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Termite Communities Along a Disturbance Gradient in a West African Savanna insects Article Termite Communities along A Disturbance Gradient in a West African Savanna Janine Schyra 1,* and Judith Korb 1,2 1 Behavioral Biology, University of Osnabrueck, Barbarastr. 11, D-49076 Osnabrueck, Germany; [email protected] 2 Evolution and Ecology, Albert-Ludwigs-University Freiburg, Hauptstr. 1, D-79104 Freiburg im Breisgau, Germany * Correspondence: [email protected] Received: 23 November 2018; Accepted: 30 December 2018; Published: 8 January 2019 Abstract: (1) Background: Termites are important ecosystem engineers, crucial for the maintenance of tropical biodiversity and ecosystem functioning. But they are also pests which cause billions of dollars in damage annually to humans. Currently, our understanding of the mechanisms influencing species occurrences is limited and we do not know what distinguishes pest from non-pest species. (2) Method: We analyzed how anthropogenic disturbance (agriculture) affects species occurrences. We tested the hypothesis that strong disturbance functions as a habitat filter and selects for a subset of species which are major pests of crop. Using a cross-sectional approach, we studied termite assemblage composition along a disturbance gradient from fields to 12-year-old fallows in a West African savanna. (3) Results: We reliably identified 19 species using genetic markers with a mean of about 10 species—many of them from the same feeding type—co-occurring locally. Supporting our hypothesis, disturbance was associated with environmental filtering of termites from the regional species pool, maybe via its effect on vegetation type. The most heavily disturbed sites were characterized by a subset of termite species which are well-known pests of crop. (4) Conclusion: These results are in line with the idea that strong anthropogenic disturbance selects for termite pest species. Keywords: termite; community assembly; pest; disturbance; West Africa 1. Introduction Termites are major ecosystem engineers with crucial roles in decomposition, soil fertility, hydrology, and species diversity [1,2]. Concomitantly, a few species are also major pests [3]. Despite their importance, we hardly understand what determines the occurrence of different termite species and what distinguishes pest from non-pest species. Niche overlap between different species seems to be substantial as termites are detritivores and only four major feeding types are distinguished [4]: Dead wood feeders (group I); dead wood, micro-epiphytes, leaf litter and grass feeders (group II); and humus feeders (group III) and true soil feeders (group IV) (reviewed in [5,6]). In African savannas up to 20 higher termite species (Termitidae) of feeding group II co-exist [7–11]. These group II species can be sub-divided into two feeding type specialists, grass-feeding Trinervitermes (group IIg) and fungus-growing Macrotermitinae (group IIf). The latter cultivate an obligate symbiotic fungus within their colonies, which they provision with a broad range of dead plant material [12]. The similarity of termites’ food niches implies that competitive interactions are important in shaping local savanna assemblages [13,14]. However, recent analyses suggest that random processes play an important role in species assembly in an undisturbed West African savanna, with a structuring effect by one large mound building species, Macrotermes bellicosus [10]. Additionally, first evidence implies that assembly processes change to more environmental filtering with disturbance [11]. This suggests that disturbance Insects 2019, 10, 17; doi:10.3390/insects10010017 www.mdpi.com/journal/insects Insects 2018, 9, x FOR PEER REVIEW 2 of 12 Insects 2019, 10, 17 2 of 12 assembly processes change to more environmental filtering with disturbance [11]. This suggests that can,disturbance not only can, lead not to aonly decline lead in to species a decline richness, in species but alsorichness, to a change but also of to the a change processes of thatthe processes structure speciesthat structure assemblages. species assemblages. In the current study, wewe investigatedinvestigated termitetermite assemblage composition of different-ageddifferent‐aged fallows (measured as the the time time since since they they were were last last cultivated) cultivated) in ina West a West African African savanna savanna region region in Togo. in Togo. By Bydoing doing this, this, we we aimed aimed at atanalyzing analyzing how how species species assemble assemble over over time time from from a a strong strong anthropogenically anthropogenically disturbed habitat to less degradeddegraded settings.settings. We We expect that termite assemblages of younger-agedyounger‐aged fallows areare more more strongly strongly structured structured by by environmental environmental filters. filters. To test To this, test wethis, first we identified first identified all species all occurringspecies occurring in the different in the different assemblages assemblages using morphological using morphological and genetic and markers. genetic Amarkers. genetic A approach genetic isapproach necessary is necessary to unambiguously to unambiguously identify all identify termites. all termites. To reveal To assembly reveal assembly processes, processes, we then we applied then phylogeneticapplied phylogenetic community community analyses thatanalyses explicitly that test explicitly real, studied test real, communities studied communities against communities against thatcommunities are drawn that at randomare drawn from at therandom regional from species the regional pool. Finally, species we pool. investigated Finally, whetherwe investigated species fromwhether young-aged species from fallows young correspond‐aged fallows to pest correspond species. to pest species. 2. Materials and Methods 2.1. Termite Sampling Sampling Termites werewere systematicallysystematically collectedcollected whenwhen theythey were most active, that is, during the beginning ◦ 0 ◦ 0 of the rainyrainy season,season, near near the the Oti-Keran Oti‐Keran National National Park Park in in northern northern Togo Togo (West (West Africa; Africa; 10 10°1717 to′ 10to 10°0808 N;′ ◦ 0 ◦ 0 0N;28 0°28to′ 0to51 0°51E,′ FigureE, Figure1). This 1). This region region is a typicalis a typical West West African African savanna savanna lying lying in the in center the center of the of West the SudanianWest Sudanian biome biome (mean (mean annual annual precipitation: precipitation: 1100 mm; 1100 Worldclim mm; Worldclim database). database). Termites Termites were collected were incollected 2012 from in 2012 seven from fallows seven of agefallows 0, 2, of 4, 6,age 8, 100, 2, and 4, 126, 8, years. 10 and In 2014 12 years. we added In 2014 six we new added fallows six of new age 0,fallows 0, 1, 2, of 10 age and 0, 100, years.1, 2, 10 Our and sampling 10 years. regimeOur sampling was constrained regime was by constrained the availability by the of fallowsavailability with of a knownfallows age.with a known age. Figure 1. LocationLocation of of the the the the Oti Oti-Keran‐Keran National National Park Park in innorthern northern Togo Togo and and distribution distribution of the of the 13 13sampled sampled fallows fallows in inthe the study study area. area. Single Single lines lines are are small small roads roads and and the the double double line line in in grey grey is is a ariver. river. Sampling was done using a standardized belt transect protocol firstfirst developed for sampling termites in forests [[15]15] and then adapted to savannas [[9].9]. In short, the protocol consists of a thorough search of dead plant material on the ground, on and in trees and mounds, as well as soil sampling to assess termitetermite diversitydiversity [ 15[15].]. Plot Plot size size was was one one hectare hectare with with three three transects transects each each measuring measuring2 m 2× m50 × m50, dividedm, divided into into ten 2 ten m × 25 m m × sections, 5 m sections, arbitrarily arbitrarily located within located one within plot. Theone three plot. transects The three characterize transects onecharacterize study plot one (i.e., study the numberplot (i.e., of the species number occurring of species within occurring one hectare). within Hence,one hectare). our sample Hence, size our is thesample number size ofis the plots, number not the of number plots, not of the replicates. number Each of replicates. transect section Each transect was searched section systematically was searched systematically for termites for 15 min by a trained person. Additionally, we sampled eight soil scrapes Insects 2019, 10, 17 3 of 12 for termites for 15 min by a trained person. Additionally, we sampled eight soil scrapes per transect section measuring 15 cm × 15 cm × 10 cm. All encountered termites were stored in 99% pure ethanol for subsequent molecular analyses. As in the former studies [9,15,16], we chose a plot size of one hectare because the foraging ranges of termite colonies is within 100 m [16]. Hence one hectare represents the local scale where interactions between colonies occur, i.e., it reflects the Darwin-Hutchinson-Zone, which is most relevant to the study assembly of local communities [17]. We specifically selected plots with and without active M. bellicosus mounds as it is the main mound builder and an important ecosystem engineer, which may influence termite communities. All samples were identified to the species level: Samples containing soldiers were first identified using the keys by Webb [18] and Sands [19], and then sequenced to obtain an unambiguous
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