Original Research Articles TAXONOMIC AND ECOLOGICAL NOTES ON TERMES PROPINQUUS (HOLMGREN, 1914), KNOWN FROM SUMATRA (BLATTODEA: TERMITOIDAE: TERMITIDAE)
S. Muarrif1, S. Samadi2, J. Jauharlina3 and S. Syaukani4*
1Graduate School of Mathematics and Applied Sciences, Universitas Syiah Kuala, Darussalam Banda Aceh 23111, Indonesia
2Department of Animal Husbandry, Faculty of Agriculture, Universitas Syiah Kuala, Darussalam 23111, Banda Aceh, Indonesia
3Department of Plant Protection, Faculty of Agriculture, Universitas Syiah Kuala, Darussalam, Banda Aceh, 23111, Indonesia
4Biology Department, Faculty of Mathematics and Natural Sciences, Universitas Syiah Kuala, Darussalam 23111, Banda Aceh, Indonesia
*Corresponding author’s email: syaukani@unsyiah.ac.id
ABSTRACT
The genus Termes Linneus, 1758, consisting of a total of 24 valid named species known from the Old World, is a very heterogeneous group of termites, and seems to involve many taxonomic obscurities and confusions. In the island of Sumatra, the sixth largest island located in the Southeast Asian tropics, four species of Termes have been found, namely T. comis (Haviland, 1898), T. laticornis (Haviland, 1898), T. rostratus (Haviland, 1898), and T. propinquus (Holmgren, 1914). T. propinquus is also known from Brunei, Indonesia (Kalimantan and Sumatra), Malaysia (Mainland, Sabah and Sarawak), and Thailand. However, previous authors have mentioned that T. propinquus has been poorly discriminated from the other congeners, especially T. rostratus (Tho, 1992). Therefore, the present study aimed to clarify the discrimination of Termes propinquus (Holmgren, 1914) from the morphologically similar congeners from Sumatra. A total of 14 nests were collected using a standardized sampling protocol and visual colony searching in Sumatra and its adjacent island. As a result of careful morphological examination of the soldier caste, T. propinquus was discriminated from the three other congeners by a combination of the following characteristics: distinctly long frontal projection, larger head capsule, and 2nd antennal segment distinctly longer than the 3rd. The re-description of the soldier caste of T. propinquus and a key to Termes species known from Sundaland are provided. The nests of T. propinquus were attached to the bases of living trees, clinging to stumps or the bases of dead tree, or were epigeal.
Keywords: termite; Termes propinquus; nest; snapping mandibles; Sumatra
https://doi.org/10.36899/JAPS.2021.6.0394
Published online March 31, 2021
INTRODUCTION
Termites, from the epifamily Termitoidae (or the infraorder Isoptera), are dominant invertebrates in tropical and subtropical soil ecosystems, and perform indispensable functions as mechanical decomposers and ecological engineers, creating and preparing microhabitats for other organisms, including microbes that contribute to the decomposition process of organic matter (Pearce, 1997; Bignell and Eggleton, 2000).
Termitoidae is a monophyletic lineage consisting of more than 2900 valid named species (Engel et al., 2009; Syaukani et al., 2019), belonging to 281 genera and nine families. Six of them, namely Kalotermitidae, Archotermopsidae, Hodotermitidae, Rhinotermitidae, Stylotermitidae, and Termitidae, are known from the Oriental region (Krishna et al., 2013), and three families, namely Kalotermitidae, Rhinotermitidae and Termitidae, have been recorded in the Indo-Malayan sub-region.
Termitidae constitutes the most species-rich and ecologically diversified family. In Southeast Asia, this family is represented by four subfamilies, namely Apicotermitinae, Termitinae, Macrotermitinae, and Nasutitermitinae (Tho, 1992; Gathorne-Hardy, 2001). The genus Termes was classified by Holmgren (1914) and consists of a total of 24 valid named species, of which most are known from the Ethiopian, Neotropical, and Oriental regions, and a few from the Paleartic region (Krishna et al., 2013). The soldier caste of the genus has slightly asymmetrical (Tho, 1992) or asymmetrical snapping mandibles and a frontal projection (Bourguignon et al., 2008). The classification of the genera of the Capritermes complex has been in a confused state, because some of the genera, including those involving Termes, seem to be composed of heterogeneous lineages (Tho, 1992; Gathorne-Hardy, 2004). The nesting behavior of Termes is also diverse; various shapes of nests are found, and inquilism is also seen (Consarinsky, 2004).
On the island of Sumatra, the sixth largest island located in the Southeast Asian tropics, four species of Termes are known, namely T. comis (Haviland, 1898), T. laticornis (Haviland, 1898), T. rostratus (Haviland, 1898), and T. propinquus (Holmgren, 1914). Termes propinquus is known from Indonesia (Kalimantan and Sumatra), Malaysia (Mainland, Sabah and Sarawak), Brunei, and Thailand, and its type locality is Sumatra (Tandjong Slamat) (Holmgren, 1914; Gathorne-Hardy, 2004; Krishna et al., 2013). However, Holmgren (1914) and other authors (John, 1925; Thapa, 1981) have mentioned that T. propinquus has been poorly discriminated from the other congeners, especially T. rostratus (Tho, 1992).
The present article, therefore, aimed to give a re-description of the soldier caste of T. propinquus, and to clarify the discrimination of T. propinquus from the other three Sumatran congeners based on the external morphology of the soldier caste. In addition, information on the nesting behavior of T. propinquus is provided.
MATERIALS AND METHODS
The specimens of T. propinquus examined in the present study were collected from various habitats and altitudinal zones of Sumatra between 1998 and 2017 (Figure 1; Table 1).
Table 1. Colonies of T. propinquus from Sumatra and adjacent islands. examined. Abbreviations (Abb.) of sampling sites: NS-KM, Kemiri, North Sumatra; NS-BL, Bukit Lawang, North Sumatra; NS-SB, Suaq Balimbing, North Sumatra; WS-KS, Kerinci Seblat, West Sumatra; MT-SB, Siberut, Mentawai; MT-PS, Pulau Sipora, Mentawai (see Fig. 1)
Colony ID
|
Sampling site
|
Forest Type
|
Nest type
|
|
Abb.
|
Coordinates
|
Altitude (m)
|
|
|
KMR-SYK-1999-C015
|
NS-KM
|
03° 47' 50" N
97° 33' 02" E
|
1,100
|
Primary sub-montane
|
Attached to the bases of living trees
|
KMR-SYK-1999-C008
|
NS-KM
|
03° 47' 50" N
97° 33' 02" E
|
1,100
|
Primary sub-montane
|
Clung to stumps or the bases of dead tree
|
KMR- SYK-2000-C106
|
NS-KM
|
03° 47' 50" N
97° 33' 02" E
|
1,100
|
Primary sub-montane
|
Clung to stumps or the bases of dead tree
|
KMR- SYK-2014-C018
|
NS-KM
|
03° 47' 50" N
97° 33' 02" E
|
1,100
|
Primary sub-montane
|
Clung to stumps or the bases of dead tree
|
KMR- SYK-2014-C022
|
NS-KM
|
03° 47' 50" N
97° 33' 02" E
|
1,100
|
Primary sub-montane
|
Epigeal
|
SUAQ- SYK-1999-C011
|
NS-SB
|
03° 02' 51" N
97° 25' 01" E
|
100
|
Primary low land dipterocarp
|
Epigeal
|
SUAQ-TT-2017-C012
|
NS-SB
|
03° 02' 51" N
97° 25' 01" E
|
100
|
Primary low land dipterocarp
|
Clung to stumps or the bases of dead tree
|
SUAQ-TT-2017-C022
|
NS-SB
|
03° 02' 51" N
97° 25' 01" E
|
100
|
Primary low land dipterocarp
|
Epigeal
|
BL- SYK-2002-C061
|
NS-BL
|
03° 32' 18" N
98° 08' 50" E
|
350
|
Primary low land dipterocarp
|
Attached to the bases of living trees
|
BL SYK--2014-C034
|
NS-BL
|
03° 32' 18" N
98° 08' 50" E
|
350
|
Primary low land dipterocarp
|
Attached to the bases of living trees
|
KSNP SYK--2006-C-27
|
WS-KS
|
00° 41' 32" S
100° 26' 36" E
|
1,200
|
Primary sub-montane
|
Clung to stumps or the bases of dead tree
|
SNP- SYK-2000-C014
|
MT-SB
|
01° 29' 22" S
98° 58' 09" E
|
50
|
Primary low land dipterocarp
|
Attached to the bases of living trees
|
SNP- SYK-2007-C098
|
MT-SB
|
01° 29' 22" S
98° 58' 09" E
|
50
|
Primary low land dipterocarp
|
Clung to stumps or the bases of dead tree
|
SI- SYK-2007-006
|
MT-PS
|
02° 11' 57" S
99° 40' 02" E
|
50
|
Secondary low land dipterocarp
|
Clung to stumps or the bases of dead tree
|
For the other three congeners from Sumatra, the syntypes in the collection of the Entomology Department, the Natural History Museum (UK), were examined. The focus stacking images of the head, body, pronotum, and antenna of the soldier caste were created using Helicon Focus 6 software based on source images taken as multi-layer montages using a Leica M205C stereomicroscope, controlled by Leica Application Suite version 3 software at the Fort Lauderdale Research and Education Center, University of Florida (USA). The images were taken by placing the specimen in a transparent Petri dish filled with ethanol gel (Purell Hand Sanitizer) in order to keep the specimen at an appropriate angle. A line drawing was also prepared based on the focus stacking images for T. propinquus, while T. rostratus, T. comis, and T. laticornis were redrawn with minor editorial modifications from Tho (1992). General morphological terminology and definitions of measuring characters followed Roonwal and Chhotani (1989). Head Capsule Length (HL) and Maximum Head Width (HW) were measured by following Roonwal and Chhotani (1989), Thapa (1981), and Tho (1992).
Fig. 1. Sampling sites of Termes propinquus examined.
RESULTS AND DISCUSSION
Re-description of Termes propinquus Holmgren, 1914 based on the soldier caste: Head capsule brownish yellow; mandibles dark reddish-brown; antenna and pronotum of thorax pale brownish yellow; labrum, meso- and metanotum of thorax, abdominal tergites and legs pale ivory white (Figure 2). Head with several scattered hairs; frontal projection with long hair at the tip and on the dorsal side; postmentum with several hairs along the anterior and anterolateral margins; pronotum with long and short hair along the margins; abdominal tergites with dense hairs. Head capsule in dorsal view elongate, almost 1.5 times longer than broad, rectangular or sub-rectangular; lateral margins straight and parallel. Frontal projection very long, in dorsal view cone-shaped; the apex in lateral view upcurved, acutely pointed; anterior margin in lateral view convex (Figures 2a, 2b, 3d). Antenna 14-segmented; 2nd longer than 3rd; 4th shorter than 3rd; 5th–14th gradually increased in length toward the apex. Labrum elongate, longer than broad; lateral margin almost straight and parallel; anterior margin sinuate. Mandibles almost symmetrical; left mandible long, slender, gently incurved in the basal half and acutely incurved at the tip. Postmentum in ventral view slightly swollen posteriorly. Pronotum saddle-shaped; anterior margin without a notch; posterior margin weakly concave at the middle. Legs short; apical tibial spurs 3:2:2.
Fig. 2. Soldier caste of Termes propinquus from Suaq Balimbing, North Sumatra (Suaq Balimbing Field Station; colony (SUAQ-TT-2017-C012). Head capsule in lateral view (a), dorsal view (b), body in left view (c).
Taxonomic remarks: Termes propinquus can be discriminated from the three other congeners from Sumatra based on the external morphology of the soldier caste. In the lateral view of the head, the frontal projection is less elongate in T. laticornis (Figure 3c) than in T. propinquus (Figure 3d). The head capsule is distinctly larger in T. laticornis (HL ≈ 1.82 mm, HW ≈ 1.13 mm) than in the other congeners from Southeast Asia (Tho, 1992; Thapa, 1981). In the dorsal view, the frontal projection is more elongate in T. propinquus (Figure 3d) than in T. rostratus (Figure 3b). The 2nd antennal segment is distinctly longer than the 3rd in T. propinquus, but only slightly longer than the 3rd in T. comis; the frontal projection in the lateral view is extremely elongate and has sparse hairs in the former (Figure 3d), but is moderately elongate and has dense hairs in the latter (Figure 3a).
Fig. 3. Dorsal and lateral views of head of the soldier castes of the four Termes known from Sundaland (a-d). Termes comis (a), T. rostratus (b), T. laticornis (c), T. propinquus (d). (a-c) Redrawn with minor editorial modification from Tho (1992), (d) drawn from the specimen (SUAQ-TT-2017-C012).
A key to the Termes species from the Sundaland of Southeast Asia, based on the soldier caste, is provided as below. For HL and HW, the range (n=10) and mean are given.
1
|
-
|
Lateral view: Frontal projection less elongate; HL 1.80–1.85 mm, 1.82 mm; HW 1.00–1.15 mm, 1.13 mm. …. T. laticornis (Haviland, 1898)
|
|
-
|
Lateral view: Frontal projection moderately to extremely elongate .. 2
|
2
|
-
|
Lateral view: Frontal projection extremely elongate; HL 0.95–1.113 mm, 1.12 mm; HW 0.70–0.73 mm, 0.72. ……………………….…………….. T. propinquus (Holmgren, 1914)
|
|
-
|
Lateral view: Frontal projection moderately elongate ……….……... 3
|
3
|
-
|
Dorsal view: Frontal projection with dense hairs (especially on anterior face); HL 1.40–1.45 mm, 1.44 mm; HW 0.90–1.10 mm, 0.94 mm. ………….… T. comis (Haviland, 1898)
|
|
-
|
Dorsal view: Frontal projection with sparse hairs; HL 1.00–1.20 mm, 1.13 mm; HW 0.60–0.72 mm, 0.68 mm. …………………………………………. T. rostratus (Haviland, 1898)
|
Nesting behavior: A total of 14 nests of T. propinquus (Holmgren, 1914) were found in this study. Four nests (28%) were attached to the bases of living trees, and seven nests (50%) were attached to stumps or the bases of dead trees (Figure 4). The advantages of this type of nest might be (1) to increase physical robustness of the nests (resistance to disturbances by ground-dwelling mammals and heavy rain), (2) to economize the total amount of building material for building nests, (3) to reduce dehydration by reducing the surface area of the nests, and (4) to gather food and building materials, such as rotten wood and humus, which accumulate around the tree base and stumps.
Three nests (22%) were epigeal (standing from the ground), however epigeal nests might be destroyed by ground-dwelling mammals (Figure 5). Mammals are probably ranked as the second top of the most important predators for termites; the first position is likely occupied by ants (Deligne et al., 1981; Wilson, 1971). Four of the 14 epigeal nests showed signs of having been attacked by ants, such as Camponotus gigas (Latreille, 1802), Pheidole sp. and Oecophylla smaragdina (Fabricius, 1775). Ants prey on termites and also often destroy their nests. The irregular-shaped nests clinging to the forest floor (Figure 5) are likely to be rebuilt from destroyed epigeal nests. Therefore, multiple physical and biotic factors on the forest floor might influence the diversity of nest architecture of T. propinquus.
Fig. 4. Nest of Termes propinquus attached to a stump, in a dipterocarp forest of Suaq Balimbing, North Sumatra (Suaq Balimbing Field Station; colony (SUAQ-TT-2017-C012).
Fig. 5. A rebuild nest of Termes propinquus after being destroyed probably by a mammal, in a dipterocarp forest of Suaq Balimbing, North Sumatra (Suaq Balimbing Field Station; colony (SUAQ-TT-2017-C022).
Acknowledgements: We thank the Termite Research Group (Universitas Syiah Kuala, Indonesia), Sugesti, M. Rapi, Tarmizi, M. Isa, Usman, and Mat Plin (Leuser Development Program, Indonesia), Manager and Field Staff at Suaq Balimbing Field Station for assistance in the field and laboratory. We are grateful to Katsuyuki Eguchi (Tokyo Metropolitan University, Japan), Seiki Yamane (Kagoshima University Museum, Japan) for support, Paul Eggleton and David Jones (Natural History Museum, UK) and staff at the Museum Zoologicum Bogoriense (MZB, Indonesia) for allowing the corresponding author to examine the type material. We thank to staff in the Forestry Department in Indonesia for their help and assistance during field surveys. Rudolf Scheffrahn (Florida University, USA) for facilitating Syaukani in taking specimen photos. This research was partly funded by the PMDSU Doctoral Program, the Ministry of Research, Technology and Higher Education, Indonesia (MRTHE) (Leader Syaukani: FY 2016-18), H-Index Research Grant 2020 (Leader Syaukani). Fundamental Grant, MRTHEI (Leader Syaukani FY2018-FY2020).
REFERENCES
- Bignell, D.E and P. Eggleton (2000) Termite in ecosystems. In: Abe, T., Bignell, D.E. & Higashi, M. (eds.). Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, the Netherlands.
- Bourguignon, T., M. Leponce, and Y. Roisin (2008) Revision of the Termitinae with snapping soldiers (Isoptera: Termitidae) from New Guinea. Zootaxa. 1769: 1-34.
- Cosarinsky, M (2004) Nest micromorphology of the Neotropical Termite Termes saltans (Isoptera: Termitidae). Sociobiology. 43(3): 1-11.
- Deligne, J., A. Quennedey, and M.S. Blum (1981) The enemies and defend mechanisms of termites. In: Hermann, H.R (ed.). Social Insect Academic Press, New York, USA.
- Eggleton, P (2000) Global patterns of termite diversity. In: Abe, T., Bignell, D.E. & Higashi, M. (eds.). Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, the Netherlands
- Engel, M.S., D.A. Grimaldi, and K. Krishna (2009) Termites (Isoptera): Their phylogeny, classification, and rise to ecological d Ame. Mus. Novi. 3650; 1–7.
- Gathorne-Hardy, F (2001) A review of the South-East Asian Nasutitermitinae (Isoptera: Termitidae), with descriptions of one new genus and a new species and including a key to the genera. J. Nat. His. 35: 1486-1506.
- Gathorne-Hardy, F.J (2004) The termites of Sundaland: A taxonomic review. Sar. Mus. J. 60: 89-133.
- Haviland, G.D (1898). Observations on termites; with description on new species. J. Linn. Soc. Zoo. 26: 358-442.
- Holmgren, N (1913-14) Wissenschaftliche Ergebnisse einer Forschungsreise nach Ostindien, ausgefuhrt im Auftrage der Kgl. Preuss. Akademie der Wissenchaften zu Berlin von H.v. Buttel-Reepen. III. Termiten aus Sumatra, Java, Malacca und 140 Ceylon. Gesammelt von Herrn Prof. Dr. v. Buttel-Reepen in den Jahren 19111912. Zool. Jahrbu. Abteilu. Syste. 36: 229-290.
- John, O (1925) Termiten von Ceylon, der Malayaischen Halbinsel, Sumatra, Java und den Aru-Inseln. Treubia. 6: 360-419.
- Krishna, K., D.A. Grimaldi, Krishna, and M.S. Engel (2013) Treatise on the Isoptera of the world. Bull. Ame. Mus. Nat. Hist. 377: 1-2704
- Pearce, M.J (1997) Termites biology and pest management. CAB International: 172.
- Roonwal, M.L and O.B. Chhotani (1989) The Fauna of India and the Adjacent Countries, Vol. 1, Zoological Survey of India: 672.
- Syaukani, S., G.J. Thompson, T. Yamasaki, S Othman, S. Muarrif, M.A. Sarong, D. Djufri, and K. Eguchi (2019) Taxonomy of the genus Longipeditermes Holmgren (Termitidae, Nasutitermitinae) from the Greater Sundas, Southeast Asia. Zoosyst. Evol. 95(2): 309-318.
- Thapa, R.S (1981) Termites of Sabah, Sabah Forest Record (12) 374.
- Tho, Y.P (1992) Termites of Peninsular Malaysia. Malayan Forest Records (36) 224.
- Wilson, E.O (1971) The Insects Societies. Harvard University Press: 548.
|