Insights into the termite assemblage of a neotropical rainforest from [PDF]

Insect Conservation and Diversity (2009) doi: 10.1111/j.1752-4598.2009.00055.x

Insights into the termite assemblage of a neotropical rainforest from the spatio-temporal distribution of flying alates THOMAS BOURGUIGNON, 1 MAURICE LEPO NCE 2 and YVES ROISIN 1 1

Behavioural and Evolutionary Ecology, Universite´ Libre de Bruxelles, Brussels, Belgium and 2Section of Biological Evaluation, Royal Belgian Institute of Natural Sciences, Brussels, Belgium

Abstract. 1. During the last decade, many studies have focused on the diversity of termite species and their ecological function, but these have been mostly based on transect protocols not designed to sample canopy-dwelling and subterranean species. Additionally, all these studies relied upon collections of foraging parties composed of workers and soldiers in the soil or in pieces of wood. 2. We hypothesised that alate-based protocols could disclose spatial and temporal patterns of termite flights and provide a more balanced picture of assemblages for ecological and biodiversity surveys. 3. Our study took place in the framework of the IBISCA-Panama project, which used numerous trapping methods to give a multifaceted overview of a complex tropical rainforest arthropod community. Two methods, flight interception traps and light traps, were efficient at collecting termite alates. All collected specimens were assigned to morphospecies which were later identified to the genus or species level, when possible. 4. Our results highlighted that: (i) alate trapping represents a powerful complement to ground-based standardised sampling protocols by allowing the documentation of the whole termite assemblage. (ii) Canopy dwellers fly preferentially in the upper strata, whereas no vertical stratification was found for ground dwellers, suggesting that height of flight is dictated by a pressure for long distance dispersal as well as the need to find a suitable site for colony-founding. (iii) Alates from closely related species do not stagger their flight period to avoid hybridisation but rather synchronise their flights according to environmental factors. Key words. Canopy, IBISCA project, Isoptera, nuptial flights, sampling protocol, spatial distribution.

Correspondence: Yves Roisin, Behavioural and Evolutionary Ecology, CP 160 ⁄ 12, Universite´ Libre de Bruxelles, Avenue F.D. Roosevelt 50, B-1050 Brussels, Belgium. E-mail: yroisin@ulb. ac.be

and experiences larger humidity and temperature variations (Szarzynski & Anhuf, 2001; Madigosky, 2004). These physical conditions, combined with other variables such as resource availability, tree architecture or predator pressure (review in Basset et al., 2003b), produce a spectrum of living conditions for the flora and fauna. After pioneering studies strictly focused on canopy arthropods, more recent approaches tend to encompass all forest strata, from the soil to the upper canopy (review in Basset, 2001). Vertical stratification has now been demonstrated for a wide range of arthropod taxa such as spiders (Sørensen, 2003), springtails (Rodgers & Kitching, 1998), butterflies (DeVries et al., 1997; Schulze et al., 2001; Fermon et al., 2003, 2005), flies (Tanabe, 2002) and beetles (Charles & Basset, 2005).

 2009 The Authors Journal compilation  2009 The Royal Entomological Society

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Introduction Understanding the spatial patterns of species distribution is crucial to describe ecological communities and to design hypotheses on the origin and maintenance of species diversity (Kneitel & Chase, 2004). Among these spatial patterns, vertical stratification is an important element of tropical rainforest heterogeneity and diversity (Basset, 2001; Basset et al., 2003b). The canopy receives much more sunlight than the understorey

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Thomas Bourguignon, Maurice Leponce and Yves Roisin

Termites represent an important proportion of animal biomass in tropical rainforests (Fittkau & Klinge, 1973; Eggleton et al., 1996) where they are major decomposers of organic matter (Holt & Lepage, 2000). During the last decade, numerous studies have described variations in termite assemblages among tropical forests according to the level of disturbance (Eggleton et al., 1995, 2002; Davies et al., 1999; Okwakol, 2000; Jones et al., 2003), altitude (Gathorne-Hardy et al., 2001; Donovan et al., 2002), degree of habitat fragmentation (Davies, 2002) or geographical location (review in Davies et al., 2003a). At a finer scale, environmental factors such as the presence of palms (Davies et al., 2003b) or terrestrial bromeliads (Roisin & Leponce, 2004) were shown to influence termite assemblage composition. However, these studies were based on standard collecting protocols (Jones & Eggleton, 2000; Roisin & Leponce, 2004) designed for sampling soil, litter, fallen wood, epigeous mounds, or other habitats situated at or near ground level. The upper strata have been almost systematically neglected, because their access is difficult and standard sampling methods for canopy arthropods, such as fogging, are not very efficient at collecting termites (Eggleton & Bignell, 1995; Basset et al., 2003a; Hurtado Guerrero et al., 2003). Nevertheless, vertical stratification of the termite assemblage was recently demonstrated in a Panamanian forest, through manual collecting: whereas soil-feeding species were logically confined to the ground strata, some wood feeders showed a definite preference for either the ground or the upper strata (Roisin et al., 2006). Presumably all termites, like most ants, produce winged morphs (alates) which fly away from their nests of origin to mate and found new colonies. In tropical rainforests, the temporal distribution of nuptial flights of ants and termites varies from broadly scattered over long periods to strongly seasonal, with high pulses at specific times of the year (Rebello & Martius, 1994; Martius et al., 1996; Kaspari et al., 2001a,b). Usually, basal termite families such as Kalotermitidae and Termopsidae repeatedly release small numbers of alates over the course of a long flight season, whereas Rhinotermitidae and Termitidae stage fewer, more massive flights, which are generally seasonal and triggered by meteorological events (Nutting, 1969; Jones et al., 1988; Martius, 2003; but see Rebello & Martius, 1994). Apart from some anecdotal observations, very little is known of the height and duration of termite flights (Nutting, 1969). Recent genetic data suggest that alates usually fly far enough to promote outbreeding and minimise detectable population structure (Brandl et al., 2005; Husseneder et al., 2006; Thompson et al., 2007). Previous studies have revealed that some taxa (e.g. Kalotermitidae) are under-represented in samples collected from nests, soil and dead wood under conventional ground-based protocols, by comparison with the occurrence of alates in light traps (Rebello & Martius, 1994). This suggests that the source assemblage from which alates are issued is broader than the fauna accessible by standard collecting protocols. A probable hypothesis is that canopy specialists should be among species specifically revealed by alate trap samples. On the other hand, some ground strata species are likely to escape detection by alate traps, because they are very eclectic as to the conditions suitable for

nuptial flights. In this study, we investigated the vertical and temporal distribution of termite flights in a neotropical rainforest. We put forward the following hypotheses: 1 By comparison with standard sampling protocols, which are unlikely to reveal canopy or deep-soil dwellers, alate trapping should provide a more comprehensive sampling of the assemblage, and may allow better estimates of its total richness and taxonomic composition. A drawback is that the overall efficiency of the trapping methods remains to be demonstrated (Jones et al., 2005). Light trapping is efficient when operated continuously over long periods, but is restricted to night-flying species. Flight interception traps have seldom been used for termites. An experiment by Rebello and Martius (1994) provided only few specimens. Here we test the efficiency of alate trapping and its potential in biodiversity surveys. 2 For all species, flying high should facilitate longdistance dispersion. One can therefore expect most species, even soil-dwelling ones, to reach the canopy during flights. By contrast, there seems to be no reason for canopy specialists to fly down to near-ground levels. Traps were set at various heights to test these predictions. 3 Closely related species may use behavioural mechanisms to avoid hybridisation and its associated cost (Stiles, 1975). In this context, it was often hypothesised that species could stagger their reproduction. However in ants, closely related species tend to fly during the same periods, without staggering (Kaspari et al., 2001a,b; Torres et al., 2001; Dunn et al., 2007). Here, we hypothesised that, as in ants, the swarming period of termites is principally influenced by environmental factors, while other mechanisms preclude hybridisation between closely related species.

Materials and methods Study site This study lies within the framework of the IBISCA-Panama project, an international initiative for investigating the arthropod biodiversity of a neotropical rainforest, targeting 57 focal taxa in all forest strata through 14 sampling protocols (Basset et al., 2007). Field work took place in the San Lorenzo protected area (917¢N, 7958¢W) (Colo´n Province, Republic of Panama). This location averages 3100 mm of annual rainfall and an annual air temperature of 26C (1998–2002 data). The climate is wet all year-round, with a comparative drier season between January and mid-April. The forest is evergreen with less than 3% loss in canopy cover by the end of the dry season (Condit et al., 2000, 2004). It has been mostly free of severe disturbance for the past 150 years. Detailed information on the study site and sampling plots is available from Basset et al. (2007).

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

Spatio-temporal distribution of termite alates Sampling methods Among the 14 collecting methods used (details in Basset et al., 2007), only two, aerial composite flight-interception traps (hereafter FI) and light traps (L), were efficient at collecting termite alates. FI traps consisted of two perpendicular perspex sheets, 60 cm tall and 23 cm wide, protected by a rain cap and supported on a funnel, itself fitted into a collecting jar (see Basset et al., 2007; p. 58 and Fig. 7 ⁄ 11). They were set up at six heights above ground (0, 1.3, 7, 14, 21, 28 m), and the catch was picked up every 10 days. They were run in October 2003 and from March to October 2004 on five plots (B1, C1, C2, C3, I1 as in Basset et al., 2007), yielding 1659 samples. L traps consisted of a vertically mounted ‘black light’ fluorescent tube with three transparent plastic vanes equidistant to it, fitting into a funnel opening in a bucket. A lid protected the trap from rainfall (see Basset et al., 2007; p. 57 and Fig. 7 ⁄ 10). These traps were placed at two heights (1.3 and 35 m). They were usually set at about 17:00 to 18:30 hours (sunset) and retrieved the following morning around 6:00 to 7:00 hours (sunrise). In 2003, eight plots (B1, B2, C1, C2, C3, I1, R1, R3 as in Basset et al., 2007) were surveyed during September and October, yielding 48 trap samples. In 2004, plots C1 and C2 were surveyed again in February, March, May and October, yielding 42 samples. Collected insects, including termite alates, were preserved in 80% ethanol. After sorting, the various taxa were dispatched to specialists for identification. Isoptera samples will be kept in the Royal Belgian Institute of Natural Sciences, Brussels, Belgium.

Data analysis As termite systematics is primarily based on soldier morphology, the identification of alates at the species level is sometimes problematic. However, the Panamanian termite fauna has been relatively well studied and alates are known for most species. As help to identification at the genus and species level, we used the extensive taxonomic work of Mathews (1977), the keys of Nickle and Collins (1992), revisions of particular taxa (Krishna, 1961, 1968), and numerous reference samples from our collection. Species were assigned to canopy or understorey-dwellers based on their known feeding habits and nest location (Roisin et al., 2006). Soldierless Apicotermitinae (Anoplotermes group) and humivorous Nasutitermitinae (Subulitermes group), whose many alate morphospecies could not be unequivocally assigned to described species, were all considered ground-level dwellers because they are soil feeders and were never encountered foraging in the canopy (Roisin et al., 2006). The ‘unassigned’ category comprises two species, Microcerotermes arboreus and Nasutitermes banksi (= Nasutitermes sp.1 in Roisin et al., 2006), found as foragers equally in both strata, as well as four additional wood feeding species, Neotermes sp.A, Dolichorhinotermes sp.A, Nasutitermes ephratae and Nasutitermes corniger, not previously recorded. One occurrence was defined as the presence of one species in one trap sample, no matter how many individuals of this species

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occurred in the trap. Occurrences are more informative than actual numbers of individuals, because the latter may strongly depend on random effects: in particular, traps are likely to capture huge numbers of alates from the same colony if placed close to a nest. v2 tests on alate occurrences were performed on all samples collected both in 2003 and 2004, to compare the efficiency of FI and L traps, to test for differences in termite alate distribution between strata (from ground to canopy), according to foraging habits (ground level vs. canopy) or taxonomic position (Kalotermitidae, Rhinotermitidae or Termitidae). In order to compare the efficiency of alate trapping (FI traps) and standard collecting protocols (data from Roisin et al., 2006) at sampling termite species diversity, we compared rarefaction curves computed with all samples collected in 2003 and 2004 using ESTIMATES v.7.00 (Colwell, 2005). Graphs were scaled using number of occurrences as sampling effort (Gotelli & Colwell, 2001) and 95% confidence intervals were calculated using the Mao-Tau method (Colwell et al., 2004). To compare phenology, families and the most abundantly represented species were plotted for the year 2004. As most species have similar phenology and differ only in flight intensity, plots were only compared visually.

Results In total, FI and L traps together yielded 1630 individuals in 551 occurrences representing 36 species. FI collected 34 species for 478 occurrences, whereas L collected 16 species for 73 occurrences (Table 1). FI results indicated that termite alates were not equally distributed among forest strata: alate occurrences were more abundant in the canopy (v2 = 42.54, d.f. = 5, P < 10)6). Alates of canopy-dwelling species were significantly more frequent in the higher than in the lower strata (v2 = 37.94, d.f. = 5, P < 10)6). In contrast, alates of ground-dwelling species showed no significant preference (v2 = 11.07, d.f. = 5, P = 0.05) (Fig. 1a). L traps gave congruent results for both canopy dwellers (v2 = 5.4, d.f. = 1, P = 0.02) and ground dwellers (v2 = 0.31, d.f. = 1, P = 0.58) (Fig. 1b). Termitidae, Kalotermitidae and Rhinotermitidae showed clear differences in their occurrence between strata (based on FI traps), the first two families being significantly more abundant in the canopy (Termitidae, v2 = 19.05, d.f. = 5, P = 0.002; Kalotermitidae, v2 = 50.06, d.f. = 5, P < 10)6). No significant difference of distribution was found for the Rhinotermitidae (v2 = 7.48, d.f. = 5, P = 0.19) (Fig. 1c,d). Termite families also displayed differences in their phenology: Kalotermitidae flew over a long period, whereas Rhinotermitidae mostly flew in April and May (more than 90% of the captures) and Termitidae in May (78% of the captures) (Fig. 2). Only two species, Anoplotermes sp.AA and Embiratermes chagresi, had their swarming periods delayed by 2 and 4 months, respectively, compared with other Termitidae (Fig. 3). On average, an FI trap operating for 10 days yielded 0.89 individual and 0.29 occurrence, whereas an L trap

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

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Thomas Bourguignon, Maurice Leponce and Yves Roisin

Table 1. List of termite species occurrences collected by FI traps at six heights and L traps at two heights. FI traps – height (m) Family

0

Species

Canopy species K Calcaritermes brevicollis K Glyptotermes angustus K Neotermes holmgreni K Rugitermes panamae T Nasutitermes nigriceps T Termes hispaniolae Understorey species R Coptotermes niger R Heterotermes convexinotatus T Amitermes beaumonti T Anoplotermes cf. manni T Anoplotermes parvus T Anoplotermes sp.A T Anoplotermes sp.C T Anoplotermes sp.M T Anoplotermes sp.AA T Anoplotermes sp.AB T Anoplotermes sp.AC T Anoplotermes sp.AD T Anoplotermes sp.AE T Coatitermes clevelandi T Cornitermes sp.A T Cornitermes walkeri T Cylindrotermes macrognathus T Embiratermes chagresi T Nasutitermes guayanae T Orthognathotermes wheeleri T Subulitermes-group sp.A T Subulitermes-group sp.B T Subulitermes-group sp.C T Velocitermes barrocoloradensis Unassigned species K Neotermes sp.A R Dolichorhinotermes sp.A T Microcerotermes arboreus T Nasutitermes banksi T Nasutitermes corniger T Nasutitermes ephratae Total occurrences Total species

1.3

7

L traps – height (m) 14

21

28

All FI

1.3

35

All L

1 1 – – – 2

1 – – – 3 –

6 – – – 2 5

– – – – 6 1

8 2 1 1 11 5

2 1 – 1 13 4

18 4 1 2 35 17

– – 1 – – 2

– – 8 – – 3

– – 9 – – 5

3 6 4 10 2 2 2 1 – – 1 3 1 – 1 – – 3 – – – 1 – –

8 6 5 9 1 3 – – – – – 3 1 – – 1 1 13 1 2 – 1 1 2

5 1 – 19 1 1 3 – 2 – – 3 2 – – 1 – 9 – 1 1 – – –

6 7 1 22 5 1 1 3 1 – 2 3 1 – – – – 3 – – 1 – 1 –

14 4 1 28 5 5 5 3 – 1 1 1 – – 1 – 2 – 1 – – 1 –

6 8 1 15 1 1 7 7 5 – – 3 4 – 1 – – 3 – 2 – – – –

42 32 12 103 15 8 18 16 11 – 4 16 10 – 2 3 1 33 1 6 2 2 3 2

4 – – – – – 1 – – – – – – 5 – – – – 3 3 – – – –

5 – – 1 1 – – – – 3 – – 1 2 – – 1 – – – – – – –

9 – – 1 1 – 1 – – 3 – – 1 7 – – 1 – 3 3 – – – –

– – 2 2 – –

– – 3 – – 1

3 – 4 – 1 1

4 – 5 – – –

14 – 4 – 2 1

5 1 4 – 2 –

26 1 22 2 5 3

19 1 – 2 – 1

5 – – – – 1

24 1 – 2 – 2

48 19

66 20

71 20

74 19

122 25

97 23

478 34

42 11

31 11

73 16

K, Kalotermitidae; R, Rhinotermitidae; T, Termitidae.

operating for a single night yielded 1.74 individual and 0.81 occurrence. For FI traps, these values reached 4.18 individuals and 1.23 occurrence per trap during the flight peak in May. L traps collected significantly higher numbers of alate occurrences than FI traps (v2 = 40.557, d.f. = 1, P < 10)6). Compared with standard, ground-based collecting (Roisin et al., 2006), FI traps provided similar values of species richness for a given number of species occurrences, whereas the diversity of L-collected samples was lower (Fig. 4). Two species, Anoplotermes sp.AB and Coatitermes clevelandi were collected only with L traps, all the

others were collected only by FI traps or by both FI and L traps (Table 1).

Discussion Hypothesis 1: Alate trapping as an unbiased alternative to standard ground-based sampling protocols? Standardised sampling protocols aim at producing representative samples of the taxonomic and functional composition of a

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

Spatio-temporal distribution of termite alates FI traps

(a) 80

(b) 25

Ground Not assigned Canopy

Occurrences

15 40 10 20

0

5

0.0

1.3

7.0 14.0 Trap height (m)

21.0

0

28.0

FI traps

(c) 80

(d) 25

Termitidae Rhinotermitidae Kalotermitidae

Occurrences

1.3 35.0 Trap height (m) L traps

20

60

15 40 10 20 5

0

16

0.0

1.3

7.0 14.0 Trap height (m)

Kalotermitidae

50

21.0

Rhinotermitidae

Number of occurrences

1.3 35.0 Trap height (m)

Termitidae 300 250

40

12

0

28.0

14

Fig. 2. Pooled flying activity of Kalotermitidae, Rhinotermitidae and Termitidae from March to October 2004, as revealed by number of occurrences in FI traps.

L traps

20

60

Fig. 1. Distribution of termite occurrences in flight interception (FI) and light (L) traps, according to trap height above ground level. (a,b) Species classified according to foraging strata; (c,d) species classified by family.

5

200

10

30

8

150 20

6

100

4 10

50

2 0

0 M A M J J A S O N Month

local termite assemblage (Bignell & Eggleton, 2000; Jones & Eggleton, 2000; Roisin & Leponce, 2004). However, they present the major pitfall not to sample the soil below 5–10 cm and the forest strata above a standing man’s height, which makes deep

MAM J J A S ON Month

0

M A M J J A S O N Month

subterranean and canopy-dwelling species likely to be overlooked. Based on individual occurrences, the species rarefaction curve obtained from FI traps was not significantly different from that

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

Thomas Bourguignon, Maurice Leponce and Yves Roisin Number of occurrences

6

6

8 Calcaritermes brevicollis

6

0 J

A

S O N

M A M

J

J

A

S O N

100 Heterotermes convexinotatus

20

60

10

40

5

20 M A M

J

J

A

S O N

10 Anoplotermes sp. A

8 6 4 2 M A M

J

J

A

S O N

10 8 Anoplotermes sp. AA 6 4 2 M A M

J

J

A

Anoplotermes cf. manni

80

15

Number of occurrences

Number of occurrences

J

25

Number of occurrences

5

1 M A M

S O N

10

0 16 14 12 10 8 6 4 2 0 18 16 14 12 10 8 6 4 2 0

M A M

J

J

A

S O N

Anoplotermes sp. C

M A M

J

J

A

S O N

8

15

4

10

2

5

0

0

M A M 14 12 10 8 6 4 2 0 18 16 14 12 10 8 6 4 2 0

J

J

A

S O N

Anoplotermes parvus

M A M

J

J

A

S O N

Anoplotermes sp. M

M A M

J

J

A

S O N

Anoplotermes sp. AE

10 8 6 4 2

M A M

J

J

A

S O N

0

M A M

J

J

A

S O N

A

S O N

30 Microcerotermes arboreus

20

6

0

12 Anoplotermes sp. AD

25 Amitermes beaumonti

Embiratermes chagresi

25 20 15

M A M

J Number of occurrences

Number of occurences

10

2

0

0

15

3

2

0

Coptotermes niger

20

4

4

0

25 Neotermes sp. A

5

J 16 14 12 10 8 6 4 2 0

A

S O N

10 5 M A M

J

Termes hispaniolae

M A M

J

J A Month

S O N

J 18 16 14 12 10 8 6 4 2 0

A

S O N

0

M A M

J

J

Nasutitermes nigriceps

M A M

J

J A Month

S O N

Fig. 3. Flying activity of the most common termite species at the San Lorenzo forest from March to October 2004, as revealed by number of occurrences in FI traps.

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

Spatio-temporal distribution of termite alates

provided only 7–11 species from a deciduous forest in Belize (Davies et al., 2003a). Although the number of encounters reported by Davies et al. (2003b) is not equivalent to our definition of occurrence and does not allow the construction of comparable rarefaction curves, our data from the San Lorenzo forest (this work and Roisin et al., 2006: 11–22 species per 200m2 transect and 20–30 species for 100–200 occurrences) clearly reveal a lower termite diversity than in French Guiana.

Number of species

40

30

20

10

0

7

FI traps Ground transects L traps 0

100

200

300

400

Hypothesis 2: Vertical distribution of alates

500

Occurrences

Fig. 4. Rarefaction curves for termite assemblages established from FI traps (data from this study), light (L) traps (data from this study) and ground-based transects (data from Roisin et al., 2006). Graphs show most likely estimates (black) and 95% confidence intervals (grey), calculated by the Mao-Tau method (Colwell et al., 2004).

obtained from standard, ground-based transect protocols (data from Roisin et al., 2006). Both methods therefore appear equally efficient at accumulating termite species. However, the transects collected only Calcaritermes brevicollis as representative of the Kalotermitidae and failed to collect most canopy specialists, whereas FI traps collected five species of Kalotermitidae. This latter method provided samples encompassing all forest strata and was more representative of the local taxonomic diversity. FI traps set in the canopy (21 m above ground) were the most efficient in terms of number of species captured and total alate occurrences. FI trapping has however three drawbacks: (i) the difficulty in identifying species on the sole basis of alates, although one can argue that biodiversity studies do not necessarily require species identifications (Basset et al., 2004); additionally, emerging methods such as DNA barcoding can facilitate matching alates with corresponding neuters (workers and soldiers) (Webb et al., 2006; Ahrens et al., 2007); (ii) the seasonality of flights and their dependence on meteorological conditions; and (iii) the relatively low efficiency of individual traps. These last two factors make long periods of continuous sampling necessary to obtain a representative sample of the whole assemblage. Among the numerous trapping methods used in the IBISCAPanama project, only FI and L traps were really efficient at collecting termite alates. For an equal number of traps, L traps captured by far more specimens than FI traps within a few days of collection. Previous studies emphasised the potential of L traps as well (Rebello & Martius, 1994). Light traps can collect rare species not easily traceable by other methods, and appear as a cost-effective method to collect alate termites. There are few comparative data available on termite richness in neotropical forests. Thirteen ground transects of 200 m2 in French Guiana rainforests yielded 38–51 termite species in 185– 306 encounters (Davies et al., 2003b), whereas two transects

In spite of their reputation of being weak flyers (Nutting, 1969; Mill, 1983), alates of 20 of 24 ground-dwelling species reached at least a height of 21 m, and 17 of them reached at least 28 m. These data suggest that flying high is an important feature of dispersal for tropical rainforest termites and support previous genetic works which hypothesised a long dispersal distance in alates of several termite species (Brandl et al., 2005; Husseneder et al., 2006; Thompson et al., 2007). By flying high, alates may take advantage of air currents, which greatly increase in strength and turbulence in or above the upper canopy (Kruijt et al., 2000). The vertical distribution of alates was however not homogeneous. Both FI and L traps highlighted the same pattern: canopy dwellers fly preferentially in the canopy, whereas understorey dwellers fly equally throughout all strata. Overall, these results are consistent with our hypothesis 2: to maximise their dispersion, alates should fly high into the canopy, but they should also spend time flying in the strata in which appropriate landing sites for colony founding are situated. Whereas both factors concur for canopy dwellers to keep them flying in the upper strata, they are antagonists for ground dwellers, which explains the lack of vertical pattern in the latter.

Hypothesis 3: Reproductive phenology staggering as way to avoid hybridisation? Although no FI traps were run from November to February, all species previously recorded more than twice by ground transects (Roisin et al., 2006) and whose alates were unequivocally identifiable were trapped. This suggests that few, if any, species have escaped detection for flying specifically during that period. With the exception of Anoplotermes sp.AA and Embiratermes chagresi, most species of Termitidae and Rhinotermitidae flew at the same period, around May, which is the time rains resume after the January–April drier spell (Basset et al., 2007). A similar concentration of flights at resumption of rain was reported by other authors (Nutting, 1979; Mill, 1983; Medeiros et al., 1999), although flights may occur all year-round in regions without pronounced dry season, such as central Amazonia (Rebello & Martius, 1994; Martius et al., 1996). A lack of reproductive phenology staggering among species was also found in tropical and temperate ant communities (Kaspari et al., 2001a,b; Dunn et al., 2007). Other mechanisms, such as flying at different times of the day, under different meteorological conditions or towards different landmarks, and specific behavioural mechanisms of species

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

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Thomas Bourguignon, Maurice Leponce and Yves Roisin

recognition (Cle´ment, 1982, 1986; Peppuy et al., 2004), are therefore likely to prevent the formation of hybrid pairs. In contrast to the Termitidae and Rhinotermitidae, the Kalotermitidae displayed nearly continuous flight activity over several consecutive months (Fig. 3). In Amazonia as well, kalotermitid alates could be caught throughout the year (Rebello & Martius, 1994; Martius et al., 1996). Differences in social organisation and colony dynamics between Kalotermitidae on the one hand and Rhinotermitidae and Termitidae on the other can explain the phenological differences observed between them. The Kalotermitidae usually form small colonies confined into single pieces of wood, where most immatures retain the potential to develop into reproductives (Nutting, 1969; Roisin, 2000). They can proceed to the alate under colony-specific conditions, in particular when the resources of the housing wood dwindle (Korb & Katrantzis, 2004; Korb & Lenz, 2004). The Rhinotermitidae and Termitidae, in contrast, form large colonies capable of exploiting external sources of food, which makes them less dependent on the intrinsic colony condition. Consequently, nuptial flights depend mostly on external factors (Nutting, 1969; Roisin, 2000).

Acknowledgements The IBISCA-Panama project was set up by Pro-Natura International, Oce´an Vert, l’Universite´ Blaise Pascal, la Universidad de Panama´ and the Smithsonian Tropical Research Institute (STRI), with core funding from Solvin-Solvay SA, STRI, the United Nations Environment Programme, the Smithsonian Institution (Walcott fund), the European Science Foundation and the Global Canopy Programme. Special thanks are due to Yves Basset, Bruno Corbara and He´ctor Barrios for their contribution to the project organisation. The Belgian National Fund for Scientific Research (F.R.S.–FNRS) provided additional support, through grants to YR and a predoctoral fellowship to TB. Experiments complied with the current laws of the Republic of Panama.

References Ahrens, D., Monaghan, M.T. & Vogler, A.P. (2007) DNA-based taxonomy for associating adults and larvae in multi-species assemblages of chafers (Coleoptera : Scarabaeidae). Molecular Phylogenetics and Evolution, 44, 436–449. Basset, Y. (2001) Invertebrates in the canopy of tropical rain forests. How much do we really know? Plant Ecology, 153, 87–107. Basset, Y., Corbara, B., Barrios, H., Cue´noud, P., Leponce, M., Aberlenc, H.-P., Bail, J., Bito, D., Bridle, J.R., Castan˜o-Meneses, G., Cizek, L., Cornejo, A., Curletti, G., Delabie, J.H.C., Dejean, A., Didham, R.K., Dufreˆne, M., Fagan, L.L., Floren, A., Frame, D.M., Halle´, F., Hardy, O.J., Herna´ndez, A., Kitching, R.L., Lewinsohn, T.M., Lewis, O.T., Manumbor, M., Medianero, E., Missa, O., Mitchell, A.W., Mogia, M., Novotny, V., Ødegaard, F., Oliveira, E.G., Orivel, J., Ozanne, C.M.P., Pascal, O., Pinzo´n, S., Rapp, M., Ribeiro, S.P., Roisin, Y., Roslin, T., Roubik, D.W., Samaniego, M., Schmidl, J., Sørensen, L.L., Tishechkin, A., Van Osselaer, C. & Winchester,

N.N. (2007) IBISCA-Panama, a large-scale study of arthropod beta-diversity and vertical stratification in a lowland rainforest: rationale, description of study sites and field methodology. Bulletin de l’Institut Royal des Sciences Naturelles de Belgique (Entomologie), 77, 39–69. Basset, Y., Hammond, P.M., Barrios, H., Holloway, J.D. & Miller, S.E. (2003b) Vertical stratification of arthropod assemblages. Arthropods of Tropical Forests – Spatio-temporal Dynamics and Resource Use in the Canopy (ed. by Y. Basset, V. Novotny, S.E. Miller and R.L. Kitching). pp. 17–27, Cambridge University Press, Cambridge, U.K. Basset, Y., Novotny, V., Miller, S.E. & Kitching, R.L. (2003a) Methodological advances and limitations in canopy entomology. Arthropods of Tropical Forests – Spatio-temporal Dynamics and Resource Use in the Canopy (ed. by Y. Basset, V. Novotny, S.E. Miller and R.L. Kitching). pp. 7–16, Cambridge University Press, Cambridge, U.K. Basset, Y., Novotny, V., Miller, S.E., Weiblen, G.D., Missa, O. & Stewart, A.J.A. (2004) Conservation and biological monitoring of tropical forests: the role of parataxonomists. Journal of Applied Ecology, 41, 163–174. Bignell, D.E. & Eggleton, P. (2000) Termites in ecosystems. Termites: Evolution, Sociality, Symbioses, Ecology (ed. by T. Abe, D.E. Bignell and M. Higashi). pp. 363–387, Kluwer Academic Publishers, Dordrecht, The Netherlands. Brandl, R., Hacker, M., Epplen, J.T. & Kaib, M. (2005) High gene flow between populations of Macrotermes michaelseni (Isoptera, Termitidae). Insectes Sociaux, 52, 344–349. Charles, E. & Basset, Y. (2005) Vertical stratification of leaf-beetle assemblages (Coleoptera: Chrysomelidae) in two forest types in Panama. Journal of Tropical Ecology, 21, 329–336. Cle´ment, J.-L. (1982) Phe´romones d’attraction sexuelle des termites europe´ens du genre Reticulitermes. Me´canismes comportementaux et isolements spe´cifiques. Biology of Behaviour, 7, 55–68. Cle´ment, J.-L. (1986) Open and closed societies in Reticulitermes termites (Isoptera, Rhinotermitidae): geographic and seasonal variations. Sociobiology, 11, 311–323. Colwell, R.K. (2005) EstimateS: statistical estimation of species richness and shared species from samples. [7.0]. User’s guide and application published at: http://www.purl.oclc.org/ estimates. Colwell, R.K., Mao, C.X. & Chang, J. (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology, 85, 2717–2727. Condit, R., Aguı´ lar, S., Herna´ndez, A., Pe´rez, R., Lao, S., Angehr, G., Hubbell, S.P. & Foster, R.B. (2004) Tropical forest dynamics across a rainfall gradient and the impact of an El Nin˜o dry season. Journal of Tropical Ecology, 20, 51–72. Condit, R., Watts, K., Bohlman, S.A., Pe´rez, R., Foster, R.B. & Hubbell, S.P. (2000) Quantifying the deciduousness of tropical forest canopies under varying climates. Journal of Vegetation Science, 11, 649–658. Davies, R.G. (2002) Feeding group responses of a Neotropical termite assemblage to rain forest fragmentation. Oecologia, 133, 233–242. Davies, R.G., Eggleton, P., Dibog, L., Lawton, J.H., Bignell, D.E., Brauman, A., Hartmann, C., Nunes, L., Holt, J. & Rouland, C. (1999) Successional response of a tropical forest termite assemblage to experimental habitat perturbation. Journal of Applied Ecology, 36, 946–962. Davies, R.G., Eggleton, P., Jones, D.T., Gathorne-Hardy, F.J. & Herna´ndez, L.M. (2003a) Evolution of termite functional diver-

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

Spatio-temporal distribution of termite alates sity: analysis and synthesis of local ecological and regional influences on local species richness. Journal of Biogeography, 30, 847–877. Davies, R.G., Herna´ndez, L.M., Eggleton, P., Didham, R.K., Fagan, L.L. & Winchester, N.N. (2003b) Environmental and spatial influences upon species composition of a termite assemblage across neotropical forest islands. Journal of Tropical Ecology, 19, 509–524. DeVries, P.J., Murray, D. & Lande, R. (1997) Species diversity in vertical, horizontal, and temporal dimensions of a fruit-feeding butterfly community in Ecuadorian rainforest. Biological Journal of the Linnean Society, 62, 343–364. Donovan, S.E., Eggleton, P. & Martin, A. (2002) Species composition of termites of the Nyika plateau forests, northern Malawi, over an altitudinal gradient. African Journal of Ecology, 40, 379–385. Dunn, R.R., Parker, C.R., Geraghty, M. & Sanders, N.J. (2007) Reproductive phenologies in a diverse temperate ant fauna. Ecological Entomology, 32, 135–142. Eggleton, P. & Bignell, D.E. (1995) Monitoring the response of tropical insects to changes in the environment: troubles with termites. Insects in a Changing Environment (ed. by R. Harrington and N.E. Stork). pp. 473–497, Academic Press, London, U.K. Eggleton, P., Bignell, D.E., Hauser, S., Dibog, L., Norgrove, L. & Madong, B. (2002) Termite diversity across an anthropogenic disturbance gradient in the humid forest zone of West Africa. Agriculture, Ecosystems & Environment, 90, 189–202. Eggleton, P., Bignell, D.E., Sands, W.A., Mawdsley, N.A., Lawton, J.H., Wood, T.G. & Bignell, N.C. (1996) The diversity, abundance and biomass of termites under differing levels of disturbance in the Mbalmayo Forest Reserve, southern Cameroon. Philosophical Transactions of the Royal Society of London, Series B-Biological Sciences, 351, 51–68. Eggleton, P., Bignell, D.E., Sands, W.A., Waite, B., Wood, T.G. & Lawton, J.H. (1995) The species richness of termites (Isoptera) under differing levels of forest disturbance in the Mbalmayo Forest Reserve, southern Cameroon. Journal of Tropical Ecology, 11, 85–98. Fermon, H., Waltert, M. & Mu¨hlenberg, M. (2003) Movement and vertical stratification of fruit-feeding butterflies in a managed West African rainforest. Journal of Insect Conservation, 7, 7–19. Fermon, H., Waltert, M., Vane-Wright, R.I. & Mu¨hlenberg, M. (2005) Forest use and vertical stratification in fruit-feeding butterflies of Sulawesi, Indonesia: impacts for conservation. Biodiversity and Conservation, 14, 333–350. Fittkau, E.J. & Klinge, H. (1973) On biomass and trophic structure of the Central Amazonian rain forest ecosystem. Biotropica, 5, 2–14. Gathorne-Hardy, F.J., Syaukani & Eggleton, P. (2001) The effects of altitude and rainfall on the composition of the termites (Isoptera) of the Leuser Ecosystem (Sumatra, Indonesia). Journal of Tropical Ecology, 17, 379–393. Gotelli, N.J. & Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4, 379–391. Holt, J.A. & Lepage, M. (2000) Termites and soil properties. Termites: Evolution, Sociality, Symbioses, Ecology (ed. by T. Abe, D.E. Bignell and M. Higashi). pp. 389–407, Kluwer Academic Publishers, Dordrecht, The Netherlands.

9

Hurtado Guerrero, J.C., da Fonseca, C.R.V., Hammond, P.M. & Stork, N.E. (2003) Seasonal variation of canopy arthropods in Central Amazon. Arthropods of Tropical Forests – Spatio-temporal Dynamics and Resource Use in the Canopy (ed. by Y. Basset, V. Novotny, S.E. Miller and R.L. Kitching). pp. 170–175, Cambridge University Press, Cambridge, U.K. Husseneder, C., Simms, D.M. & Ring, D.R. (2006) Genetic diversity and genotypic differentiation between the sexes in swarm aggregations decrease inbreeding in the Formosan subterranean termite. Insectes Sociaux, 53, 212–219. Jones, D.T. & Eggleton, P. (2000) Sampling termite assemblages in tropical forests: testing a rapid biodiversity assessment protocol. Journal of Applied Ecology, 37, 191–203. Jones, D.T., Susilo, F.X., Bignell, D.E., Hardiwinoto, S., Gillison, A.N. & Eggleton, P. (2003) Termite assemblage collapse along a land-use intensification gradient in lowland central Sumatra, Indonesia. Journal of Applied Ecology, 40, 380–391. Jones, D.T., Verkerk, R.H.J. & Eggleton, P. (2005) Methods for sampling termites. Insect Sampling in Forest Ecosystems (ed. by S. Leather). pp. 221–253, Blackwell Publishing, Oxford, U.K. Jones, S.C., La Fage, J.P. & Howard, R.W. (1988) Isopteran sex ratios: phylogenetic trends. Sociobiology, 14, 89–156. Kaspari, M., Pickering, J., Longino, J.T. & Windsor, D. (2001a) The phenology of a Neotropical ant assemblage: evidence for continuous and overlapping reproduction. Behavioral Ecology and Sociobiology, 50, 382–390. Kaspari, M., Pickering, J. & Windsor, D. (2001b) The reproductive flight phenology of a neotropical ant assemblage. Ecological Entomology, 26, 245–257. Kneitel, J.M. & Chase, J.M. (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecology Letters, 7, 69–80. Korb, J. & Katrantzis, S. (2004) Influence of environmental conditions on the expression of the sexual dispersal phenotype in a lower termite: implications for the evolution of workers in termites. Evolution & Development, 6, 342–352. Korb, J. & Lenz, M. (2004) Reproductive decision-making in the termite, Cryptotermes secundus (Kalotermitidae), under variable food conditions. Behavioral Ecology, 15, 390–395. Krishna, K. (1961) Generic revision and phylogenetic study of the family Kalotermitidae (Isoptera). Bulletin of the American Museum of Natural History, 122, 303–408. Krishna, K. (1968) Phylogeny and generic reclassification of the Capritermes complex (Isoptera, Termitidae, Termitinae). Bulletin of the American Museum of Natural History, 138, 261–324. Kruijt, B., Mahli, Y., Lloyd, J., Nobre, A.D., Miranda, A.C., Pereira, M.G.P., Culf, A. & Grace, J. (2000) Turbulence statistics above and within two Amazon rain forest canopies. Boundary-Layer Meteorology, 94, 297–331. Madigosky, S.R. (2004) Tropical microclimatic considerations. Forest Canopies, 2nd edn (ed. by M.D. Lowman and H.B. Rinker). pp. 24–48, Elsevier Academic Press, Burlington, Massachusetts, U.S.A. Martius, C. (2003) Rainfall and air humidity: non-linear relationships with termite swarming in Amazonia. Amazoniana, 17, 387–397. Martius, C., Bandeira, A.G. & Medeiros, L.G.S. (1996) Variation in termite alate swarming in rain forests of Central Amazonia. Ecotropica, 2, 1–11.

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity

10

Thomas Bourguignon, Maurice Leponce and Yves Roisin

Mathews, A.G.A. (1977) Studies on Termites From the Mato Grosso State, Brazil. Academia Brasileira de Cieˆncias, Rio de Janeiro, Brazil. Medeiros, L.C.D., Bandeira, A.G. & Martius, C. (1999) Termite swarming in the northeastern Atlantic rain forest of Brazil. Studies on Neotropical Fauna and Environment, 34, 76–87. Mill, A.E. (1983) Observations on Brazilian termite alate swarms and some structures used in the dispersal of reproductives (Isoptera: Termitidae). Journal of Natural History, 17, 309–320. Nickle, D.A. & Collins, M.S. (1992) The termites of Panama (Isoptera). Insects of Panama and Mesoamerica: Selected Studies (ed. by D. Quintero and A. Aiello). pp. 208–241, Oxford University Press, Oxford, U.K. Nutting, W.L. (1969) Flight and colony foundation. Biology of Termites (ed. by K. Krishna and F.M. Weesner). pp. 233–282, Academic Press, New York, U.S.A. Nutting, W.L. (1979) Termite flight periods: strategies for predator avoidance? Sociobiology, 4, 141–151. Okwakol, M.J.N. (2000) Changes in termite (Isoptera) communities due to the clearance and cultivation of tropical forest in Uganda. African Journal of Ecology, 38, 1–7. Peppuy, A., Robert, A. & Bordereau, C. (2004) Species-specific sex pheromones secreted from new sexual glands in two sympatric fungus-growing termites from northern Vietnam, Macrotermes annandalei and M. barneyi. Insectes Sociaux, 51, 91–98. Rebello, A.M.C. & Martius, C. (1994) Dispersal flights of termites in Amazonian forests (Isoptera). Sociobiology, 24, 127– 146. Rodgers, D.J. & Kitching, R.L. (1998) Vertical stratification of rainforest collembolan (Collembola: Insecta) assemblages: description of ecological patterns and hypotheses concerning their generation. Ecography, 21, 392–400. Roisin, Y. (2000) Diversity and evolution of caste patterns. Termites: Evolution, Sociality, Symbioses, Ecology (ed. by T. Abe, D.E. Bignell and M. Higashi). pp. 95–119, Kluwer Academic Publishers, Dordrecht, The Netherlands. Roisin, Y., Dejean, A., Corbara, B., Orivel, J., Samaniego, M. & Leponce, M. (2006) Vertical stratification of the termite assemblage in a neotropical rainforest. Oecologia, 149, 301–311.

Roisin, Y. & Leponce, M. (2004) Characterizing termite assemblages in fragmented forests: A test case in the Argentinian Chaco. Austral Ecology, 29, 637–646. Schulze, C.H., Linsenmair, K.E. & Fiedler, K. (2001) Understorey versus canopy: patterns of vertical stratification and diversity among Lepidoptera in a Bornean rain forest. Plant Ecology, 153, 133–152. Sørensen, L.L. (2003) Stratification of the spider fauna in a Tanzanian rainforest. Arthropods of Tropical Forests – Spatiotemporal Dynamics and Resource Use in the Canopy (ed. by Y. Basset, V. Novotny, S.E. Miller and R.L. Kitching). pp. 92– 101, Cambridge University Press, Cambridge, U.K. Stiles, F.G. (1975) Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia species. Ecology, 56, 285–301. Szarzynski, J. & Anhuf, D. (2001) Micrometeorological conditions and canopy energy exchanges of a neotropical rain forest (Surumoni-Crane Project, Venezuela). Plant Ecology, 153, 231– 239. Tanabe, S. (2002) Between-forest variation in vertical stratification of drosophilid populations. Ecological Entomology, 27, 720–731. Thompson, G.J., Lenz, M., Crozier, R.H. & Crespi, B.J. (2007) Molecular-genetic analyses of dispersal and breeding behaviour in the Australian termite Coptotermes lacteus: evidence for non-random mating in a swarm-dispersal mating system. Australian Journal of Zoology, 55, 219–227. Torres, J.A., Snelling, R.R. & Canals, M. (2001) Seasonal and nocturnal periodicities in ant nuptial flights in the tropics (Hymenoptera : Formicidae). Sociobiology, 37, 601–626. Webb, K.E., Barnes, D.K.A., Clark, M.S. & Bowden, D.A. (2006) DNA barcoding: a molecular tool to identify Antarctic marine larvae. Deep-Sea Research Part II – Topical Studies in Oceanography, 53, 1053–1060. Accepted 14 March 2009 Editor: Yves Basset Associate editor: Jerome Orivel

 2009 The Authors Journal compilation  2009 The Royal Entomological Society, Insect Conservation and Diversity