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Bourguignon, T. (2010). The Anoplotermes group in French Guiana : systematics, diversity and ecology (Unpublished doctoral dissertation). Université libre de Bruxelles, Faculté des Sciences – Sciences biologiques, Bruxelles.

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D 03780

UNIVERSITÉ LIBRE DE BRUXELLES. UNIVERSITÉ D'EUROPE

Service d’Évolution Biologique et Écologie

ULB

The Anoplotermes group in French Guiana:

systematics, diversity and ecology

Dissertation submitted in partial flilfillment of the requirements for the degree of Doctor in Science (Biological Sciences) by Thomas Bourguignon

2010

Supervisor

Yves Roisin Université Libre de Bruxelles (Belgium) Co-supervisor

Maurice Leponce Institut Royal des Sciences Naturelles de Belgique (Belgium) Jury members

Jean-Christophe de Biseau Chantal De Ridder

Guy Josens

Corine Rouland-Lefèvre

Université Libre de Bruxelles (Belgium) Université Libre de Bruxelles (Belgium) Université Libre de Bruxelles (Belgium)

Institut pour la Recherche et le Développement, Bondy (France)

Université L bre de Bruxelles

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Service d’Évolution Biologique et Écologie

The Anoplotermes group in French Guiana:

systematics, diversity and ecology

Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor in Science (Biological Sciences) by Thomas Bourguignon

2010 Supervisor

Yves Roisin Université Libre de Bruxelles (Belgium) Co-supervisor

Maurice Leponce Institut Royal des Sciences Naturelles de Belgique (Belgium) Jury members

Jean-Christophe de Biseau Chantal De Ridder

Guy Josens

Corine Rouland-Lefèvre

Université Libre de Bruxelles (Belgium) Université Libre de Bruxelles (Belgium) Université Libre de Bruxelles (Belgium)

Institut pour la Recherche et le Développement, Bondy (France)

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Remerciements

L'aboutissement de ma thèse n'est pas uniquement le fruit d'un travail personnel, mais plutôt le résultat de nombreuses collaborations et du soutien inconditionnel de mes proches.

Je remercie chaleureusement mon chef, Yves Roisin, pour m'avoir soutenu durant toutes ces années. Tes connaissances encyclopédiques et ta méthodologie m'ont fait prendre goût au monde des termites, que je compte bien ne pas quitter de sitôt. J'espère encore travailler avec toi dans les années à venir, et pourquoi pas, visiter l'Afrique.

Je remercie également Maurice Leponce pour sa disponibilité, ses remarques constructives et ses mises en garde qui m'ont souvent été bien utiles.

I aiso thank Honza Ëobotnîk for the good time spent under tropics and other places. I really enjoy your company, great ideas such as boiling the Solenopsis, and working with you. l'm waiting for our next fruitfui collaboration.

Merci à tous les membres du laboratoire d'Évolution Biologique et Écologie, particulièrement ceux de mon bureau, pour l'ambiance conviviale dans laquelle il fait bon de travailler.

Merci à mes parents pour m'avoir toujours soutenu dans ce que J'ai pu entreprendre, ainsi qu'à Andréa pour ta spontanéité et ton autodérision.

Et enfin, merci à ma petite femme, Josepha, pour ta Joie de vivre, pour les bons moments que tu me fais passer, mais aussi pour ton sale caractère qui me manque tellement durant mes missions à l'étranger. Je t'aime très fort.

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Termites are an important animal taxon in tropical rainforests, where their species richness is much higher than in any other ecosystem. They basically feed on ail kind of végétal organic matter, from sound wood to highly mineralized soil organic matter. However, this food source diversification only occurs in the Termitidae, sometimes called “higher termites”, whereas other families are only wood- or grass-feeders. Soil-feeding termites are extremely abondant in Afrotropical and Neotropical régions where they probably constitute more than half the termite species richness. Unfortunately, they are poorly known in comparison to wood- feeding représentatives. This is especially true for the Anoplotermes-group, which represents the most unexplored termite lineage, as many aspects of its fundamental biology still remain mysterious. This work aims at shedding light upon the ecology and biodiversity of this strictly soil-feeding group, and comprises the following sections. (1) Standardized sampling of seven forest sites in French Guiana revealed that with few exceptions, wood-feeding termites did not présent a clear spécialisation toward any sites. By contrast, the Anoplotermes-group species, as well as other soil-feeders, are specialised toward some particular kind of forest. This was especially true for two sites presenting a singular physiognomy: a low forest growing on the slope of the Nouragues inselberg and a palm swamp. Such a spécialisation likely contributes to species diversification, and thus, enhances the total soil-feeding termite species richness.

(2) Using and ô'^N isotopic ratios, we also found that species spécialisation occurs along a humification gradient in the Anoplotermes-group, from the interface between decayed wood and soil to deep soil poor in organic matter. Therefore, at least two factors favored the Anoplotermes-gromp species richness in the soil, despite the weak evidence for spatial or temporal séparation between species. Species specialization reduces interspecific compétition to species which feed within the same range of organic matter décomposition State. (3) This mechanism is likely not restricted to Anoplotermes-growp species as ô'^N was found to vary a lot among soil-feeding termites as a whole. Soil-feeding termites include species with varions diet requirements and therefore separate ecological niches. This diet diversification did not occur randomly along the termite phylogenetic tree and closely related species tend to feed on the same substrate. (4) At the intraspecific level, we hypothesized that compétition constraints the population dynamics of colonies. Indeed, in Anoplotermes banksi, we found that mature nests are overdispersed. New nests are mainly found at a distance from the established nests, especially in gaps left by recently dead nests. Whether this pattern results from nest site sélection or from compétitive exclusion of new nests is unknown, but it highlights anyway the compétitive interactions in soil-feeding termites of the Anoplotermes-gioup. (5) In view of the

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local species richness and diversity of the Anoplotermes-group species, the number of described species remains remarkably low. We thus examined most of the available type material of this group and found that only 30 described species are valid in the South American Anoplotermes-group, whereas 80% of the species we collected are new to science.

This disproportion between what is known and what actually exists pinpoints the need for a spécial effort towards the Anoplotermes-group, to fill one of the major gaps in our présent knowledge of termites.

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Introduction ...1 Aims of the work... 23 Article 1: Beta-Diversity of Termite Assemblages among Pristine French Guiana Rainforests

...25 Article 2: Feeding ecology and phylogenetic structure of a complex neotropical termite assemblage, revealed by nitrogen stable isotope ratios... 43 Article 3: Niche différentiation among neotropical soldierless soil-feeding termites revealed by stable isotope ratios... 61 Article 4: Is the spatio-temporal dynamics of colonies in soldierless humus-feeding termites, Anoplotermes spp. (Isoptera: Termitidae), shaped by intraspecific compétition? ... 67 Article 5: Towards a révision of the Neotropical soldierless termites: redescription of the genus Anoplotermes, taxonomy and phylogeny of prévalent species of this group... 85 Discussion and perspectives...109 ANNEXES... 115 Annexes 1: Insights into the termite assemblage of a neotropical rainforest from the spatio­

temporal distribution of flying alates...117 Annexes 2: The frontal gland in workers of Neotropical soldierless termites...127

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The Anoplotermes group in French Guiana - Introduction 1

Introduction

Part I: Soil organic matter as a diet The soil

Soils constitute a heterogeneous environment whose strueture and eomposition is greatly influenced by environmental and biological factors. Since these conditions are not uniform across the earth surface, many different kinds of soil occur. At the global scale, latitude, or more generally climatic régime, is the major factor influencing soil formation whereas topography is the dominant factor at the régional scale. Soil composition may also vary within a single site (e.g. particle granulometry), making soil type heterogeneously distributed at the local scale (Lavelle and Spain 2001).

The soil is a mixture of various materials from different origins. The inorganic particles form the bulk of this mixture both in term of mass and area, whereas the soil organic matter is mainly located in the top 20cm soil layer and comprises a few per cent of the total mass of the soil (Sanchez et al. 1982, Post et al. 1982, Zhong et al. 2000). Organic matter compounds and particles may be classified according to their Chemical composition, their lability or their morphology. Following this latter classification, soil organic matter occurs under 5 different forms: (i) the live organisms which include bacteria, invertebrates (e.g.

nematodes, earthworms, oribatid mites, springtails, termites...), plant roots, fimgal hyphae, algae; (ii) dead organism remains still retaining part of their original shape; (iii) sécrétions produced by organisms such as earthworms and mollusks and animal feces (iv) détritus from leaf litter and végétation; and (v) humic substances which resuit from bacterial activity or spontaneous Chemical reactions (Lavelle and Spain 2001).

Apart from the live organisms which participate to organic matter dégradation, other above-mentioned forms are the product of this dégradation. Freshly dead organisms are fractionated and decomposed under the action of different agents, such as bacteria, microarthropods or fimgi. This dégradation does not act on ail Chemicals in the same way and some molécules such as lignin and tannins are particularly récalcitrant. More precisely, their polyphenolic cycles are particularly stable and stay untouched for long time. These aromatic compounds therefore accumulate during organic matter dégradation and condensate with other compounds such as carbohydrates and proteinaceous materials to form heavier molécules: humic and fulvic acids (Schulten and Schnitzer 1995, 1998, Piccolo 2002)

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Feeding on the soit

Soil is an abundant habitat hosting a diversified fauna composed of nematoda, earthworms and many arthropod taxa such as mites, myriapods, isopods, collembolans, ants, termites, etc.

Members of these animal groups generally feed on bacteria, roots, fimgi, other animais or on leaf litter but only rarely on the humic substance itself. However, some earthworms and termites specialised on this latter food source and became among the major decomposers of soil organic matter in varions ecosytems.

Earthworms are traditionally classified into 3 ecological types: (i) epigeics which both live and feed within the litter layer; (ii) anecics which live in soil burrow but feed on the litter layer that they mix with soil; and (iii) endogeics or geophagous earthworms which both live and feed on deeper soil layers (Bouché 1977). The latter group may additionally be subdivided into 3 categories: (1) polyhumics are small species which selectively ingest organic particles; (2) mesohumics are of medium size and feed on the top 15cm soil layer without any sélection of the particles they ingest; and (3) oligohumics are large worms living on deep soil poor in organic matter (Lavelle 1981). This classification reflects the wide range of organic matter kinds earthworms may feed on. A précisé détermination of the components assimilated within the digestive tract is more complicated as significant enzymatic activity occurs in the gut, but it is not clear how much is due to the worms themselves and to the soil microflora (Curry and Schmidt 2007). Carbohydrates and proteins appear readily digested as well as some cellulose and phenolic compounds, but not lignin (Curry and Schmidt 2007).

Some species might also supplément their diet with bacteria and protozoa (Lavelle 1988).

Organic matter assimilation greatly differs according to earthworm ecology; epigeic species may assimilate up to 75% of the soil organic matter they ingest whereas in geophagous species it ranges between 1% and 19% (Lavelle and Spain 2001, Curry and Schmidt 2007).

Finally, the microbial composition of the earthworm gut generally reflects that of ingested soil or plant residues, but some species with specialised feeding habits may possess a distinctive gut microflora (Curry and Schmidt 2007).

Whereas earthworms are distributed worldwide, humivorous termites are limited to tropical and subtropical areas (Lavelle and Spain 2001, Davies et al. 2003a). A classification of termites into feeding groups has been proposed by Donovan et al. (2001). It comprises four groups (I - IV), which supposedly include species feeding on increasingly degraded substrates. Group I comprise ail non-Termitidae, wood- or seldom grass-feeders. Group II includes wood-, grass- or litter-feeding Termitidae (see Table 1 for a current classification of

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The Anoplotermes group in French Guiana - Introduction 3

Isoptera). Groups III and IV comprise species feeding on very rotten wood, at the wood-soil interface, or on mineral-rich soil, and may collectively be called "soil feeders". The transition from wood to soil-feeding is a key event in the history of the Termitidae. Noirot (1992) suggested that this transition occurred several times independently during Termitidae évolution, but Eggleton and Tayasu (2001) proposed that a single acquisition of soil-feeding habits occurred at the origin of a clade comprising ail Termitidae except the fungus growers (Macrotermitinae).

Family Subfamily Diet Presence in

(feeding group) French Guiana Mastotermitidae

Termopsidae Porotermitinae

Wood (I) Wood (I)

Termopsinae Wood (I) -

Stolotermitinae Wood (I) -

Hodotermitidae Grass (I) -

Kalotermitidae Wood (I) +

Serritermitidae Wood (I) +

Rhinotermitidae Rhinotermitinae Wood (I) +

Prorhinotermitinae Wood (I) -

T ermitogetoninae Wood (I) -

Psammotermitinae Wood (I) -

Stylotermitinae Wood (I) -

Coptotermitinae Wood (I) +

Heterotermitinae Wood (I) +

Termitidae Macrotermitinae Fungi (II) -

F oraminitermitinae Soil (III) -

Sphaerotermitinae Wood (II) -

Apicotermitinae Soil (III, IV) -1-

Syntermitinae Wood, litter, soil (II, III, IV) + Nasutitermitinae Wood, litter, soil (II, III, IV) +

Termitinae Wood and soil +

Table 1. Classification of extant termites, diet and occurrence in French Guiana (after Davies 2002, Bourguignon et al. 2009); feeding groups according to Donovan et al. (2001).

Soil-feeding termites are able to select small soil particles, richer in organic matter but of poor quality and récalcitrant to décomposition (Brauman et al. 2000, Lavelle and Spain 2001). Additionally to this behavioural adaptation, they differ from wood-feeders by morphological characters, mainly in the architecture of the digestive tract (Noirot 1995, 2001). They hâve a longer highly compartmentalized hindgut allowing an increase of the

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transit time (Fig. 1), with first, second and third hindgut compartments having strongly alkaline pH, up to 12 (Bignell and Eggleton 1995, Brune and Kühl 1996, Brauman et al.

2000). This extremely high pH allows an alkaline hydrolysis of the food bolus before microbial dégradation (Bignell and Eggleton 1995, Brune 1998). Additionally, a radial oxygen gradient occurs in the hindgut and allows the dégradation of the organic matter in aerobiosis towards the periphery of the gut lumen and in anaerobiosis in its centre (Brune

1998). The high pH and the oxygen gradient are not spécifie to soil feeders but constitute a general trend in Termitidae; however, they likely contribute to the food source diversification in the family (Brauman et al. 2000). Like ail Termitidae, soil-feeding termites are associated with symbiotic bacteria helping in the digestion of the material they ingest. The précisé composition of the assimilated Chemicals is still not fully resolved but could include tannin- protein complexes, polyaromatic compounds and humic components of the soil (Brauman et al. 2000).

Fig. 1. Unrolled digestive tract of; A. Kalotermes flavicollis; B. Ruptitermes xanthochiton (modified from Noirot and Noirot-Timothée, 1969; Mathews, 1977).

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The Anoplotermes group in French Guiana - Introduction 5

Part II: The soldierless Apicotermitinae: insight into a poorly known ecologically dominant tropical taxon

Introduction

With their populous colonies and nests reaching up to several man heights, termites form a conspicuous component of tropical ecosystems. They are extremely abundant in tropical rainforests and savannas where they represent the most abundant animal taxa, accounting for a large part of the total animal biomass (Eggleton et al. 1996, Bignell and Eggleton 2000, Ellwood et al. 2002). These two characteristics make them essential targets for understanding both the mechanisms leading to complex social Systems like eusociality, and the flinctioning of ecosystems.

Among the major independent lineages of eusocial insects, ants are by far the most studied, whereas termites hâve received much less attention in spite of their comparable abundance. Similarly, a few termite clades concentrate the attention of most researchers, while others are almost completely neglected. This is especially true for the Apicotermitinae, which constitute the least studied termitid subfamily, with many fundamental aspects of their biology still remaining unexplored. For instance, a search in the Web of Science for the flagship genus of neotropical Apicotermitinae, Anoplotermes, yields no more than 30 references published after 1990; by contrast, about 1200 references will be found for the généra Coptotermes or Reticulitermes. Our global view of the termite world is thus strongly biased towards a few economically important généra, and passes over one of the most ecologically important and diverse taxa whose workers achieved many new adaptations allowing them to abandon the soldier caste.

The literature focusing on Apicotermitinae is scarce and many punctual observations scattered over 100 years of scientific research are sometimes diffîcult to access. Here, we critically review the existing sources directly focusing on Apicotermitinae, as well as those which provide more casual information.

Systematics and Phylogeny The Apicotermitinae

The subfamily Apicotermitinae was created for a few Termitidae généra on the basis of the anatomy of their worker digestive tract (Grassé and Noirot 1954). Sands (1972) revised the

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subfamily and included in it ail the soldierless termites previously lumped in the genus Anoplolermes. The Apicotermitinae form a monophyletic group (Inward et al. 2007), among which a large clade is the Anoplotermes-group, characterised by the loss of the soldier caste.

Species détermination

Some décades ago, termite taxonomy was mainly based on the extemal morphology of soldiers and alate imagos, whereas worker morphology was considered unimportant (e.g.

Holmgren 1912, Emerson 1925, Snyder 1926). However, most species of Apicotermitinae are soldierless, and the simultaneous collection of alates and workers is difficult due to the seasonal development of alates and the subterranean lifestyle of many species. Most early termite taxonomists therefore neglected the soldierless Apicotermitinae, whose richness was greatly underestimated until Sands's (1972) révision of African species. Early species descriptions were based on alates only and were often inaccurate: for instance, of 43 described species from the Neotropics, at least 10 are junior synonyms (Bourguignon and Roisin, Personal observation).

In absence of a soldier caste, Grassé and Noirot (1954) introduced a new set of taxonomie characters, requiring a close examination of the digestive tube. Two segments are particularly important: the junction between midgut and hindgut and the enteric valve. The midgut-hindgut junction may vary a lot in shape, from straight and circular to oblique and elliptical, or developed in a mixed segment (Noirot and Kovoor 1958, Noirot 2001). The enteric valve is a short segment, located at the end of the first proctodeal segment and partly invaginated into the paunch (Noirot and Kovoor 1958, Noirot 2001) (Fig. 2). It is primarily composed of 6 armed ridges (or cushions) with a radial symmetry, but diversified in many ways in the Apicotermitinae: development of the ridges and often sclerotized armatures such as a bunch of spines, a crown of thoms, dot-like spines... (Fig. 3). Other characters such as the relative development and disposition of the varions hindgut segments, the shape of mandibles or the shape and pilosity of legs can also be used for taxonomie purposes but give a lower resolution and are thus of secondary importance as taxonomie criteria.

Species diversity and distribution

Sands (1972) First revealed the actual diversity of the Apicotermitinae when he removed the African members of the group from the genus Anoplolermes, whose type-species is the neotropical A. pacificus. He distributed the 60 African species into 16 new généra, putting

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The Anoplotermes group in French Guiana - Introduction 7

Fig. 2. Schematic drawing of the worker digestive tract in dorsal (left drawing) and ventral (right drawing) view of: A. Grigiotermes bequaerti; B. Ruptitermes sp.; C. Aparatermes cingulatus', D.

Anoplotermespacificus. PI: first proctodeal segment; P3: paunch; P4: colon; P5: rectum; c: crop; mg:

midgut. Grey arrows point to the mixed segment and black arrows point to the enteric valve.

forward that the soldierless termites previously labelled as Anoplotermes actually form a heterogeneous group. Despite the enormous contribution of this pioneer work to termite systematics, the real diversity of the group is far from being completely resolved. Many new species were not described by Sands (1972) because alates were absent from collections. For example, 11 new species were found when the genus Amicotermes was revised, and many more undescribed species are still likely to occur in Africa (Sands 1999). This highlights that even soldierless généra that are presently monospecific may reveal plentiflil new species at the continental scale. In addition, American taxa of this group hâve received little attention.

According to the scarce data available on Apicotermitinae, we cannot obtain a clear view of the group diversity. However, some dues suggest that a complété révision of the group would yield many new species, both in Africa and in South America. In the latter continent, faunistic surveys of termites indeed indicated that about 30% of ail termite species

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Fig. 3. Complété enteric valve armature of: A, Anoplotermes parvus in situ; B, Anoplotermes manni in situ; C, Anoplotermes nigripunctatus in situ; D, Grigiotermes nr. metoecus opened with 5 of the 6 cushions on display; E, Aparatermes cingulatus opened and spread; F, new genus sp A, full enteric valve with a single cushion.

belong to the Anoplotermes-group (Eggleton et al. 1996, Davies 2002, Davies et al. 2003b), Roisin et al. 2006, Bourguignon et al. 2009a). Paradoxically, on 505 species described from the Neotropics, only 41 are from the Anoplotermes-group, which thus represent about 8% of the known species in the région (Constantino 1998). The discrepancy between the high diversity of the group within local assemblages and its low overall taxonomie diversity might be explained by a lower beta-diversity compared to other termite taxa. However, there is no data supporting this hypothesis, and we believe that this discrepancy is rather due to a global lack of interest from taxonomists, who still hesitate at describing or redescribing species of the group.

Overall, the Apicotermitinae regroup 42 généra and 208 species distributed across African, Neotropical and Oriental régions. In the latter, Bornéo is the eastem limit of the group with only a few species of Euhamitermes occurring there (Tho 1992, Eggleton et al.

1999). Continental areas possess a more diversified Apicotermitinae community, e.g.

Euhamitermes, Eurytermes, Indotermes and Speculitermes occur in India where they are represented by 29 species (Roonwal and Chhotani 1989, Chhotani 1997). However, the Oriental région lacks soldierless Apicotermitinae and the local fauna is by far less diversified than in South America and Africa. These two régions clearly host the richest communities, but are difficult to compare because taxonomie efforts hâve been very inéquitable. About 30

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The Anoplotermes group in French Guiana - Introduction 9

généra hâve been described in Africa (Sands 1998) whereas only five are known from South America (Fontes 1992, Constantino 1998). The African generic diversification is thus better established and most species can reliably be assigned to a genus even if staying unnamed at the species level (e.g. Eggleton et al. 1996, 2002). By contrast, South American species are usually referred to Anoplotermes (e.g. Davies et al. 2003b), including in a broad sense ail soldierless termites, which might be split into a dozen of généra if a complété révision were carried out (Eggleton 1999). The most striking différence between the two continents is probably the lack of Apicotermitinae with a soldier caste in South America, where only the Anoplotermes-gwup occurs.

Phylogeny

Recent phylogenetic studies placed the Apicotermitinae as sister group of Termitinae + Nasutitermitinae + Syntermitinae (Donovan et al. 2000, Inward et al. 2007) (Fig. 4). The Apicotermitinae form a monophyletic taxon, with South American members forming a monophyletic group nested within African représentatives (Inward et al. 2007). African species which hâve retained the soldier caste form a paraphyletic assemblage basal to soldierless termites (Inward et al. 2007), suggesting that Apicotermitinae first diversified in Africa, then spread out into South America. According to this hypothesis, the American soldierless termites would be monophyletic and originate from the African species pool, through the dispersai of a single soldierless ancestral species (Fig. 4).

Fig. 4. Phylogeny of the Apicotermitinae (redrawn after Inward et al. 2007).

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Diet diversification reaches its utmost in Termitidae which can feed on lichens, fungi, wood, leaves or soil organic matter (Abe 1979). As ail Apicotermitinae but the neotropical leaf litter feeder Ruptitermes (Mathews 1977) are soil-wood interface or soil feeders, the most recent common ancestor of the group was likely a soil feeder too. Eggleton and Tayasu (2001) suggested that the major shift toward soil diet occurred after the Macrotermitinae branched off, at the base of ail remaining Termitidae. It is indeed likely that when termitids appeared, lower termites were the dominant wood-feeders and the rapid diversification of the clade could only be achieved through the conquest of free niches. Additionally, given the omniprésence of soil-feeders at the base of the clade Termitinae + Nasutitermitinae (Inward et al. 2007), it is likely that they share a common soil-feeding ancestor with Apicotermitinae, while some of their members hâve subsequently reverted to a wood-feeding habit.

The soldier caste is undoubtedly ancestral to ail termites (Roisin 2000), but in the Apicotermitinae, this caste is often represented by very low numbers of individuals. For instance, among the 10 Indian species of Speculitermes, only S. sinhalensis is known to hâve soldiers (Chhotani 1997). The soldier caste is evcn completely missing in several gênera. How many times the soldier caste was actually lost is still incompletely resolved. According to Inward et al. (2007), the soldierless Apicotermitinae might be monophyletic but their cladogram features the Oriental soldierright clade Speculitermes-Euhamitermes as nested within the African soldierless généra. In any case, the loss of the soldier caste occurred independently in the Termitinae généra Invasitermes, Protohamitermes and Orientotermes (Ahmad 1976, Miller 1984), but these lineages never reached the diversity and ecological importance attained by soldierless Apicotermitinae.

Reproduction and development

Termite colonies are generally initiated by a primary pair of imagos (Nutting 1969), but in a few species such as Macrotermes michaelseni and Nasutitermes corniger, several females can cooperate to found a colony together, a situation called pleometrosis (Atkinson and Adams 1997, Hacker et al. 2005). Such colonies may ultimately be headed by more than one queen at maturity. Altematively, polygyny may resuit from the replacement of the primary queen by multiple sexuals. As in other termites, colony foundation of Apicotermitinae generally relies upon the association of one male and one female and foundation by multiple queens has never been reported. However, after careful dissection of 70 nests of Anoplotermes banksi, we

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The Anoplotermes group in French Guiana - Introduction 11

found two nests headed by two highly physogastric imaginai queens (Fig. 5A). Since queen replacement seems impossible in this species (see below), we believe that pleometrosis occasionally occurs in some species of Apicotermitinae.

Fig. 5. A. Nest of Anoplotermes banksi opened, showing two queens extracted from the royal cell (upper left); B. Ruptitermes sp. from eentral Panama foraging on the leaf litter.

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Worker Larvae 2 t

\

Alate Nymph 4 t

Nymph 3 t

Nymph 2 t

Nymph 1 t

Larvae 1

t

Egg

Fig. 6. Caste developmental patways of Anoplotermes pacificus after Kaiser (1956).

In the Apicotermitinae, as in ail Termitidae, an apterous developmental line splits up irreversibly at the first moult from the imaginai pathway to produce a distinctive worker caste, entirely devoted to colony tasks (Fig. 6) (Kaiser 1956, Roisin 2000). In the Termitidae, the worker caste often présents a sexual dimorphism or consists in a succession of several instars (Roisin 2000). Data on sex ratio and development of workers in Apicotermitinae are non existent.

Preliminary observations revealed the extreme diffïculty of observing sexual vestiges in Anoplotermes nigripunctatus and Aparatermes cingulatus and the absence of workers engaged into fürther moulting. Although Myles (1999) reported that workers of the Oriental soldierright genus Speculitermes can develop into ergatoid (=

worker-derived) néoténies, workers of the Anoplotermes-growp seem completely stérile, as not a single ergatoid has ever been found (Myles 1999). In the same way, nymphoids (=nymph-derived neotenic reproductives) hâve never been found in any Apicotermitinae but many species can develop adultoids (Sands 1972), which likely represent the only chance to replace dead primary reproductives in Anoplotermes-group species. To test the potential of workers in Anoplotermes, we orphaned 10 nests of A. banksi, which contained both nymphs and workers, at the beginning of February: five of these nests were retrieved after two and half months, they were still alive but contained neither eggs nor developing néoténies; the remaining five nests were ail dead one year later.

One surprising trait in the developmental scheme of Anoplotermes pacificus is the nymphal line reported to comprise only 4 nymphal instars (Kaiser 1956). This contrasts with other termitids which all reach the alate stage after 5 nymphal instars (Noirot 1985, Roisin 2000). Unfortunately, Kaiser's (1956) study is the only one to address nymphal development in Apicotermitinae. This question deserves further investigation.

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The Anoplotermes group in French Guiana - Introduction 13

Colony defence in a soldierless context Nest architecture

The nest structure of African soldierright Apicotermitinae has been intensively studied in the mid 20th century (Desneux 1953, Grassé 1984); unfortunately, these studies were purely descriptive and did not give any insight into the function of nest architecture and its impact on termite defence or communication. Nevertheless, they provided basic information on nest shape diversity and building location for a few généra. In Apicotermes, ail species build complex underground nests which can be single, twins (or connected nests), polycalic, or associated to nests of other species (Coaton 1962, Desneux 1953, 1958, Grassé and Noirot 1948, Grassé 1981, 1984). In several Neotropical soldierless termites such as Ruptitermes arboreus and Anoplotermes banksi, the nests are built aboveground, at low heights on trees (Emerson 1938). These nests are probably initiated in the soil, then the colony moves onto a small tree. Our observations on Anoplotermes banksi support this hypothesis, as small nests are generally only filled with workers and lack other castes. Epigeous nests may also occur, e.g. in Anoplotermes parvus (pers. obs.). Beside these cases where nests are observed, most Apicotermitinae species are found in underground galleries or chambers and nest structures are seldom encountered. For example, on the 34 morphospecies we collected in French Guiana, only 4 build conspicuous aboveground nests which serve, at least in A. banksi, as a shelter to survive flooding events in swamps or flooded forests (Martius 1994).

Nest architecture plays an important rôle in colony defence, e.g. in Cubitermes spp.

(Termitinae) a low connectivity of peripheral chambers permits a rapid isolation of the part under attack, whereas a high connectivity of central chambers favours a rapid traffic inside the nest (Pema et al. 2008). We believe this pattern is likely the rule in most nest-building termites, including Anoplotermes-group species and other Apicotermitinae. Flowever, these considérations are highly spéculative and likely to stay unconfirmed as nests of many soldierless termites are hidden belowground, and some species may hâve no centralized nests but only a diffuse network of chambers and galleries.

Worker défensive behaviour

The major rôle of the soldier caste is to defend the colony against predators and competitors.

In its absence in the Anoplotermes-group, this rôle is filled by workers which hâve developed

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many défensive strategies including anatomical, physiologieal, and behavioural specializations.

A particular défensive behaviour, common in members of the Anoplotermes-group, is défécation on opponents. This strategy is not a singularity of the group and also occurs in other termite généra such as Armitermes and Labiotermes, as well as in several other soil- feeders (Mill 1984). However, it seems particularly widespread in the Anoplotermes-group, and represents for many species the main way to repel intruders (Sands 1972, Mathews 1977).

In Skatitermes, the worker abdomen is highly manoeuvrable and can be whipped forward, on either side or dorsally over the head to apply a drop of sticky faecal fluid on enemies (Coaton 1971). In neotropical soldierless termites such as Grigiotermes (Mathews 1977), workers perform the same behaviour although we never observed such an extreme abdominal flexibility.

One common défensive behaviour performed by workers of termites from ail familles is biting in a similar way to soldiers (Thome 1982). The worker mandibles inflict comparatively little damage to opponents, but in the Anoplotermes-group, the movement is often coupled with alternative weaponry. In two undescribed species close to Anoplotermes distans and A. subterraneus, we observed that workers émit a drop of hyaline liquid from the mouth, either after a worker bites an enemy or following contact with it. The substance is secreted by enlarged labial glands and stiffens after air exposure, highlighting its défensive fimction. A similar défensive behaviour also occurs in Ruptitermes (Mathews 1977), probably in Grigiotermes which has well developed labial glands (Costa-Leonardo and Cruz-Landim 1991), as well as in many other neotropical soldierless termites.

Another mechanism sometimes coupled with biting is body wall rupture through abdominal dehiscence. For example, when a worker of the African soldierless genus Alyscotermes achieves to grip an ant appendage, the termite’s abdomen breaks along the posterior part of the metanotum, leaving two droplets of sticky clear fluid emerging from the wound (Sands 1982). Such a mechanism implying worker self-sacrifice is commonplace in the Anoplotermes-group. In the African soldierless termites, Sands (1972, 1982) reported that 11 généra out of the 16 he described présent at least occasional abdominal dehiscence; but it does not especially follow mandibular attack by the worker. The mechanisms causing the body rupture involve abdominal muscles, which contract until rupture of the abdominal wall occurs along a line of weakness, allowing the intestine to spread outside the abdomen (Costa- Leonardo 2004). Additional substances expelled together with the digestive tract are often

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The Anoplotermes group in French Guiana - Introduction 15

produced by labial glands (Sands 1982), but specialised glands entirely devoted to défensive purpose can also be involved. In Ruptitermes, a pair of dehiscence glands situated anteriorly on the side of the abdomen produce a sticky substance which appears harmful to ants (Costa- Leonardo 2004). Unfortunately, contrary to défensive compounds produced by soldiers whose composition is well-known (Prestwich 1984, Sobotnik et al. 2010a), worker défensive substances bave never been studied yet. Finally, the frontal gland is présent in workers of neotropical Apicotermitinae, where it appears as a small white spot located at the top of the head. However its function is unknown and the gland may or may not be involved in defence (Sobotnik et al. 2010b).

Adaptation toward a defence of the colony by the worker caste is the rule in Apicotermitinae, but is not the exclusiveness of this group. For example, we observed that workers of Crepititermes verruculosus (Termitidae) systematically poured out their digestive tract when grabbed with a forceps. Dehiscence is also known in soldiers of Serritermitidae, Globitermes, Apilitermes and Dentispicotermes where it involves the frontal gland (Bordereau et al. 1997, Deligne and De Coninck 2006, Sobotnik et al. 2010c).

Ecology Feeding habits

The diet of the Termitidae generally lies along a wood-soil décomposition gradient, from Sound wood to heavily mineralized organic matter remaining in the soil (Bignell and Eggleton 2000). In the Apicotermitinae, feeding habits are restricted to a narrow part of this range and mainly consists in decomposed organic matter, except for Ruptitermes (Fig. 5B) which feeds on leaf litter (Matthews 1977, personal observation). Apicotermitinae workers are generally encountered either in the soil or in rotten wood where they feed on organic matter already degraded by wood-feeding termites or other decomposers (Bourguignon et al. 2009b).

Abandoned termite nests are also frequently colonised by soldierless Apicotermitinae, benefiting from the higher proportion of organic matter in the termite nest compared to the surrounding soil (Amelung et al. 2002). Some généra such as Grigiotermes and Aganotermes are specialised nest colonisers and are mainly found in dead or living termite nests, respectively (Sands 1972, Ferrar 1982a, personal observation).

Although the soil-feeding habits of Apicotermitinae are well established (Donovan et al. 2001, Bourguignon et al. 2009b), their précisé food requirements remain largely unknown.

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The diet of soil-feeders appears to consist exclusively of non-cellular organic matter mixed with minerai material, but nothing is known about the nutritive component utilised by soil- feeders (Brune and Kühl 1996). The soil they ingest is a mixture composed of minerai aggregates and organic particles; termites cannot get resources from the mixture as a whole but only from the palatable organic matter. We do not know to what extent they select soil particles before ingestion, or whether they rely on digestive processes through specialised gut segments such as the enteric valve (Donovan et al. 2002). In French Guiana, resource partitioning along the humification gradient occurs in Neotropical soldierless termites (Bourguignon et al. 2009b). Stable isotopes revealed that Anoplotermes-group species living within the top 10cm of soil feed on different substrates, either through selecting particles or by specifically feeding on a definite layer. This différentiation of the feeding niches could account for the high species richness and diversity of the group.

Abundance and impact

Many termite species spend their entire lifespan tuimelling, building, feeding and foraging on and in the soil. Their impact is twofold: by feeding on the soil they dégradé the organic matter and participate to dead plant material recycling; through building nests and galleries, termites hâve an influence on the soil profile (Holt and Lepage 2000). Termite activities therefore hâve a profound effect the physical and Chemical properties of soil, especially in tropical rainforests and savannas where they can reach a huge abundance (Fittkau and Klinge 1973, Eggleton et al. 1996, Wood 1996, Fall et al. 2001). With the exception of a few taxa such as Aganotermes in South African savaimas (Ferrar 1982b), Apicotermitinae are generally not abundant in this ecosystem (Wood 1996). However, they are extremely abundant in rainforest where they often constitute about half the diversity of soil-feeding termites, or even more (Table 2). Martius (1996) estimated to about 200g the total weight of Anoplotermes banksi on one hectare of Amazonian rainforest, highlighting the abundance of Apicotermitinae species.

Given this huge abundance, we can assert without doubts that the group has a major impact on soil nutrient recycling processes in Afrotropical and Neotropical forests.

Acknowledgment

We thank J. Sobotnik for his advice during the writing of the manuscript. J. Cillis provided technical assistance with SEM operation. Financial support was provided by

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The Anoplotermes group in French Guiana - Introduction 17

the Fund for Scientific Research (F.R.S.-FNRS), Belgium, through a predoctoral fellowship to T. Bourguignon.

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The Anoplotermes group in French Guiana - Introduction 21

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Africa

Cameroon primary forest to plantation 114 72-74 42 Eggleton et al. 1995, 1996 Cameroon primary to secondary forest 133 79 49 Eggleton et al. 2002a

Congo primary forest 80 75 41 Eggleton et al. 2002b

Uganda semi-deciduous forest 25 20 4 Okwakol 2000

South America

Formosa, Argentina semi-deciduous forest 24 46 21 Roisin and Leponce 2004

Paraiba, Brazil savanna 20 35 30 Sena et al. 2003

Pemambuco, Brazil primary forest to plantation 21 57 29 Bandeira and Vasconcellos 2002 Pemambuco, Brazil primary forest to plantation 26 54 19 Bandeira et al. 2003

Amazonas, Brazil primary forest to plantation 67 69 33 Ackerman et al. 2009

French Guiana primary and fragmented forest 100 73 34 Davies 2002, Davies et al. 2003

Panama Primary forest (ground) 34 66 45 Roisin et al. 2006

Asia

Sabah, East Malaysia primary to secondary forest 93 50 3 Eggleton et al. 1999

Sabah, East Malaysia mountain forest 37 35 0 Jones 2000

Table 2. Observed species richness (OSR) and relative proportion of soil-feeders (SF) and Apicotermitinae (Ap) in varions locations and ecosystems, sampled following standardised transect protocols.

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TheAnoplotermesgroupinFrenchGuiana-Introduction

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The Anoplotermes group in French Guiana - Objectives 23

Aims of the work

This thesis brings together the results of our work on the Anoplotermes group members. At the early stage, we were interested in termite ecology as a whole, but we quickly became especially attracted by the singularities of the Anoplotermes group. Beside the fact that very few studies addressed it before us, we were astonished by its abundance and diversity in the soil and deeply rotten pièces of wood. Additionally, the absence of soldiers is a remarkable trait which, besides posing spécial taxonomie difficulties, correlates with ecological and behavioural peculiarities since as ail tasks, including defence, are carried out by workers. AU these characteristics drove us to focus our attention on this particularly challenging group and to improve our knowledge of these termites as much as four years of work could allow it, with the ultimate purpose of understanding how and why this group diversified so broadly and became one of the dominant soil-dwelling taxa in the Neotropics. More specifically, we mainly focused our work on the three following topics;

1. Biodiversity (Article 1): We worked with the entire Anoplotermes group community in three French Guiana locations: the Nouragues station, the Petit Saut dam and the Kaw Mountain. This study allowed us to compare the diversity at the régional scale (100 km) and to provide information on the group diversity in French Guiana.

2. Ecology (Articles 2, 3, 4): With the help of stable isotope analyses, we studied the feeding ecology of the Anoplotermes group species. We characterised the feeding niches occupied by species of this group with respect to other termite families and termitine subfamilies (Article 2), and we investigated the feeding niches of individual Anoplotermes-gTOUTp species (Article 3). We also studied the distribution of colonies at the local scale in one focal species, A. banksi, as well as the dynamics of their population over a 3-year period (Article 4).

3. Systematics (Article 5): A complété révision of the Anoplotermes group is outside the scope of this thesis. However, systematic knowledge is a prerequisite for other disciplines. Here, we provide a solid basis for future taxonomie work on this group by redescribing Anoplotermes pacificus, type-species of the genus, and of a few common and widespread related species.

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