column label Column description
Collection number Museum collection number
Order Taxonomic rank
Family Taxonomic rank
Family author Author(s) and publication date of family
Genus Taxonomic rank
Genus author Author(s) and publication date of genus
Species Taxonomic rank
Species author Author(s) and publication date of species
Subspecies Taxonomic rank
Subspecies author Author(s) and publication date of subspecies
Determinator Determinator of specimen
Determination year Determination year
Accuracy Accuracy of determination
Field number Unique identifier of specimen
Locality Sampling locality
Altitude Altitude of sampling location in metres
Altitude max Maximum altitude
Country iso code CD
Country Democratic Republic Congo
Latitude Latitude of sampling locality in decimal degrees
Longitude Longitude of sampling locality in decimal degrees
Collector Collector of specimen
Date collected Date of collection
Date collected end End of data collection
Sex m, Male - f, Female
Sexual condition name Sexual condition, see above
Sexual condition code Sexual condition code
Age Age of specimen
Weight Weight in gram
Type Holotype, paratype or syntype
Trap Type of trap used
Available Whether the specimen is present in the collection
Basis of record Preserved specimen or observation
Tissues Whether tissue samples are available
url Link to the specimen information on African Mammalia
Data set name: 
Sequences
Data format: 
.csv
Description: 

Export of DNA sequences and metadata.

Column label Column description
Collection number Museum collection number
Field number Field number
Basis of record Preserved specimen or observation
Family Family, Soricidae
Genus Genus name
Species Species name
Subspecies Subspecies name
Accession number Genbank accession number
Sequence number Unique sequence code
Sequence DNA sequence
url Link to the specimen information on African Mammalia.
Data set name: 
Measurements
Data format: 
.csv
Description: 

Export of morphological measurements and metadata.

Column label Column description
Collection number Museum collection number
Field number Unique field code
Basis of record Preserved specimen or observation
Familiy Family, Soricidae
Genus Genus name
Species Species name
Subspecies Subspecies name
Sex Sex (Male or Female)
hb Head-body length
tl Tail length
hf Hind foot length
el Ear length
m1-m25 Craniometric measurement, description available on http://projects.biodiversity.be/africanmammalia/about/data#measurements
url Link to the specimen information on African Mammalia.

Additional information

Results communication:

Results of diversity analyses have already been published in peer-reviewed journals (in chronological order):

  • Mukinzi et al. (2005)
  • Gambalemoke et al. (2008a)
  • Gambalemoke et al. (2008b)
  • Mukinzi et al. (2009)
  • Van de Perre et al. (2018)

Acknowledgements

Fieldwork was carried out in collaboration with the Centre de Surveillance de la Biodiversité at the University of Kisangani. We thank Y. Mutafchiev, R. Mesibov, R. Hutterer, V. Nicolas, S. Solari, A. Balakirev and an anonymous reviewer for helpful comments on earlier versions of this manuscript.

Author contributions

Jean-Claude Mukinzi Itoka, Sylvestre Gambalemoke Mbalitini and Frederik Van de Perre are the main collectors of specimens and observations. Frederik Van de Perre sequenced the specimens. Julien Cigar developed the online database. Frederik Van de Perre wrote the first version of the manuscript and all co-authors contributed to the writing.

References