Nyambai Forest Park and Tanji Bird Reserve ( The Gambia )

From October 28 to November 05, 2013, we conducted a termite sampling in 3 protected sites in The Gambia (West Africa). Termites sampling is carried out in 100 m x 2 m transects repeated 3 times in each site. A total of 33 species of termites have been recorded. Of the 33 species, 22 are new to The Gambia. Additionnal measurements are given for several collected termite species. Euchilotermes arcuata Silvestri is elevated to the rank of species.


Study Sites
The Gambia is a small country in West Africa enclosed by the Senegalese territory (fig.1).
The climate is characterized by a short rainy season from July to September and a dry season the rest of the year.From the coast to the inland, rainfall (900-1,300 mm) declines and temperatures increase.In dry season, the inland regions have average temperature as high as 35°C, whilst the average temperature in the coastal regions ranges between 25° and 28°C.In wet season, average temperature can be below 25°C at the coast and up to 30°C in the inland.
The Termites were sampled from the Abuko Nature Reserve, Tanji Bird Reserve and the Nyambai Forest Park, wich are protected areas in the coastal region (fig.1).

Tanji Bird Reserve
The Tanji River Bird Reserve is located along the Atlantic Coast, in the Western Division, Kombo North, a few kilometers away from the fishing village Ghana town (13°23'06.67N,16°46'05.04''W).The reserve was established in 1993 and covers a surface area of 612 ha (6.12 km 2 ).The three transects locations are shown on the figure 3.  The soil is completely covered with thick layer of litter; few thriving grasses grow here and there on the finely sandy to muddy soil.The relative humidity is high in the morning and late in the evening.Monthly average of temperatures range are between 17-24 °C for the minima and 31-33°°C for the maxima.

Sampling Methods
Within each of these above sites the sampling method, a derivative of Jones & Eggleton [11] sampling method, was carried out using transect (3 transects/site) with 100 m long and 2 m wide.The duration of the sampling is not limited but depends on the time required to cover the entire transect.In each transect, a thorough search of termites is carried out in the soil, the litter, the dead wood, in stump of trees, under the bark of trees, and the arboreal termite nests.
The encountered termite soldiers, workers, swarming individuals, kings or queens are collected and kept in ethanol 70 % within labeled containers bearing the name of the site, the date, and the micro-habitat.

Species identification
Identification begins with a direct observation under the microscope with a comparison, if necessary, of specimens to be identified with reference specimens from the IFAN (Institut fondamental d'Afrique noire) collection identified by W. A. Sands and/or with reference works by Silvestri [12,13], Sjöstedt [3], Emerson [14], Grassé [15,16], Bouillon & Mathot [17] and Roy-Noël [18].The more focused works of Sands for Nasutitermitinae [19] and for the genus Amitermes [20] were also used.Identification of soldierless species of Apicotermitinae has been made after sands [6,8] on the basis of the morphology of the digestive tube: the mesenteron-proctodeum junction and the enteric valves, dissected, are observed under stereomicroscope.For the species of Cubitermes, we used the key of Josens [21] and also consulted Pr.Josens.In addition to the external morphology of the soldiers, workers enteric valves were dissected for species identification.
The head and mandible measurements are: -head width corresponding to the maximum width in dorsal view; -head length measured in dorsal view from the occiput to the base of labrum (soldier) or anterior of clypeus (worker), -length of left mandible measured in dorsal view, from the lateral most proximal visible point to the apical point.

Termite diversity in the three sites
Thirty one (31) termite species have been recorded in the three sites.They belong to the following two families, six subfamilies and nineteen genera.

Termites diversity in Abuko Nature Reserve
At Abuko Nature Reserve, 27 species of termites belonging to 2 families and 5 subfamilies were recorded (table 1).The variable number of collected species between transects in the site (as shown in table 1) suggests a certain heterogeneity of the termite distribution.
In terms of functional diversity, there is predominance of the humivorous termites with 11 species followed by the fungus-growing Macrotermitinae which are represented by 9 species.
The xylophagous (6 species) and the haverster termites (1 species) are the least diverse.This type of termite assemblage in Abuko is characteristic of a forestry profile.

Termites diversity in Nyambai Forest Park
The species richeness of termites in Nyambai Forest Park is of 20 species (table 2).At functional level, there is still a greater diversity of the humivorous termites represented with 12 species followed by the fungus-growing termite (8 species).The harvester termites and the xylophagous termites are represented each by 1 species.
The spatial distribution of the termite species is rather heterogeneous: 12 species are recorded in the station 1, 10 species in station 2 and 16 species in the station 3. The species richness and spatial distribution heterogeneity in Nyambai Forest are less important than in Abuko and could be associated with the relatively low botanical diversity in this artificial site.

Termites diversity in Tanji Bird Reserve
At Tanji Bird Reserve, with 20 species, the species richness is less important than in the other two sites (table 3).The spatial distribution is also heterogeneous in this site as 15 species are recorded in the station 1, 12 species in the station 2 and 4 species in the station 3.
In terms of functional diversity, the fungus-growing termites (11 species) largely dominate the humivorous (5 species) and the xylophagous (1 species).

New termite species recorded in The Gambia
Among  Odontotermes erraticus Grassé, 1944 The head of the soldier (figure 5) is yellow-orange in colour or dark-brown.The antennae are with 16 articles.The left mandible shows a marginal tooth.The two soldier head measurements are: head length 1.61 mm and 1.64 mm, head width 1.27 mm and 1.28 mm, left mandible length 1.10 mm and 1.15 mm, hind tibia length 1.09 mm.

Figure 5. Head of of Odontotermes erraticus Grassé 1944 soldier in dorsal (left), profile (middle) and ventral (right) views
The large worker have 17 articles in their antennae whereas the small worker individuals have 16 articles in their antennae.Head measurements are shown in table 4 and table 5. Cubitermes severus Silvestri, 1914 It is a species characteristic by the shape (fig.6) and the size (table 6) of its soldier.The table 7 shows the dimensions of workers.It is the largest size Cubitermes in the collection.Cubitermes severus has been collected both in nests without cap (fig.7a) and in typical mushroom nests (fig.7b).The column of the nest is much higher than that of Cubitermes near proximatus.This mound builder species occupies alone his nest or shares it with the inquilines Promirotermes holmgreni, Noditermes cristifrons and Pericapritermes urgens.The observation of the enteric valves of the workers of these Cubitermes shows their proximity to C. proximatus.However, based on the morphology, the color and the dimensions of the soldier's head, we divided them into two morphotypes.

Morphotype 1 of Cubitermes near proximatus
It is a species recognizable by the shape and the ochraceus colour of the head of its soldiers (fig.8).The table 8 shows the dimensions of the soldier and the table 9 those of worker.Euchilotermes arcuata Silvestri, 1914 The head of E. arcuata soldier (fig.11) is distinctly rectangular in shape and yellowish in color with light brown mandibles.The mandibles are strongly curved.The labrum is long and wide with two apical large and rounded lobes.The measurements of the soldiers are noted in table 12 and those of the workers in the table 13.The specimens so designated seem different from all known species of the genus.
However more specimens, particularly of soldiers, are needed before the description of a new species.

Noditermes cristifrons (Wasmann, 1911)
The measurements of soldiers of Noditermes cristifrons recorded in table 14.The nests of Noditermes cristifrons (fig.12), are free standing or backed to a tree which affects in this case the shape.However in both cases, the nest displays a scaly appearance.Noditermes cristifrons occupies alone its nest or shares it with Pericapritermes urgens.

DISCUSSION
The compilation of the references on the termites of The Gambia gives for this country, 30 species.The present study has extended the number of termites species recorded from The Gambia to 46.On the overall 31 species that have been newly collected, nineteen (16) species are new for The Gambia of which one is probably new for science.
Of the thirty one (31) species recorded during this study, only the morphotype 2 of Cubitermes sp.near proximatus and Euchilotermes arcuata are not known in Senegal.
Odontotermes, described from Niger by Grassé [16], was indeed supposed to be restricted to Niger [5] Ndiaye [23] points out for the first time its occurrence in Senegal.
As one of the newly added species to Gambia's termite, its presence is seemingly thoroughout West Africa.O. erraticus would be widespread in the Sudano-Sahelian zones of West Africa.Its presence was probably hidden by numerous misidentifications, particularly confusions with the species O. vulgaris and O. latericius of southern Africa.
As Ruelle [24] pointed out, the genus Odontotermes is the most difficult of the Macrotermitinae.
The genus Euchilotermes, exclusively known in the Ethiopian region comprises four described species [5].E. quadriceps described by Emerson [14] is known in Congo-Zaire (now RD Congo) and Malawi.E. umbraticola described by Williams [25,26] is a species of East Africa (Kenya, Tanzania) [5].Silvestri described E. tensus and the two varieties E. tensus var.acutidens and E. tensus var.Arcuata [13].The variety acutidens has been elevated to the rank of species by Emerson [14] on the basis of the following differences: «mandibles more prolonged and curved at apex than with M. tensus, the teeth are smaller and sharper with a wider gula».
The comparison of E. tensus and E. arcuata shows significant differences: more fleshy labrum in E. arcuata; mandibles are curved at the middle in E. arcuata and straight in E. tensus; stronger marginal teeth at the base of the mandibles in arcuata; the shape of the indentation below the marginal teeth is different in the two species; upper side of the head, in profile view, is convex in E. arcuata and concave in E.
On the base of these differences, which are of the same order as those which have justified the elevation of the E. acutidens variety to the rank of species, we consider E. arcuata as a distinct species from E. tensus.
According to Krishna et al. [5], Microtermes hollandei Grassé is put in synonymy with M. lepidus Sjöstedt by Emerson (unpublished catalog).This synonymy is fully justified considering the perfect resemblance between the two species.Grassé [15], author of the original provisional description of M. hollandei, found himsel minor the differences between the two species and explained them by geographical distribution.However, it should be noted that the specimens used in the description of M. lepidus [27] and M.
Microcerotermes fuscotibialis is easily distinguished by the morphology, the size and the ecology from M. solidus, M. parvus, and M. parvulus, which are referred to as small Microcerotermes [22].The difficulties in the discrimination of these small Microcerotermes are the source of multiple misidentifications.Described from tropical Africa and cited from all African regions, M. parvulus was also recorded from Saudi Arabia [28].This wide distribution can be explained by a strong plasticity of the species or due to misidentification, the most parsimonious hypothesis.As noted by several authors [29,30,22,23], we believe that the revision of the African Microcerotermes is necessary.

Figure 1 .
Figure 1.Location of the study sites Abuko Nature Reserve, Tanji Bird Reserve and Nyambai Forest Park

Figure 2 .
Figure 2. Transects of termite sampling at Abuko Nature Reserve

Figure 3 .
Figure 3. Transects of termite sampling at Tanji Bird Reserve

Figure 4 .
Figure 4. Transects of termite sampling at Nyambai Forest Park

Figure 8 .
Figure 8. Head of morphotype 1 of Cubitermesnear proximaus Silvestri 1914 soldier in dorsal (left) and ventral (right) views Morphotype 2 of Cubitermes near proximatus The soldier of the morphotype 2 (fig.9) is clearly larger (table 10).Morphologically, differencies are noted on the lateral margin of the head, which is less convergent, and the mandibles that are less curved in C. proximatus.The indentations at the base of the mandibles (ventral view of fig.8 and fig.9) are also distinctive features between the two morphotypes.

Figure 9 .
Figure 9. Head of Cubitermes proximatus Silvestri 1914 soldier in dorsal (left) and ventral (right) viewsThe measurements of the morphotype 2 workers are shown in the table 11.

Table 2 . The termites species collected in different stations in Nyambai Forest Park
the 31 termite species recorded in Abuko Nature Reserve, Nyambai Forest Park and in Tanji Bird Reserve, 19 termite species are newly recorded from The Gambia.

Table 11 . Measurements (mm) of workers of of the morphotype 2 Cubitermes near proximatus Silvestri, 1914 Worker Range Mean Number
The mushroom nests of morphotype 2 are small in size (fig.10).The column is often sufficiently developed to allow a clear distinction with the cap.The nests are occupied solely by the builber or shared with inquilines such as Allognathotermes hypogeus, Euchilotermes arcuata, Microtermes grassei and/or Promirotermes holmgreni infera. Preprints(