1.2 Western Lowland Amazon and the Las Piedras Research Centre

1. Introduction

1.1 The Importance of Termitaria

Species belonging to most terrestrial animal taxa have at some point been observed ‘nesting’ in arboreal termitaria. Considering the frequent use of these natural homes there is relatively few empirical data to highlight either the importance of termitaria as a nesting resource or the evolution of the termitaria nesting behaviour. The main objectives of this project are to establish which type of forest is most suited to high abundances of arboreal nesting termites and highlight the use of termitaria by cavity nesting birds. With the increased fragmentation of the Peruvian Amazon cavity nesting birds are under greater pressure than ever. Nesting resources other than trees may have or may become a vital component for species survival. This study presents evidence highlighting gaps in the knowledge and comments upon the reliance of other taxa on termitaria and New World termites.

1 1.2 Western Lowland Amazon and the Las Piedras Research Centre

Upper Western Amazonian forests may have the most diverse floral and faunal assemblages in the world. The Cocha Cashu site in Manu National Park,

Peru, has the world's largest published inventory of bird species (Terborgh et al.

1984). Tambopata Reserve, Peru has even more bird species (Donahue et al.

1988 and Brightsmith 2006) and the highest known butterfly diversity in the world

(Lamas 1985.) The world's largest local inventory of mammals is from Balta, Peru.

The most diverse reptilian fauna recorded is from the forest surrounding Iquitos,

Peru (Dixon and Soini, 1975, 1976) and the most diverse amphibian fauna is from

Santa Cecilia, Ecuador (Duellman 1978). Gentry (1988) provides evidence that the patterns of tree species richness parallel those of birds, butterflies, reptiles and amphibians, and mammals, with the world's greatest local concentrations of species in the relatively moist and fertile forests near the base of the Andes.

Lowland forests in Peru are however under increasing pressure from land use change. In Tambopata (area close and similar to the study site), in sparsely inhabited (<1 person/km2), remote areas, humans are altering the composition and abundance of wildlife communities (Naughton-Treves et al. 2003) which may have long term effects on the natural functioning of this forest type (Redford and

Robinson 1992). As part of an increasing number of data to come from the area this report is ecological evidence of the ‘pristine’ nature of the Upper Rio Las

Piedras. There is an urgent call for restrictions and management of resource use

2 and the implementation of conservation management plans which are sympathetic to human needs and to ecological protection as mineral prospecting was rife while this data was collected.

1.3 Termites- evolution and sociality

The earliest evidence of eusocial insects in the fossil record is of reproductive termites castes found at a lower cretaceous lithographic limestone site in Spain (Bartz 1979, Delclos and Martinell 1995). Since the cretaceous period, Isoptera (species >2700, Genera >280; Zoological Record 1996) have dispersed to every continent and thrive in many climates (Williams 1992 and

Cabrera et al. 2001). Species richness and total biomass of species increases from high latitudes to the equator (Collins 1989, Pearce and Waite 1994 and Miura et al. 2000); most species being observed in wet topical forests (Groombridge,

1992 Eggleton et al.1994). However the decrease in diversity with increasing distance from the equator (observed in most animal and plant taxa) is asymmetric in the case of termites, southern latitudes having higher generic diversity compared with similar northern latitudes (Davies et al. 2003). It has been suggested that this is evidence of Gondwanan bias in dispersal (Eggleton et al. 1994). The richest area is tropical West Africa (highest richness, southern Cameroon, 65 genera), specifically in the forested regions. Primary rain forest in South America has a

3 lower diversity (highest richness, west Amazonian forests, 54 genera) and south- east Asian forests lower still (highest richness, north Borneo, 46 genera) (Williams

1992 and Eggleton et al. 1994). Non-forested regions in all tropical regions are relatively dispauperate (Johnson et al. 1980 and Collins, 1989). Almost all species feed on dead plant material, some on soil and a number of termite species will eat carrion. Studies show that humidity levels, the degree of canopy closure, high biomass of and nutrient levels in food sources limit termite diversity and abundance, rather than the complexity or tree richness of the forest (Lee and

Wood, 1971, Bignell and Eggleton 2000, Eggleton and Tavasu 2001 and Roisin et al. 2006).

Being one of the most abundant invertebrates in tropical wet forests ranks termites as one of the most ecologically important decomposers (Bignell and

Eggleton 2000, Donavon et al. 2001). Estimates are that total decomposition by termite assemblage in any given area of tropical wet forest may be as high as 30% of leaf litter fall (Maldague 1964, Masumoto 1974), although a figure of 15% has been suggested in different studies (Lee and Wood 1971 and Masumoto 1976).

Collins (1981) estimated that the total wood fall decomposition of termites in a

Guinea wet tropical forest was 60%. The above studies highlight that, due to the decidedly abundant nature of termite colonies, many predictions of levels of decomposition may be conservative. The study of termites is based on calculations from averages in either whole nests or core samples from nests or

4 mounds. Under sampling of some species of termite, especially soil feeding and arboreal forms, has led researchers to feel that the impact of termites on a wet tropical ecosystems has been underestimated (Eggleton and Bignell 1995).

All extant termites are considered to be eusocial with a hierarchical system in the dissemination of tasks in order to increase the survivability of the colony

(Thorne 1997). Termites colonies are housed in relatively enormous structures

(sometimes 1000 times the constructor’s size) (Korb 2003). The behaviour of building arboreal termitaria and subterranean mounds evolved from a need to protect and incubate offspring and live within the walls of a food source (i.e. the nest itself) (Emerson 1934). The arboreal nests are assumed to be an extension of the protection from would be invaders; new world ant eaters (Yael et al 1977 and

1981) and armadillos (Redford 1985) being the most prolific nest raiders. The evolutionary translocation into arboreal distribution may also highlight the evolution of termites from wood eaters to mulch/soil eaters. This report highlights the niche space and abundance of arboreal termites by examining the spatial arrangement of termite colonies in 14.8 hectares of forest.

5 1.4 Arboreal Termite Nests

The arboreal location of a nest is settled by the founding pair. Evidence suggests that there is an initial phase where the young colony relocates from a subterranean base upwards using a variety of genus specific techniques (Noirot and Darlinton 2000). The substrate used to build arboreal nests is a compound of humus (wood and leaf litter), saliva and faecal matter (preponderant in arboreal nests) called ‘carton’ (Noirot and Darlinton 2000). The carton can be produced to varying levels of thickness but more importantly strength as the nests are vulnerable to predatory activity. All termitaria contain a very hard queen’s chamber located near the centre (Noirot 1970).

Constantino (1999) and Gonclaves (2005) suggests that of the New World assemblage there are 8 different genus (Ruptitermes, Armitermes,

Constrictitermes, Labiotermes, Nasutitermes, Rotunditermes, and

Microcerotermes) of termite that build arboreal termitaria. Building arboreal nests allows termites to populate unfavourable locations (Williams 1934) as the above ground nature of the nests means that phenomena such as surface flooding or heavy rain (Emerson 1934) would have a negligible impact on the colonies survival. The nature of the substrate in an arboreal nest seems to prevent the affliction of fungal growths which appear when arboreal termites are removed from a nest (Emerson 1934). Arboreal termite species build foraging ‘wood-carton’ tunnels over long distances. The nests and tunnels are common sights in tropical

6 forests worldwide (Abe 1978, 1979; Leponce et al. 1997; Dejean et al. 2003;

Goncalves et al. 2005).

1.5 Cavity Nesting Birds

The structural complexity of tropical lowland forests provides birds with many nesting niches not available to temperate species (Koepcke 1972 and

Terborgh et al. 1984). Considerable numbers of bird species depend on cavities in trees; however the evolved use of arboreal termite mounds may also play a significant role in nest site availability. Tree cavity availability is greatly reduced in managed forests, forest fragments or where land has been turned over for agriculture (Rico and Pliego 2004). In the absence of human interference, natural forest can provide usable cavities in large trees and snags. Availability increases with decay of trees and forest patches, which increase the amount of dead wood and facilitates cavity formation (Newton 1998 and Joy 2000). Continuous undisturbed areas of forest are a requisite to provide the necessary resources for many cavity nesting birds (Warren et al. 2005). The rate of deforestation and fragmentation in many tropical forests leaves cavity nesting birds vulnerable (Rico and Pliego 2004 and Kesler and Haig 2005).

Cavity nesting birds are split into two categories: primary (excavators e.g. woodpeckers) and secondary (non-excavators e.g. tree swallows) (Lohmus

7 and Remm 2004). There are some species which are considered weak excavators

(e.g. nuthatches) and fall into both categories. The primary species create cavities that are used by a large number of avian and mammalian species; creating a community with clear hierarchies and guild structures that potentially have strong interdependencies between different species (Martin and Eadie 1999). There is often intense competition for nest sites between all forms of cavity nesting birds

(Martin 1993 and Brightsmith 2005a). This competition exerts immense influence on avian evolution traits and behaviour such as nest site selection, clutch size and nestling period (Van Balen et al. 1982, Yanes and Suarez 1997 and Brightsmith

2005b). Erberard (2002) argues that in secondary species this may have influenced community and structure. Unlike other birds they are without the choice to become colonialists as they have to fly to where the nests are and this may have implications on the status of some species as forest decline. Intense competition for nest sites has evolved because when with egg during nestling periods, the whole nest is vulnerable to predation (Brightsmith 2005b). Suitable nests will provide insulation, protection and an appropriate place for the chicks to fledge.

Secondary species of birds have larger clutch sizes (Beissinger and Waltman

1991, Martin 1993, Beissinger 1996) and smaller nestling periods. This is due to the high competition for nests (Eberhard 2002).

8 1.6 Termitaria use by Cavity Nesting Birds

Species of birds from all tropical regions in the world nest in termitaria

(Hindwood 1959 and Brightsmith 2000). For some genus of bird the use of termitaria is great (Brightsmith 2000): at least 11% of all parrots (Juniper and Parr

1998), 32% of new world trogons (Willis and Eisenmann 1979, Hilty and Brown

1986) and 45% of kingfishers (Fry and Fry 1992, Brightsmith 2000 and Kesler and

Haig 2005). Only two previously published studies attempt to draw conclusions from empirical data of the importance of termitaria as nests sites (Brightsmith

2004b and Kesler and Haig 2005). There are studies which provide evidence of the use of termitaria by different species of bird. However these are often based on observations of behaviour rather than empirical frequency data.

The full extent of arboreal termitaria as an important primary and secondary nesting resource has yet to be assessed. However detailed descriptions of nest sites, dimensions of nests and use for the Great Jacamar (Jacamerops aurea),

Purus Jacamars (Galbalcyrhynchus purusianus), Bluish-fronted Jacamar (Galbula

Cyanescens) Black-tailed trogon (Trogon melanurus), (Trogon curucui) Tui

(Brotogeris sanctithomae) and Cobalt-winged (Brotogeris cyanoptera) parakeets have been published by Brightsmith (2000 and 2004). The Micronesian kingfisher

(Todiramphus cinnamominus reichenbachii) has been the focus of a study by

Kesler and Haig (2005): Which assesses nest competition, nest choice and interaction between communal groups and breeding pairs. The nesting behaviour

9 of the citroline trogon (Trogon citreolus) published by Hoelflich and Rivera (2005) highlighted the importance of primary excavators as important ecosystem engineers. The green rumped parrolet (Forpus passerinus passerinus) has also been documented nesting in termitaria cavities (Belcher and Smooker 1936,

Friedman and Smith 1950,) although neither study alludes to whether they are primary excavators. Other published work outlining the use of termitaria by cavity nesting birds can be found in Hindwood (1959), a review of termitaria cavity nesting by birds. Fry and Fry (1995) discussed the behaviour of kingfishers, bee eaters and rollers with some relation to nesting in arboreal termitaria. Forshaw

(1989) and Juniper and Parr (1998) describe their observations in field guides of the Avifauna of Venezuela and Parrots of the World (respectively), both detail nesting behaviour of New World birds.

Other studies discuss the inherited use of cavities in termitaria by secondary cavity nesters, small mammals, snakes, lizards and arthropods, however empirical data is limited. In Jullien & Cariveau (2001) the secondary use of excavated but empty termitaria nests by the wing-banded wren (Microcerculus bambla) in French

Guiana was recorded for the first time. Eberard (2002) reported that availability of already excavated nest sites may be a limiting factor for secondary excavators in reproductive success. Hoelflich and Rivera (2005) observed the citroline trogon

(Trogon citreolus) and the orange-fronted parakeet (Aratinga canicularis) building nests in termitaria in Mexico. They also examined 24 cavities of the disused termitaria, 19 of which were occupied; two by the grayish-mouse opossum

10 (Marmosa canescens), one by the Magdalena rat (Xenomys nelsoni), and two by unknown small mammals that escaped before being identified. Additionally, 14 cavities were occupied by arthropods, including tailless whip scorpions

(Amblypygi), katydids (Tettigoniidae), bees (Apidae), and wasps (Sphecidae).

Termites seem to build nest without considering nesting birds as there seems to be little benefit for the termite. Brightsmith (2000 and 2004) and Kesler and Haig (2005) explain that the termite workers build a thick wall around the excavated chamber thus creating a termite nest and an avian nest chamber (Noirot

1970) and separating the two inhabitants from interaction.

A degree of commonness in arboreal nesting may exist that has yet to be fully explored. Further studies could help contribute to understand a possible important resource interaction in light of forest and habitat fragmentation and conservation management.

1.7 Habitat Influence

Undoubtedly habitat variation will effect the termite population and the presence or absence of cavity nesting birds. Understanding temporal habitat dynamics in which termites are most abundant can in part explain abundance of termites and size of termitaria. Habitat will also influence avian presence in termitaria due to the specific dimensions all cavity nesting birds require (>9 litres in volume and > 5 metres in height) (Brightsmith 2000, 2004). Threat from predation

11 is a factor that will influence the height at which termitaria are built. This defensive strategy is limited primarily by resource availability and therefore habitat.

Termites that build arboreal nests require considerable nutrient rich biomass to sustain and build increasingly larger colonies (Noirot and Darlington 2000).

Therefore the size and presence of termite nests is limited by availability of nutrient rich food resources (Traniello et al. 2000). The species/genus of termite is also determined by the domineering habitat that abounds. The ground dwelling soil

‘eating’ termite genus are more generalist and are present many different biomes.

However the arboreal nest builders are limited by the amount of leaf litter, dead wood and substrate and are only found in tropical forests. The founding pair is also limited by habitat type (Noirot and Darlington 2000). The literature available does not provide evidence for nor even predict the type of habitat that is associated with arboreal termite abundance.

1.8 Flood Plain (FP) and Terra Firme Forests (TF)

The lowland tropical forests of Amazonia resemble a homogenous-looking landscape (Haugaasen and Peres 2005a). However there are differing temporal patterns that are present in swathes of FP and TF forest which share borders.

Temporal differences can be observed by examining fruiting, leafing or flowering schedules in forest plots (Kinnaird 1992). At similar times of the year FP and TF forests offer niche spaces which are dissimilar and this creates a mosaic of food

12 resources (Haugaasen 2005a). The main differences between FP and TF forests can be easily identified by the physiological differences in the structure of the tree forms; one example is FP forests have above ground rooted trees for the anoxic periods of flood (Wittmann and Parollin 2005) TF does not.

There are many differences and similarities that become apparent when each forest type is compared at a spatial scale. Recent studies have shown that adjacent patches of FP and TF forest have much more species similarity than patches of TF that do not share borders (DeOlivera and Nelson 2001). However assessments of tree phenologies show that the majority of pristine and late successional TF forests have higher tree species diversity than FP forests

(DeOlivera and Mori 1999, Pitmann et al. 1999), Haugaasen 2004 and Whitmann and Parollin 2005). Lower heterogeneity in FP forests has been attributed to the nutrient and mineral pulse from the yearly inundations (Haugaasen and Peres

2005b). The change between an aquatic and a terrestrial phase (Junk et al.

1989a) influences tree species diversity and the structure of the FP forests (Junk et al. 1989b), resulting in a clear zonation along the flooding gradient between FP and TF forest (Whitman and Parollin 2005). Haugaasen and Peres (2005b) also suggest that in general trees drop leaves earlier in the inundation season creating leaf litter. The new leaves will also drop at the start of the dry season in preparation for increased radiation. Increased leaf fall thus increased food resource may account for the higher numbers of termites recorded in FP forests.

13 1.9 Anthropogenic Effects on Termite Colonies

Anthropogenic effects (forest clearance and agriculture) on the structure of termite assemblages have until recently been relatively undocumented in comparison to other vertebrate species (Okwakol 2000). Examples can be found in Abe & Watanabe (1983) and Watanabe, Takeda & Ruaysoongnern (1984) in subtropical areas of Japan and Thailand, Matsumoto (1974 and 1976) in Malaysia,

DeSousa and Brown (1994) in the Brazilian Amazon, Okwakol (2000) in Uganda and Deblauwe et al. (2007). All of the above concluded that termite species richness is dramatically reduced when plots are dug for agriculture due to the niche space of most termites being transformed. Okwakol (Uganda, 2000) found that out of 33 termite species in adjacent forest only seven species persisted over one year of cultivation, 4 species remained after 5 years and after 20 years only 2 species remained with 39 individuals/m2. This was half the number of individuals that was counted at year 1 (74 individuals/m2). On ‘just cleared land’ the total number of individual termites was recorded at >600 individuals/m2. Similar results were recorded by DeSousa and Brown (1994) who compared a contiguous undisturbed part of forest to two distinctly isolated patches nearby. They found that more specialist and rare species were important numerically in the forest fragments but were less species rich than in the contiguous forest. Species that needed large quantities of leaf litter fall could not survive in the forest patches. Deblauwe et al.

(2007) concluded that the more disturbed an area is the more ‘dipauparate’ the

14 species richness of the termite assemblage is. They also suggested similar to

DeSousa and Brown (1994) that the soil feeding termites were more greatly affected by increased disturbance. Strong correlations between disturbance and a decline in wood feeding individuals/ m2 were also observed. As termites are one of the chief decomposers in a tropical forest a great amount of leaf litter or dead wood is needed to ensure the survivability of a colony. In agriculturally disturbed land food availability declines with the increase in disturbance. Pointedly all the three studies above mark microclimate change as one of the biggest other influences on termite assemblage. Many arboreal termite species can survive on agricultural land that has maintained a closed canopy (like some home gardens or shade coffee/cacao plantations). Arboreal species are especially sensitive to forest clearance or tree fall as the niche space to build nests is reduced and food resources fragmented.

15 1.10 Summary

This report attempts to highlight the distribution of arboreal termites and niche space through examining the spatial arrangement of termite colonies in 14.8 hectares of forest. Assessing the abundance/km2 of termitaria will determine whether FP or TF forest support the largest arboreal termite presence. This report will assess the influence on the yearly inundation on termitaria abundance. Habitat heterogeneity and the influence on termitaria will be explored, highlighting the niche space that termite need to survive in tropical wet forests. Data comparing FP and TF forests have not yet been explored in the literature on arboreal termitaria.

This report will not only fill gaps in knowledge on arboreal termitaria but will also comment upon termite populations providing nesting opportunities for cavity nesting birds and the sensitivity of colonies to disturbance. Both previous points provide levity for the instigation of land use management in the South Eastern

Peruvian Amazon as termitaria may offer bird species a refuge in ever fragmenting forests. Large populations of arboreal termites offer evidence that at least part of the biodiversity matrix in the Las Piedras Research Centre Concession is not suffering from anthropogenic interference.

16 1.11. Aims

This project is primarily concerned with the abundance of termitaria and the apparent reasons for their spatial distribution in FP and TF forest. Further the use of termitaria as an important resource for cavity nesting birds will be assessed.

Therefore the aims and objectives of this project are as follows:

1. Determine the abundance (per km2) of arboreal termitaria in both terra firma and

FP forest.

2. Describe the similarities or differences between the two types of forest in relation to termitaria.

3. Examine the relationship between termitaria density and type of habitat recorded.

4. Examine the relationship between size of termitaria and habitat type and termite species.

5. Suggest a total number of the arboreal termitaria recorded that would be of suitable size and type as a nesting resource for cavity nesting birds.

6. Assess the importance of arboreal termitaria as a resource for cavity nesting birds.

17 2.0 Methodology

2.1 The Las Piedras Biodiversity Station

The Las Piedras Biodiversity Station (map reference S12 07.013’, W69 54.166’) is in the department of Madre de Dios in south eastern Peru, on a 4,000 hectare (ha) conservation and Brasil nut concession situated between Manu National Park

(1,532,806 ha) and Bajuaja-Sonene National Park (537,000 ha). It lies at the boundary between tropical moist and subtropical wet forest at 150 m elevation and receives 3,200 mm of rain per year (Brightsmith 2004a, Tosi 1960). The dry season extends from April – October during which monthly rainfall averages 90 to

250 mm (Brightsmith 2004a). The research centre is located in a small (<1 ha) clearing surrounded by mature/successional floodplain (FP) and terra firme forest

(TF) and patches of Aguache palm (Mauntia flexuosa) swamp (Foster et al. 1994).

Although selectively logged over 40 years ago the surrounding forest bore no immediate scars: 86% of trees sampled bore branches above half height suggesting a continued period growth with little disturbance

2.2 Sampling Methods

A pilot study assessing distance sampling was undertaken. At 1Km/h 3 teams of 5 individuals walked 3 different 2000 metre transects in both FP and TF forest. Each time a team member observed a termitaria the clock watch was stopped and the distance from the path (m) and the height (m), width (m), height

18 from ground (m) and termite species (if inhabited) was recorded. The variation in the ability of an individual to observe termitaria from the side of a path was too great. The abundance of termitaria per unit area (km2) was calculated as being average length (cm) from the path multiplied by the length of the path; this was not considered robust enough. A standardised and more robust method for collecting termitaria was proposed, using quadrats of 20 m2, counting and measuring the termitaria within. This method would give a maximum per unit area (either ha or km2). This method was similar to that used by Brightsmith (2000 and 2004).

2.3 Marking the Transects and Negating Edge Effects

By marking each transect every 50 metres the total amount of quadrats per transect and a total area surveyed could be calculated, also providing a standardised method for eliminating bias when selecting plots. Each transect was marked to start 25 metres into the forest to negate ‘edge effect’. Although there are no studies which assess edge effects on arboreal termitaria there are studies which suggest figures for the decline in both species richness and overall individual numbers of termites when edges are created (see section on anthropogenic effects). Clearances of land for a small farm (the start of transect 1) and the clearance of land for a research lodge (at the start of transect 6) (both approximately a hectare) may have caused declines of termitaria near the edge of

19 the forest. Although effects of the edge created by the farm and lodge were not tested in this study, termitaria were observed on all transects for the first 25 metres. All quadrats were measured 1 metre in from the transect paths, again to negate any edge effect. Although 1 metre was an arbitrary distance, a standardised method was required so that measurements began within the

Understorey (interior) rather than in the middle of a transect path (exterior).

2.4 Maximising Termitaria Observations

There were 4 transects in the TF area of the forest that were 4Km and one that was 2.5 Km. In the FP area of the forest 1 transect was 2.5Km and the other

2Km. A possible 520 quadrats could be surveyed in TF and a total of 120 that could be performed in the FP forest using existing transects.

Another pilot was undertaken to assess the maximum number of quadrats that could be measure in 23 days of investigation. Due to the thick understorey foliage in some of the quadrats, initial estimates of between 15 to 20 quadrats per day with two people surveying a quadrat were predicted. This meant that a maximum of 460 quadrats could be surveyed. As the maximum number of quadrats (640) available was larger than 460 not all the available transect could be assessed in 23 days. Therefore transects were marked alternatively on the left and the right hand side. This distribution negated any boundary effect that

20 bisecting the forest with a path may have created. 370 quadrats (20 m2)were assessed; a total area of 14.8 hectares.

The quadrats were then marked at each corner to permit accurate reassessment if required. Two investigators per quadrat observed termitaria by each walking half a quadrat in a standardised way; from the furthest corner to the front and then back again after moving a metre towards the centre of the quadrat until the two investigators met. If termitaria were found then the individual investigator measured it themselves and then resumed walking.

2.5 Measuring Termitaria and Termite Identification

Termitaria was measured (in cm) by hand from the crown to the base

(height) and then at the widest point (standing in front of the termitaria) to give the diameter and therefore the dimensions to re-create an oblate ellipsoid (r1=r2>r3).

Due to the nature of termitaria architecture some of the termitaria are not perfect oblate ellipsoids therefore the final volumes are an approximation based on the height, width and depth at the stipulated points. If the termitaria were too high to reach the following method was used; the dimensions of the termitaria were measured at an angle of 45o using a clinometer. Pythagorean law states that the distance of the investigator from the tree and height of the termitaria from the ground are the same. Using a football as a substitute termitaria a factor can be

21 calculated with which the apparent size of the football diminished each metre from the first measurement at 1 metre. The factor/metre was 1.57. Using the factor the diameter (cm) and height (cm) of the termitaria were calculated using the hypotenuse which was calculated from the length from the tree measurements.

Once these measurements were factored the volume of termitaria could be calculated using the following equation for an oblate ellipsoid:

2 Volume = 4/3 π r1 r2

Brightsmith (2000 and 2004) used a similar technique to measure high termitaria; however when measuring the dimensions of the termitaria the present study used callipers in replacement for measurement grids at the end of a

‘telescope’ (see Brightsmith 2000). The grids needed to be very small (=1mm2) to be accurate, this was almost impossible to do by hand at the research station. The callipers were accurate to 1mm therefore a worthy replacement, less cumbersome and more robust. This final decision was taken after the use of callipers was presented to Brightsmith and the idea was endorsed by all parties. The method of using callipers may be more efficient, enabling measurements of higher termitaria more accurately due to the clear view and sharp edges. If the view of the termitaria was somehow obscured then a different angle was measured and the length from tree was taken.

22 Also recorded were any cavities found in the termitaria; they were measured in the same way as the termitaria. In hindsight measurements of the depth of the cavity could have provided a useful insight into which species may have made the cavity or if the nest was still in use. This would have involved ascending trees which would have been very time consuming and only one member of the team had the necessary skills to attempt the rope work involved. The dimensions were sufficient to assess whether there were animals that had been or were living in the termitaria based on the work performed by Brightsmith (2000 and 2004). Any cavities in trees that were observed were measured in the same way. Termitaria were judged to be inside of a quadrat if the host tree was outside the quadrat. If the host tree was inside the quadrat yet the termitaria was outside of the quadrat then it was not measured. If the termitaria were on a vine then it was estimated inside the quadrat if any part was inside the quadrat boundary. Similarly if the tree housing a cavity was inside the quadrat but the cavity was outside of the quadrat it was not included in the observations and vice versa.

Termites were identified either in the termitaria (nests that could be reached by hand) or in the tunnels that connect the ground to the termitaria. Touching either structure produced an anti predator swarming effect and the termites were easily identifiable. There were no field guides to identify the species of termite that was found therefore each was labelled and given a number 1-6 and stored in alcohol for identification back in the UK. Identification was made possible to genus

23 level. Experts that can identify termites were found in Brazil, Japan and America and the overall identification process was costly, however it was not deemed necessary to procure their services for the scope, analysis and synthesis of this study.

2.6 Habitat Surveys

The growth and successional stages of the forest may influence the abundance of termitaria. Central to this study was the assessment of the significant differences and relationships between tree and plant assemblages in FP and TF forests. The vast majority of each transect (lowest; transect 5= >84%) surveyed was in either FP or TF forest. Variables that were recorded can be found in Appendix A, Table 1. Techniques used to record different variables are presented here. Canopy cover was measured using a sheet of clear plastic with

25 dots placed 2 cm apart to create a measurement square. Each dot represented

4% canopy cover. At each corner of the quadrat the measurement square was held 12 cm away from the face of the observer. The amount of dots that were silhouetted against the sky were recorded. If four dots were counted then this represented an estimated 84% canopy cover. When counting the amount of specific trees each half of the quadrat was assessed by 1 person from each corner.

Each person then estimated how much of the other person they could see and this

24 gave density on a rank of 1-4. Average tree girth was calculated from the five largest trees per quadrat. These were standardised methods used by all to ensure a level of fairness. The height of the two types of forests was considered to be significant due to the yearly inundation however yearly rainfall and temperature were not affected by the height difference. Yearly humidity levels were not assessed.

2.7 Temporal Considerations

The method of collection was deemed not to differ despite the time of year.

It was thought that the rainy season may affect data collection in the FP forest as there may have been large areas that would have been inaccessible. However there is no literature that suggests that the size of termitaria differ from season to season; this assumption is worthy of further investigation. The investigations took place from sunrise to sunset. Both these periods reduced visibility. However this did not affect the ability of the investigators due to the distinctive shape and the silhouette of the termitaria. During heavy rain the ability to see termitaria was impaired and therefore investigations were halted. High wind also halted proceedings due to the danger of being present in the forest at these times.

However the quadrat where the last measurements were taken was noted and then returned to once the weather conditions permitted. Diurnal periods,

25 temperature, or precipitation were not being evaluated for influence on termite abundance. Rain followed by a particularly humid period in the weather may encourage swarming of termite amagos. This was not observed during the investigation.

2.8 Data Analysis

To assess abundance the amounts of termitaria/km2 were calculated (Table

1). The data recorded were non normal and therefore non-parametric tests in

SPSS were performed. For significant differences between FP and TF forests and transects 1 and 2 a Mann Whitney U test was performed. For transects 3-6 a

Kruskal Wallace test was performed. Both were used to assess the whole data set and only quadrats where termitaria or suitable termitaria were found. To assess the dependence of volume of termitaria on the termite residing within regression analysis was performed in SPSS. The habitat data was subject to a series of correlation analysis. A Spearmans rank correlation coefficient test (including calculations of coefficients of determination) was performed to examine relationships between FP and TF forests in quadrats where termitaria were found and where only suitable termitaria were found. This method was also used to analyse relationships between the different transects in either FP or TF forests where termitaria or suitable termitaria were found.

26 Non-Metric Multidimensional Scaling illustrates the distribution of data in space on ordination axis. This is the most widely used distance based ordination method (Palmer 2008). The method minimises the poorness of fit between the ordination and measured ecological distances. In this instance the Gower method was used in the statistics program Past because different data scales were used to describe the different variables in the data set. Using the ordination values (Axis

1= y and Axis 2=x) calculated in Past scatter charts (Figure 1 and 2) were created in SPSS. Each variable is classified in SPSS as a series of reference points to ‘set markers by’ (legacy dialogues option); this allows the points to be plotted in relation to the ordination axis. This illustrates where the data are spatially, in relation to each other.

27 3.0 Results

3.1 Density/km2 of Arboreal Termitaria

228 termitaria were measured in 14.8 hectares of forest which equates to

1540 termitaria/km2. Remarkably 114 termitaria were recorded in both TF and FP forest, however, a smaller area of FP forest was sampled (see table 1). Therefore, termitaria abundance/km2 in the two different types of forest were significantly different (U=7384, nfloodplain=89, nterra firme=291, P=<0.001). TF forest housed 1017 termitaria/km2 and FP forest housed 3167 termitaria/km2. The distribution of termitaria abundance/km2 in FP and TF forests can be examined at transect level in table (See table 1). There was a significant difference in the mean number of termitaria recorded along the different transects (H= 62.7, df=5, P= <0.0001). The highest means were recorded on transects 2 (2.025 termitaria/quadrat) and 1 (0.66 termitaria/quadrat) both of which were FP. The average termitaria/quadrat in FP forest was 1.27 and TF 0.39.

28 Forest type Transect km2/transect surveyed No.Termitaria Termitaria/km 2

Flood Plain 1 0.020 33 2062.50

Flood Plain 2 0.016 81 4050.00

Terra Firme 3 0.034 29 966.66

Terra Firme 4 0.036 24 800.00

Terra Firme 5 0.035 26 866.66

Terra Firme 6 0.023 35 1590.90

Totals 0.148 228 1540.54

Flood Plain (Suitable termitaria only) 0.036 29 805.56

Terra Firme (Suitable termitaria only 0.122 28 220.50

Table 3.1. Shows the termitaria/km2 on transects 1-6, the number of termitaria recorded, the type of forest, total km2/transect surveyed per transect and the totals for the whole area.

29 3.2 Abundance of Active/Inactive and Suitable Termitaria

The total number of termitaria active/inactive were 168 (74%) and

60 (26%) respectively. In FP and TF forests 86 (74%) and 82 (73%) and 30 (27%) and 30 (26%) of termitaria were active/inactive respectively. 57 termitaria (25% of the overall termitaria recorded) or

385 termitaria/km2 were a suitable size (>=9 litres) and height (>=5 metres) for primary cavity nesting birds to excavate (Brightsmith 2000).

Of these, 46 (80.7%) were active and 11 (19.3%) inactive. FP and TF forests housed 23 (50%) and 23 (50%) of active termitaria and 5

(45.5%) and 6 (54.5%) of the inactive termitaria respectively. The mean number of suitable termitaria recorded were significantly higher in FP forest than TF forest (U=20861.5, nfloodplain=140, nterra firme=331, P=0.005).

3.3 Termitaria Volume (l3) and Habitat Associations

The volumes (l3) of suitable termitaria were not significantly different. Termitaria are more likely to be predated upon or become inactive due to some abiotic influence when small or lower to the ground. Only one significant difference was found in plots, where suitable termitaria were found and that was leaf litter; this is a main food source of arboreal termites and may explain the higher abundance of termitaria in FP forest. Significant differences in the habitat variables can be found in Table 2 and 3.

30 Highest Factor U P mean value

Height From Ground (cm) 13058.0 <0.001 Flood Plain

Size of Active Termitaria (l3) 14864.5 <0.001 Flood Plain

Size of Inactive Termitaria (l3) 21147.0 0.011 Flood Plain

No. of Active suitable Termitaria 17090.0 <0.001 Flood Plain

No. of Inactive suitable Termitaria 21580.0 0.011 Flood Plain

Girth of Tree Where Termitaria Was 13009.5 <0.001 Flood Plain Found (cm) Canopy Cover (%) 16134.0 <0.001 Terra Firme

Average Tree Girth (%) 16272.0 <0.001 Terra Firme

Fallen Trees 14939.0 <0.001 Terra Firme

Forest Density (rank) 15347.0 <0.001 Terra Firme

Gradient of Slope 17230.0 <0.001 Terra Firme

Width of Path (cm) 12831.0 <0.001 Terra Firme

No. Species of Flowers 20566.0 0.001 Terra Firme

Balsa Presence 21676.0 0.002 Flood Plain

Bamboo Presence 22318.0 0.013 Flood Plain

Strangler Presence 22390.0 0.042 Flood Plain

Table 3.2. The significant differences between FP and TF forest habitat data for all plots.

31 Factor U P Highest mean value Average Tree Girth (cm) 4657.5 0.024 Terra Firme

Fallen Trees 4395.5 <0.001 Terra Firme

Forest Density 4588.5 0.014 Terra Firme

Gradient of Slope 4932.0 0.042 Terra Firme

Width of Path (cm) 4207.0 0.001 Terra Firme

No. Species of Flowers 4821.0 0.001 Terra Firme

Balsa Presence 5241.0 0.020 Flood Plain

Leaf Litter (only suitable termitaria 159.0 <0.001 Flood Plain plots) (cm)

Table 3.3. The significant differences between FP and TF forest habitat where all termitaria and suitable termitaria were recorded

3.4 Correlations between Plots with All and Suitable Termitaria

Plots that housed just termitaria produced significant correlations.

For comparison the results of these correlations (including coefficient of determination) can be found Appendix B, tables 1 (FP correlations) and

2 (TF correlations). These tables are evidence of habitat relationships that may increase termitaria abundance. There are many different factors that may influence suitable termitaria abundance. The volume

(l3) of suitable termitaria was correlated negatively to four habitat data

(Table 4) suggesting that increased presence of these factors would predict a fall in suitable termitaria size. However the coefficient of

32 determination is low in all cases therefore further investigation in different FP and TF forests may strengthen this assumption. Table 4 highlights significant correlations between habitat variables that were recorded in plots where suitable termitaria were present. Palms >5 metres were highly prevalent in many of the plots where suitable termitaria were found. Many of the factors that influence the longevity of termitaria survival were strongly correlated with each other. These initial investigations show part of the habitat matrix in which termites will flourish.

s 2 Factor 1 Factor 2 r Rs P

Canopy Cover Palms >5m 0.88 77.44 <0.001

Average Tree Girth Palms >5m 0.84 70.56 <0.001

Fallen Trees Palms >5m 0.53 28.09 <0.001

High Density Palms >5m 0.85 72.25 <0.001

High Leaf Litter Palms >5m 0.90 81.00 <0.001

Cercropia Presence Palms >5m 0.34 11.56 <0.001

Balsa Presence Palms >5m 0.35 12.25 <0.001

Balsa Presence Cercropia Presence 0.49 24.01 <0.001

Table 3.4. The significant correlations between different variables which were present in the quadrats where suitable termitaria were found. These results are indication of where termitaria of a suitable size may be found.

33 2 Factor1 Factor2 rs +/- Rs P

High Density Canopy Cover 0.59 34.81 <0.001

High Density Fallen Trees 0.64 40.96 <0.001

High Density High Leaf Litter 0.85 72.25 <0.001

Fallen Trees High Leaf Litter 0.43 18.49 <0.001

Cecropia Presence High Leaf Litter 0.59 34.81 <0.001

Balsa Presence High Leaf Litter 0.20 4.00 0.02

Palms >5m Size of Suitable -0.27 7.29 0.05 Termitaria Palms rank Size of Suitable -0.30 9.00 0.03 Termitaria Forest Density Size of Suitable -0.27 7.29 0.04 Termitaria Average Tree Girth Size of Suitable -0.29 8.41 0.03 Termitaria

Table 3. 4. Continued.

There was no significant correlations with any of the Diptocarp

(Dipteryx) species, strangler fig (Ficus) species, Aguache Palm

(Maunitia flexousa), Ceiba (Ceiba) species, Brasil Nut

(Bertholletia excelsa) or Bamboo (tribe Bambuseae). The

above were not present in any of the quadrats that housed suitable

termitaria. There were numerous significant positive and negative

correlations between FP and TF forest habitat data (Appendix 2

34 Table1 and 2). To highlight the distribution of these relationships

and show clusters of habitat data a Non-Metric Multidimensional

Scaling was performed on data for all plots and just plots where

suitable termitaria were found.

3.5 Non-Metric Multidimensional Scaling (NMDS)

Figure 1 illustrates the differences between FP and TF forest at a spatial scale and shows that there is a major split between the two different types of forest. This is possibly due to the inundation amongst other temporal dynamisms. Figure 2 illustrates the distribution of palms

>5 metres. This was the only variable in plots that housed suitable termitaria that showed any clustering.

Each of the points relates to a single plot and the space within the data set where the plot can be found. Plotted on ordination axis the drivers for the spatial distribution of each plot can be derived by correlating each variable with the ordination values. The significant correlations (with coefficient of determination) between axis 1 and 2 and the habitat data illustrated figure 1 and 2 are shown in Appendix 3, tables 1 and 2.

. f o o n

, . h t e s c d e i n e w r e

t , s e e n r p e l p o l l a a s f i

f , p o y o

t r t i c s n r n e i e e c d

d , a t r s s r g

e e , t r h e o t f r i m , g s

5 e e i < e c r s t e

p m e l

s Figure 1. NMDS plot showing the major axes of variation g a r a p e r

f in the dataset of all quadrats. Quadrats closer together on e w o v

o r l a f

the plot are more similar in the ecological parameters that e f n b i o

m r e persist there. The line shows the separation using u s e n a b

, e r m r c e u v n n i

o , c n s

h R a e y i Type of Forest

e 0.20 p c s

g o e n

n p Flood Plain

Terra Firme e

m h r p

a R p o

n c 0.10

0.00 x

r m -0.10

n -0.20

-0.20 -0.10 0.00 0.10 0.20 Axis 1

Represents an increase in gradient of slope, canopy cover, no. of fruit species, no. of flower species, balsa presence

Represents an increase in average tree girth, width of path, girth of tree where termitaria were found, no. palms >5 metres, palm presence, cercropia presence, strangler fig presence,36 forest density, fallen trees, height from ground. .

a ) i 3 r l ( a

t i e m m r u e l t

o e v l

a discriminate analysis based on the split between TF and FP a i t r i a u t forest. i s

m e r v i e t t

c e a l n b i / a t e i v u i t s

c f a o

f ) 3 o l

h e g i m e u l h

o , v a

i r d a e t i s a m r e r e t c

v i n t a c

a s t n i

s R n /

o e s v

p p i e t

r Ranked no. of palms c

i .00 3.00

s h 1.00 4.00

0.10 2.00

i 0.00

e -0.10

-0.20 -0.10 0.00 0.10 0.20 0.30 Axis 1

no. of fallen trees, gradient of the slope species of fruit and flowers.

Volume (l3) of active and inactive termitaria

37 Figure 2. . NMDS plot showing the major axes of variation in the dataset of all plots (Quadrats). Two distinct clusters of plots show where 60% of all suitable termitaria were recorded. Quadrats closer together on the plot are more similar in the ecological parameters that persist there. The line shows the separation using discriminate analysis based on the split between TF and FP forest.

3.6 Termites Diversity and Distribution

There was a significant difference between the different types of termite found in all quadrats (H=16.507, df=8, P= <0.036). The termite

Nasutitermes corniger had the highest mean rank. The distribution of termitaria species for all plots and plots with only termitaria can be found in table 5. The volume of a termitaria was not dependent on the inhabiting species of termite (y=20454.9 -17105.1x, F 1,421=0.7,

P=0.405). There were a total of 6 cavities observed in termitaria and they all appeared to be situated in suitable termitaria.

38 Termite or Ant Terra Flood Totals Terra Firme Flood Plain Totals Firme Plain (Termitaria only) (Termitaria only) Plots with no termite presence 73.6 34.3 62.1 36.1 25.9 31.7 Nasutitermes species (T1) 5.2 20.9 10.2 19.5 18.5 19.0 Nasutitermes species (T2) 0.6 0.0 0.4 0.0 0.0 0.0 Nasutitermes corniger (T3) 13.9 34.3 20.1 25.0 48.1 34.9 Costrictorforms cavifrons (T4) 3.3 0.0 2.3 16.7 0.0 9.5 Nasutitermes species (T5) 1.2 0.0 0.8 2.8 3.7 3.2 Nasutitermes species (T6) 0.3 3.0 0.6 0.0 3.7 1.6 Red Biting Ant (T7) 0.3 3.0 0.6 0.0 0.0 0.0 Black Biting Ant (T8) 1.5 4.5 2.3 0.0 0.0 0.0

Table 3.5. The percentage of termites found in the two forest types in all plots and plots with just suitable termitaria.

39 3.7 Cavities and Cavity Nesting Bird Presence

Termitaria Cavities and Tree cavities were measured however zero birds were observed nesting in either. There were 12 cavities in termitaria recorded and 2 cavities in trees recorded (Averages =

22.2cm2 and 4cm2 respectively). This may have been due to the time of year as the study took place 1 month before nesting season for all of the primary excavators. However there was a flush of cobalt winged parakeets observed from a termitaria that was not present on the study transects. This sighting was confirmed twice, suggesting that birds may use this resource both in an out of nesting season. Therefore further studies into the annual cycles of termitaria use would be strongly recommended. There were no birds observed nesting in the termitaria, however detailed descriptions of the dimensions of the nests different species of cavity nesting birds use can be found in Brightsmith (2000,

2003 and 2004).

40 4.0 Discussion

4.1 Termitaria Abundance (km2) and Influencing Factors

Termitaria were more abundant/km2 in FP and on both of the FP transects than TF forests (table 1). In relation to these findings the discussion will highlight the direct and indirect influence of temporal dynamisms within the two forests types on the behaviour of arboreal termites. In particular the discussion focuses on:

 FP inundations

 Habitat Heterogeneity

 Nest building behaviour

 Foraging behaviour

 Food resources

 Predation

The foraging, feeding and nest building behaviour of termites support the results of this study (Lepage and Darlington 2000 and Noirot 2000).

The importance of termitaria use by cavity nesting birds and areas for further study and development are recommended.

41 4.2 Termites, Habitat and Temporal Dynamisms

The phenomenon of the annual inundation is a noteworthy difference between the FP and TF forests (Philips et al. 1994). The forest surrounding the Las Piedras have no data which highlight the level of flooding in the FP forests. If flooding happens irregularly the effects on termite populations are still apparent on a yearly timescale due to the rise of the water table (Darlington and Noirot 2000 and Nebel et al, 2001). The FP forest at Las Piedras housed typical FP specialist species, further evidence of consistent flooding. The inundation in FP forests creates ‘special’ environments (Nebel et al 2001; South Eastern

Peru). Regular flooding with nutrient rich sediment promotes significantly higher soil nutrient levels. The impacts of which are highlighted in the significant differences and relationships between FP and TF forests shown in shown in table 2 and 3 and in Appendix B tables 1 and 2. Leaf litter levels, canopy cover, forest density, girth of tree, girth of tree where termitaria were found and the existence of pioneer species being noteworthy differences and relationships.

Haugaasen and Peres (2005a) confirm that FP trees generally drop leaves early in the inundation season creating leaf litter. The new leaves will also drop at the start of the dry season in preparation for increased radiation. Therefore increased biomass comes from litter left from before and after the inundation.

42 Forest structure and abundant food resource have a profound effect on termite and therefore termitaria abundance from the initial phases of building new nests through to the expansion and protection of a colony. The founding termite pair of an arboreal nest often begins the colonisation of a new site in a subterranean phase (Noirot and

Darlington 2000) and then with satellite nests on smaller branches

(Oster 1978 and Wilson, Roisin 1987). It would seem that FP forests offer more opportunity for termite founding pairs to purport this sort of behaviour. FP Understorey density was significantly lower than that of

TF (table 2). The FP Understorey is characterised by hardy pioneer tree species with a limited amount of understorey shrubbery (Haugassen and

Peres 2005a). Canopy cover was lower in FP forest; evidence of smaller pioneer species. This also highlights the different successional stages of the understorey in two forest types. TF forests have a higher average tree girth and canopy cover but a lower number of pioneer species. Therefore opportunities for termites to colonise new sites may be reduced by lower amounts of exploitable space (fewer smaller branches on fewer pioneer species) in the TF forests. FP Understorey growth is in a constant flux of successional stages due to the inundation

(Nebel et al 2001), thus suggesting that there are many new colonisation opportunities in FP forests and fewer in TF. Appendix B, tables 1 and 2 show clearly that termitaria in FP forests are found in plots where pioneer species abound yet in TF forests the pioneer

43 species correlate with very few other factors, due to low representation.

The assumption that FP forest offers more opportunities for higher rates of colonisation is made more plausible because there was no significant difference between the heights of suitable termitaria (height =>5 metres, volume=>9 litres) recorded. This suggests that in both types of forest termites in larger nests nest at the same range of heights. Termitaria

(regardless of volume) are significantly lower in height (Table 2) in TF forests suggesting that there were more opportunities for termites to nest at a greater number of lower heights. However the realities of TF forest survival is that worker termites will need to expend more energy to get less nutritious food, therefore building a nest closer to the ground is a sensible option. Proximity to the ground equates to less energy expenditure and a closer proximity to food source. This would also render a nest at a higher risk of predation. Possibly due to the inundation termites in FP forest build nests higher; to protect from predation and flood but also because of a higher nutritional value in the food source; building a nest higher is therefore less of a limiting factor.

This prediction has not yet been quantified but is based on the behaviour traits of arboreal species of termite (Noirot and Darlinton

2000).

Further assessment of termitaria using the above methods but recording differences based on FP and TF forest successional stages

44 and using more detailed habitat quantifiers may unmask optimum conditions in which termites thrive.

4.3 Heterogeneity Levels in FP and TF Forests

The inundation is a form of ecological regulation and renewal which is a major indirect driver of larger abundances of termites and therefore suitable termitaria for cavity nesting birds to nest in. The inundation is also a main driver for decreased heterogeneity in FP forests (Nebel et al. 2001, Philips et al. 1994). Stress factors such as persistent flood pulses, anoxic or hypoxic water conditions, interruption of photosynthesis by complete or partial submergence of many trees is a cause for lower floristic diversity in FP forests (Kubitzki 1989). FP forest environments have a considerably simplified forest structure due to the lack of Understorey and proximity to the water table (Haugaasen and Peres 2005a). As a result many of the species in forest where there is flooding have developed specialist mechanisms for survival, for example above ground roots (Halle et al. 1978 and Pavliss and Jenik

2000). This can explain the habitat differences recorded in this study

(Tables 2, 3 and 4 and Appendix A, B, C and D tables 1 and 2) and further weight the evidence of higher termite abundance in FP forest.

Analysis of each transect showed that there was far greater heterogeneity in the TF forest. Almost twice as many significant

45 differences were recorded between transects 3, 4, 5 and 6 in TF than there were on transects 1 and 2 in FP forest (Appendix C table 1 and 2).

Lower heterogeneity of habitat is suited to termite presence and abundance (large colonies with a large range over similar resource rich habitat). The ranges of the termites in this study have not been thoroughly assessed, however based on past studies a general rule exists; the higher the density of nests the higher the opportunities for connectivity, if the habitat is not a limiting factor (Noirot and Darlington

2000). A large tract of similar habitat should suit a large amount of similar organisms. This study recorded 6 different termite species in TF yet only 3 in FP forests. At present there are no studies or literature concerned with species diversity of termites in different types of forest in

Peru. Many studies examine termite diversity in relation to evolutionary events (Eggleton 2000, Higashi et al. 2000 Nalepa and Bandi 2000).

Evidence suggests that tropical termites become less diverse at higher altitudes (Gathrone-Hardy et al. 2001) which may also highlight differences between FP and TF forests. Disturbance of habitat also impacts on termite diversity therefore a lower diversity of arboreal nesting termites in an environment where there is regular disturbance may be plausible as more specialist evolutionary traits are perhaps needed for survival.

The above proposes valid reasons for the larger termite presence in FP forest and the different limits of habitat and colonisation. However

46 the most influential driver of termite presence is food quality and quantity and foraging opportunities (See introduction).

4.4 Nest Building and Strategies for Homeostasis and Provision

Termites are very sensitive to change and the arboreal nest is a very effective air conditioning and water regulating structure (Noirot and

Davenport 2000). Nest architecture is an expression of innate behaviour and is often modified by contact with different environments

(Collias 1964 and Bonabeau et al. 1998). Arboreal nests certainly have to withstand many abiotic pressures; wind, rain, radiation, increased and decreased humidity levels, drought and in the case of FP termites increased levels of surface water and possible flooding.

Arboreal termites are very susceptible to dehydration (especially in young termites) and will often tunnel downwards to reach water and bring it back to the nest in crop or soil form. FP forests are closer to the water table and therefore less limiting than TF forests. This is possibly a major reason for higher arboreal termite abundance in FP forest. A full description of this behaviour can be found in Grasse and Noirot (1948).

TF forest humidity levels are often lower than the FP all year round. Termites prefer higher humidity levels (Noirot and Darlington

2000) and therefore will actively seek areas that are highly humid. Too high humidity and too low humidity could both limit termite abundance and development and therefore an optimum would need to be sought.

47 To test the validity of this theory a point count measure of differing humidity levels along each of the transects could be carried out further adding to the evidence optimum niche space for termites. In areas of low humidity nest design becomes even more important. Energy of the foraging workers is expended on building a tunnel for ground water; a costly exercise especially in TF forest during the dry season. The building of a cooling wind tunnel is often required to maintain temperature. Many soldiers and workers to guarding and build a ‘wind tunnel’ (Darlinton 1997), this is also a limiting factor. No data exists exploring whether termitaria in FP or TF forest termites require a

‘building extension’ at differing times of the year yet it would seem a costly but essential exercise not less suitable to an already limited nest.

Arboreal nesters Nasutitermes have been observed storing food in special chambers, hording for when disturbance is at its zenith (Thorne et al 1996), an evolutionary trait (see introduction) that may mean residing in FP forest is made more viable.

Inactive nests are often re-colonised after a disturbance has dissipated (Collins1977 and1981). Therefore if this study were performed again during the inundation period (November through to

March) an increased number of inactive termitaria may be observed in

FP forests. There is a possibility that flood waters may create islands of certain areas of forest, however many termites can link or bridge gaps between two trees if branches are close enough (pers. observation).

48 Therefore one should not assume a period of inundation is a completely limiting factor. Nest re-colonisation and the ability to create links above the forest floor further diminish the probability that flood waters would act as a significant barrier to foraging.

4.5 Foraging Behaviour of arboreal nesting Termites

Many termites (including Nasutitermes and Constrictitermes observed in this study) forage far from the nest and some colonies have

>300 nests. This phenomenon has been observed in mangroves where connectivity is not limited. In lowland moist tropical forests, colonies of

40 nests have been recorded. Colonies may not be reliant on just one nest to keep the important breeding pairs provided for (Traniello and

Leuthold 2000). A network of nests could be vital throughout a period of inundation as disturbance to flora (and therefore many nesting sites) is likely to be limiting. Unlike other animals that have not developed sterile castes termites can perform the task of foraging at an almost optimal level. The non reproductive workers are specialist foragers, feeders and builders and will spend all their time enacting this evolutionary role

(Traniello and Leuthold 2000). Due to the relatively far reaching foraging distances, multiple nests and specialist foragers, periods of inundation may not be mortally limiting.

49 4.6 Food, Nutrition and Development

Nebel et al’s (2001) aforementioned ‘special conditions’ which the inundation creates cannot be underestimated. The availability of food quality and quantity is of vast importance to the development of a nest or colony. Young termites will generally become 1 of 5 different castes.

Each stage of development requires different conditions in which to propagate the change in morphology; all caste development is subject to natural selection (Watson 1987). Most important at any stage of development is the availability of a food source (Roisin 2000). A larger biomass of, and higher nutrient content in food resources provide termites more opportunities in FP than in TF forest. Poor nutrition (in quantity and quality) in nest building insects has been documented to prevent metamorphosis and result in developmental stasis (Nalepa

1994). In termites this has been shown to stunt wing bud development

(Luscher 1961). This can lead to stasis which could bring on the demise of nest by denuding the breeding pair/s of workers to feed them or more drastically prevent new colonisation events. A nutrient deficient diet could reduce the numbers of nests in the colony until homeostasis is reached (Noirot and Darlington 2000). A probable cause of smaller numbers of termitaria in TF forest is lower nutrient content in the biomass. FP forests will experience a pulse of nutrient rich sediment during an inundation. There is much literature that states that termite presence and colony health rely on a certain homeostatic conditions

50 within the nest and of food sources (Grasse and Noirot 1948, Thomas

1987, Darlington 1997 and Darlington and Noirot 2000). The optimum management of the homeostatic conditions seems to be more suited to nesting in FP forests.

4.7 Predation of Arboreal Termites Nests

A major form of disturbance for termite nests is predation.

Therefore producing many nests in a colony and nesting higher in a tree seems to be a strategy that can give more protection against becoming victim to any of the predatory species. A resource rich environment would seem to be ideal to reproduce this evolutionary stratagem.

Evolutionary processes have shaped termite nesting behaviour (Noirot and Davenport 2000); more viable nests reduce the risk of the founding or breeding pairs being predated on. Although this study did not observe any predation of termitaria evidence shows that there are two main forms of attack. The first is from outside of the nest; a tamandu, ant eater species or armadillo raids the nest and dislodges it from its anchor point. A tamandu (and similar ant eater species) can reach up to three metres on its tail with its tongue (Lubin et al. 1977 and Lubin and

Montgomery 1981). Therefore being higher up equates to being more protected from such an attack. The second major form of predation is from an infestation or swarm of predatory ants (Brightsmith 2000). This sometimes involves colonisation by the attacking force. The larger the

51 nest the greater the number of soldiers or workers (using chemical defence) there will be to repel the attackers (Darlington 1986). Having smaller satellite nests may produce an easy target for ants. The satellite or foraging nests will often not include a breeding pair; perhaps rendering the satellite nests a calculated loss. The investment in defence by many species of the Nasutitermes is said to be relatively high (Leponce et al. 1997). Numbers of individual soldiers may dwindle if the number of workers is threatened; a weakness if the nest cannot function at a near optimal level, for example with low levels of nutrients in the food. Predation is perhaps another way that a homeostatic balance is reached in multiple nest colonies.

4.8 Suitable Termitaria for Cavity Nesting Birds

More suitable termitaria/km2 (table 1) were recorded in FP forest.

However there was no significant difference in the sizes of suitable termitaria found in either forest. Termitaria size is directly related to its age (Darlington et al. 1982); observations of a greater number of suitable and therefore large termitaria suggest greater resource/food availability in FP forests. The mortality of termite nests is an area of research where there is little literature considering the diversity and abundance of nest types. Those that have observed nests over a longer period of time suggest that some may continue to be active and therefore grow for up to 80 years (Lepage and Darlington 2000 report

52 this but feel that there is insufficient evidence to support the researcher’s claims). There is evidence to suggest that the nests may be active for a period of three (Tanno 1993) to ten years (Pomeroy 1977). Longitudinal studies of the nests at the Las Piedras concession would be possible due to the detailed recording of the plots and positions of termitaria.

Recording empirical data regarding the length of time; a) termites need to build a large enough nest and, b) a nest is viable for use by cavity nesting birds will be essential to assess the importance of termitaria as a nesting resource.

The presence of palms >5 metres also indicated where there were fewer opportunities for smaller girth Understorey growth. Large palms can block much of the light due to the large dense frond structure and are fast growing which may hinder other pioneer trees from growth.

Figure 2 showed that there were far more suitable termitaria in plots where there were no palms >5 metres. This was also true of the correlations in table 4; suitable termitaria size decreased as palms >5 metres increased. The presence of palms >5 metres was driven by many different factors (see results on NMDS Figures 1 and 2 and

Appendix D table 1 and 2) all of which were associated with decreasing termitaria size and abundance. There are very distinct biological conditions which can be illustrated by NMDS scaling and in the results of mean comparisons and correlations (Tables 1, 2, 3, and 4 Appendix

A, B, C, D table 1 and 2) which are suitable to house termitaria of such

53 dimensions and height from the ground for cavity nesting birds: areas with no palms >5 metres, where pioneer species are present, low tree girth with relatively high leaf litter, low forest density and canopy cover.

This study predicts that there are over 3 times more suitable termitaria for cavity nesting birds in FP than TF forests. This does not directly relate to the amount of birds nesting at any one time. This study recorded 12 cavities in 57 suitable termitaria and fewer in tree trunks.

Therefore 21% of suitable termitaria had a cavity which suggests that this is an important resource. However not a single bird was observed using termitaria on transect 1-6. This was partly due to the time of year; the nesting season was just about to start when the project finished.

However a greater number of; a) birds using termitaria, and b) cavities recorded was expected. This was due to anecdotal evidence from the area but also from Brightsmith (2000, and 2004) who predicted termitaria availability did not limit reproduction but was indeed a favoured way of nesting. Included in this study were the observations of termitaria along part of the Rio Las Peidras (transect 1 >=400 metres).

River bank termitaria are used as nests by kingfishers and have been shown to be an important resource in Micronesia (Kesler and Haig

2005) another reason why expectations of nesting sightings were high.

Over 20 different sightings of Kingfisher species were made yet no observations of any individuals entering termitaria were made.

54 Although 21% of all suitable termitaria were recorded as having cavities of suitable sizes to house a number of species of bird, it is possible that other animals were using the termitaria. Two termitaria were observed to house bat species and there is literature that highlighted this behaviour as not uncommon (Kalko et al.1999 and

2004).

At present the amount of suitable termitaria per km2 would not seem to limit reproduction of cavity nesting birds at the Las Piedras

Biodiversity Station. Termitaria nesting species are regularly observed at Las Piedras Biodiversity Station and there is no indication of overall bird diversity or individual richness falling (Tatum-Hume pers comm).

To establish how important termitaria are as a nesting resource empirical evidence is needed regarding the longevity of termitaria, the length of time that different species of nesting birds use the nests for, the amount of nests that are found in tree cavities and above all the abundance/km2 of the cavity nesting bird species populating the concession at the Las Piedras Biodiversity Station. The use of termitaria by cavity nesting birds seems low during the dry season therefore another assessment during the nesting and rainy season would highlight, a) any differences between the two seasons and b) the type of forest (if any) that each species of termitaria nesting bird was limited by.

55 6. Conclusions and Recommendations for Future Study

Termitaria are more abundant and larger in FP forests. This is driven primarily by the yearly inundation which creates favourable opportunities for termite colonisation, foraging, feeding and therefore proliferation and reproduction. More empirical studies regarding the daily dynamisms which drive termite abundance and diversity is required to add to the wealth of data collected in this study. The aim of a new investigation would be to highlight spatial and habitat heterogeneity or homogeneity where termitaria abound (partly recorded in this study). FP forest produces the optimum conditions for termitaria colonisation and development. However it is also possible that there may be areas in TF forest where conditions are more suitable than those found in less optimal areas of FP forest. Investigations could also distinguish areas of forest which may be most important for conservation management.

With such wealth of habitat data a combination of more detailed descriptions of the plants that are present in both types of forest where termitaria are present would highlight further the subtle differences between the two types of forest, the transects and even each plot.

Other sites would be sought for investigation for further comparisons

Tunnels were observed (either on trunks of trees or branches) to be active however the nests were non existent; evidence of satellite nest building and/or a subterranean phase. Colonisation of and connectivity in FP and TF forests should be assessed by counting termite tunnels

56 that lead to ‘no nest’ (known as prospective sites) in the two forests types. This would highlight the optimum conditions for connectivity and colony size.

Lowland tropical rainforests are under threat from the expansion of large and small scale agriculture. It is clear that at present there is an abundant resource of nest sites for cavity nesting birds. However it is also apparent that the same forest that holds the highest number of suitable termitaria/km2 in which cavity nesting birds may reside is the same that is under most threat. This is partly due to FP forests fertility but also because many new settlements use the river very much like roads. Thus new river settlements in FP forests are the most accessible for development.

Breeding pairs of birds have larger ranges and are far less abundant than termites and termitaria therefore habitat alteration creating fragmented islands may render termitaria a non resource for cavity nesting birds. Conversely termitaria may become the only viable nest site in a habitat island. The diversity and abundance of termitaria and cavity nesting bird reproduction in fragmented patches of FP and TF forests would highlight the importance of termitaria as a nesting resource.

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67 Appendices

Appendix A. Table 1. Full list of variable recorded on habitat survey

Variable Terra Firme Flood Plain Terra Firme Flood Plain (Termitaria only) (Termitaria only)

Height of termitaria from ground 122.01+/-13.07 312.65+/-28.73 742.51+/-33.24 843.30+/-61.13

Total litres N/A N/A 98.45+/-19.60 112.74+/-35.39

Litres of active termitaria 67.37+/-8.46 90.7+/-16.15 77.79+/-17.03 90.18+/-31.30

Litres of inactive termitaria 104.1+/-28.49 109.1+/-38.85 20.66+/-14.31 22.56+/-20.73

Girth of tree where termitaria was found (CM) 56.05+/-7.87 97.61+/-8.32 158.07+/-24.33 158.21+/-19.77

Average tree girth in plot (CM) 98.79+/-4.05 65.34+/-6.14 59.29+/-13.75 65.37+/-14.18

Canopy Cover (%) 86.35+/-0.80 84.63+/-3.36 87.13+/-0.89 87.41+/-1.66

Fallen Tree Old 0.43+/-0.03 0.36+/-0.04 0.20+/-0.12 0.11+/-0.06

Fallen Tree New 1.01+/-0.07 0.48+/-0.13 0.50+/-0.16 0.22+/-0.12

Forest Density 1.69+/-0.08 0.98+/-0.10 1.00+/-0.25 0.82+/-0.19

68 Appendix A. Table 1 Continued

Variable Terra Firme Flood Plain Terra Firme Flood Plain (Termitaria only) (Termitaria only) Leaf Litter Average 0.90+/-0.04 1.11+/-0.11 1.38+/-0.10 2.28+/-0.16

Path 87.99+/-4.21 35.32+/-3.66 39.23+/-12.95 35.52+/-7.97

No Species Fruiting 0.24+/-0.03 0.19+/-0.04 0.27+/-0.13 0.15+/-0.09

No Sp Flowering 0.17+/-0.02 0.06+/-0.03 0.23+/-0.10 0.07+/-0.05

Dipt 0.02+/-0.01 0.01+/-0.01 0.00+/-0.00 0.04+/-0.04

Balsa 0.02+/-0.01 0.09+/-0.03 0.03+/-0.03 0.07+/-0.05

Palm 0.19+/-0.02 0.16+/-0.03 0.10+/-0.06 0.19+/-0.08

Cercropia 0.06+/-0.01 0.14+/-0.05 0.03+/-0.03 0.26+/-0.14

Strangler 0.01+/-0.01 0.04+/-0.02 0.00+/-0.00 0.04+/-0.04

Palms >5 Metres 1.96+/-0.12 3.23+/-0.37 1.43+/-0.42 3.89+/-1.02

Ceiba 0.01+/-0.00 0.01+/-0.01 N/A N/A

Bamboo 0.01+/-0.00 0.22+/-0.19 N/A N/A

69 Appendix B

Table 1. Significant Correlations within the FP area of the forest on the Rio Las Piedras

70 s 2 Factor 1 Factor 2 r Rs P

s 2 FactorCercropia 1 Presence PalmsFactor > 2 5 Metres 0.33r 10.89Rs <0.001P Path (cm) Canopy Cover (%) 0.81 65.61 <0.001 Balsa Presence Palms > 5 Metres 0.45 20.25 <0.001 No. of Flower Species Canopy Cover (%) 0.37 13.69 0.001 Palms in Understorey Palms > 5 Metres 0.31 9.61 0.001 No. of Fruit Species Canopy Cover (%) 0.26 6.76 <0.001 No. of Flower Species Palms > 5 Metres 0.19 3.61 <0.023 Cercropia Presence Canopy Cover (%) 0.27 7.29 0.004 No. of Fruit Species Palms > 5 Metres 0.25 6.25 <0.046 Balsa Presence Canopy Cover (%) 0.33 10.89 0.001 Path Width (cm) Palms > 5 Metres 0.58 33.64 <0.001 Palms in Understorey Canopy Cover (%) 0.48 23.04 <0.001 Gradient Palms > 5 Metres 0.46 21.16 <0.001 Fallen Trees Average Tree Girth of Where 0.28 7.84 0.004 Leaf Litter (cm) PalmsTermitaria > 5 MetresFound (cm) 0.82 67.24 <0.001 Leaf Litter (cm) Average Tree Girth of Where 0.82 67.24 <0.001 Forest Density PalmsTermitaria > 5 MetresFound (cm) 0.78 60.84 <0.001 Gradient Average Tree Girth of Where 0.37 13.69 <0.001 Fallen Trees PalmsTermitaria > 5 MetresFound (cm) 0.53 28.09 <0.001 Path (cm) Average Tree Girth of Where 0.75 56.25 <0.001 Average Tree Girth (cm) PalmsTermitaria > 5 MetresFound (cm) 0.80 64.00 <0.001 No. of Flower Species Average Tree Girth of Where 0.32 10.24 0.001 Canopy Cover (%) PalmsTermitaria > 5 MetresFound (cm) 0.82 67.24 <0.001 No. of Fruit Species Average Tree Girth of Where 0.20 4.00 0.036 Bamboo Presence PalmsTermitaria > 5 MetresFound (cm) 0.17 2.89 0.012 Cercropia Presence Average Tree Girth of Where 0.25 6.25 <0.001 Average Tree Girth (cm) CanopyTermitaria Cover Found (%) (cm) 0.88 77.44 <0.001 Balsa Presence Average Tree Girth of Where 0.39 15.21 <0.001 Fallen Trees CanopyTermitaria Cover Found (%) (cm) 0.37 13.69 <0.001 Palms in Understorey Average Tree Girth of Where 0.37 13.69 <0.001 Forest Density CanopyTermitaria Cover Found (%) (cm) 0.80 64.00 <0.001 Forest Density Fallen Trees 0.26 6.76 0.007 Leaf Litter (cm) Canopy Cover (%) 0.85 72.25 <0.001 Leaf Litter (cm) Fallen Trees 0.39 15.21 <0.001 Gradient Canopy Cover (%) 0.45 20.25 <0.001 Gradient Fallen Trees 0.32 10.24 0.001

Path (cm) Fallen Trees 0.24 5.76 0.012

Appendix B, Table 1. Continued

71 Appendix B, Table 1 Continued

s 2 Factor 1 Factor 2 r Rs P Forest Density Fallen Trees 0.26 6.76 0.007

Leaf Litter (cm) Fallen Trees 0.39 15.21 <0.001

Gradient Fallen Trees 0.32 10.24 0.001

Path (cm) Fallen Trees 0.24 5.76 0.012

Leaf Litter (cm) Forest Density (rank) 0.72 51.84 <0.001

Gradient Forest Density (rank) 0.41 16.81 <0.001

Path (cm) Forest Density (rank) 0.73 53.29 <0.001

No. of Species of Fruit Forest Density (rank) 0.25 6.25 0.010

Cercropia Presence Forest Density (rank) 0.31 9.61 0.001

Balsa Presence Forest Density (rank) 0.32 15.21 0.001

Palms in Understorey Forest Density (rank) 0.31 53.29 0.001

Gradient Leaf Litter (cm) 0.39 10.24 <0.001

Path (cm) Leaf Litter (cm) 0.73 5.29 <0.001

No. of Species Fruit Leaf Litter (cm) 0.32 4.84 0.001

Cercropia Presence Leaf Litter (cm) 0.23 7.29 0.010

Balsa Presence Leaf Litter (cm) 0.22 7.29 0.010

Understorey Palm Leaf Litter (cm) 0.27 6.76 0.006 Presence Path (cm) Gradient 0.27 12.25 0.029

No. of Species Fruit Gradient 0.26 10.89 0.021

72 Cercropia Presence Gradient 0.35 4.84 <0.001

Appendix B. Table 1 Continued

s 2 Factor 1 Factor 2 r Rs P Balsa Presence Gradient 0.33 21.16 0.002

No. of Species Fruit Path (cm) 0.59 9.00 <0.001

No. of Species Flowers Path (cm) 0.41 16.81 <0.001

Balsa Presence Path (cm) 0.19 3.61 0.046

Understorey Palm Path (cm) 0.49 24.01 <0.001 Presence No. Species Flowers No. of Species Fruit 0.33 10.89 <0.001

Balsa Presence No. of Species Fruit 0.22 4.84 0.027

Understorey Palm No. of Species Fruit 0.46 21.16 0.001 Presence Understorey Palm No. of Species Flowers 0.30 9.00 0.002 Presence Balsa Presence Cercropia Presence 0.41 16.81 <0.001

73 Appendix B. Table 2. Significant Correlations with Coefficient of Determination within the TF area of the forest on the Rio Las Piedras

s 2 Factor 1 Factor 2 r Rs P Palms in Understorey Palms > 5 Metres 0.35 12.25 0.001

No. of Flower Species Palms > 5 Metres 0.31 9.61 <0.001

No. of Fruit Species Palms > 5 Metres 0.38 14.44 <0.001

Path Width (cm) Palms > 5 Metres 0.69 47.61 <0.001

Gradient Palms > 5 Metres 0.47 22.09 <0.001

Leaf Litter (cm) Palms > 5 Metres 0.67 44.89 <0.001

Forest Density (rank) Palms > 5 Metres 0.77 59.29 <0.001

Fallen Trees Palms > 5 Metres 0.60 36.00 <0.001

Average Tree Girth Palms > 5 Metres 0.70 49.00 <0.001 (cm) Canopy Cover (%) Palms > 5 Metres 0.75 56.25 <0.001

Inactive Termitaria Palms > 5 Metres -0.22 4.84 <0.001 Volume (l) Average Tree Girth Canopy Cover (%) 0.78 60.84 <0.001 (cm) Fallen Trees Canopy Cover (%) 0.55 30.25 <0.001

Forest Density (rank) Canopy Cover (%) 0.76 57.76 <0.001

Leaf Litter (cm) Canopy Cover (%) 0.77 59.29 <0.001

Gradient Canopy Cover (%) 0.58 33.64 <0.001

Path (cm) Canopy Cover (%) 0.66 43.56 <0.001

Palms in Understorey Palms > 5 Metres 0.35 12.25 0.001

Appendix B, Table 2. Continued

74 Appendix B, Table 2. Continued

s 2 Factor 1 Factor 2 r Rs P No. Species Fruit Fallen Trees 0.27 7.29 0.005 Factor 1 Factor 2 rs R 2 P Active Termitaria Fallen Trees -0.30 9.00s 0.002 Volume HeightNo. of FlowerFrom Ground Species CanopyFallen Trees Cover (%) -0.220.33 10.894.84 0.001 (cm) No. of Fruit Species Canopy Cover (%) 0.29 8.41 0.003 Leaf Litter (cm) Forest Density (rank) 0.82 67.27 <0.001 Palms in Understorey Canopy Cover (%) 0.33 10.89 0.001 Gradient Forest Density (rank) 0.47 22.09 <0.001 Height From Ground Canopy Cover (%) -0.28 7.84 0.014 Path(cm) (cm) Forest Density (rank) 0.73 53.29 0.005 Inactive Termitaria Canopy Cover (%) -0.38 14.44 <0.001 No.Volume of Species (l) Fruit Forest Density (rank) 0.26 6.76 <0.001 Fallen Trees Average Tree Girth of Where 0.61 37.21 <0.001 No. of Species Flowers TermitariaForest Density Found (rank) (cm) 0.32 10.24 <0.001 Gradient Average Tree Girth of Where 0.69 47.61 <0.001 Height From Ground TermitariaForest Density Found (rank) (cm) -0.27 7.29 <0.001 (cm)Leaf Litter (cm) Average Tree Girth of Where 0.80 64.00 <0.001 Palm in Understorey TermitariaForest Density Found (rank) (cm) 0.77 59.29 <0.001 Gradient Average Tree Girth of Where 0.57 32.49 <0.001 Inactive Termitaria TermitariaForest Density Found (rank) (cm) -0.28 7.84 0.005 VolumePath (cm) (l) Average Tree Girth of Where 0.66 43.56 <0.001 Gradient TermitariaLeaf Litter Found (cm) (cm) 0.43 18.49 <0.001 No. of Flower Species Average Tree Girth of Where 0.34 11.56 0.001 Path (cm) TermitariaLeaf Litter Found (cm) (cm) 0.63 39.69 <0.001 No. of Fruit Species Average Tree Girth of Where 0.42 17.65 0.002 No. of Species Fruit TermitariaLeaf Litter Found (cm) (cm) 0.35 12.25 0.006 Inactive Termitaria Average Tree Girth of Where 0.30 9.00 0.001 No.Volume of Species (l) Flowers TermitariaLeaf Litter Found (cm) (cm) 0.39 15.21 0.001 Palms in Understorey Average Tree Girth of Where 0.26 6.67 0.007 Balsa Presence TermitariaLeaf Litter Found (cm) (cm) 0.23 5.29 <0.001 Forest Density (rank) Fallen Trees 0.55 30.25 <0.001 Understorey Palm Leaf Litter (cm) 0.41 16.81 <0.001 PresenceLeaf Litter (cm) Fallen Trees 0.50 25.00 <0.001 Inactive Termitaria Leaf Litter (cm) -0.28 7.84 0.003 VolumeGradient (l) Fallen Trees 0.62 38.44 <0.001 Height From Ground Leaf Litter (cm) -0.24 5.76 0.012 Path (cm) Fallen Trees 0.68 46.24 <0.001 Path Gradient 0.63 39.69 <0.001 No. Species Flower Fallen Trees 0.27 7.29 0.005

75 Appendix B. Table 2 Continued

s 2 Factor 1 Factor 2 r Rs P Inactive Termitaria Gradient 0.26 6.76 0.007 Volume (l) Height From Ground Gradient -0.38 14.44 <0.001

No. of Species Fruit Path (cm) 0.25 6.25 0.006

No. of Species Flowers Path (cm) 0.31 9.61 0.001

Understorey Palm Path (cm) 0.20 4.00 0.040 Presence Inactive Termitaria Path (cm) -0.28 7.84 0.007 Volume (l) Active Termitaria Path (cm) -0.21 4.41 0.030 Volume (l) No. Species Flowers No. of Species Fruit 0.39 15.21 <0.001

Balsa Presence No. of Species Fruit 0.31 9.61 0.001

Balsa Presence No. of Species Flowers 0.29 8.41 0.002

Understorey Palm Balsa 0.32 10.24 0.001 Presence Cercropia Presence Understorey Palm Presence 0.39 15.21 <0.001

76 Appendix C: Table 1 Significant differences between transects 1 and 2 in the FP forest.

Forest Type Factor U P Order of Mean Rank (Transect)

Flood Plain Girth of tree where termitarium was found (cm) 1772.5 0.037 2,1

Flood Plain Fruit and Flower species present 2069.0 0.020 2,1

Flood Plain No. of Species of Fruit 1757.0 <0.001 1,2

Flood Plain Gradient of Path 1741.0 <0.001 2,1

Flood Plain Palm Presence 1285.0 <0.001 1,2

Flood Plain Cercropia Presence 2000.0 0.015 2,1

Flood Plain Bamboo Presence 2052.5 0.014 1,2

77 Appendix C: Table 2. Significant differences between transects 3-6 in TF forest.

Forest tyupe Factor H P Order of Mean Rank (Transect)

Terra Firme Girth of tree where termitaria was found (cm) 13.37 0.004 6,3,5,4

Terra Firme Canopy Cover (%) 10.59 0.014 3,4,5,6

Terra Firme Architecture 10.98 0.012 6,3,4,5,

Terra Firme Fruits and flowers present 10.17 0.017 4,6,3,5

Terra Firme No. of Species Fruit 8.02 0.046 3,4,5,6

Terra Firme Gradient 12.65 0.005 4,6,5,3

Terra Firme Dipteryx Presence 16.76 0.001 3,4,5,6

Terra Firme Balsa Presence 22.48 <0.001 3,4,5,6

Terra Firme Palm Presence 234.8 <0.001 3,4,5,6

Terra Firme Cercropia Presence 64.63 <0.001 3,4,5,6

Terra Firme Bamboo 8.30 0.040 3,4,5,6

Terra Firme Strangler Fig Presence 11.10 0.011 3,4,5,6

Terra Firme Palms >5 Metres 20.30 <0.001 3,6,5,4

78 Appendix D. Table 1. Significant Correlations (with coefficient of determination) between ordination axis 1 and 2 and the habitat data for all plots.

s 2 Factor 1 Factor 2 r Rs P

Axis 1 (x) Average tree girth (cm) 0.36 12.96 <0.001

Axis 2 (y) Average tree girth (cm) -0.40 16.00 <0.001

Axis 1 (x) Gradient of slope 0.35 12.25 <0.001

Axis 2 (y) Gradient of slope 0.18 3.24 <0.001

Axis 1 (x) Width of path (cm) 0.46 21.16 <0.001

Axis 2 (y) Width of path (cm) -0.26 6.76 <0.001

Axis 1 (x) Girth of Tree Where -0.53 28.09 <0.001 Termitaria Was Found (cm) Axis 2 (y) Girth of Tree Where -0.18 3.24 <0.001 Termitaria Was Found (cm) Axis 1 (x) Canopy Cover (%) 0.40 16.00 <0.001

Axis 2 (y) Canopy Cover (%) 0.45 20.25 <0.001

Axis 1 (x) Numbers of palms >5m 0.23 5.29 <0.001

Axis 2 (y) Numbers of palms >5m -0.50 25.00 <0.001

Axis 2 (y) Palm Presence -0.27 7.29 <0.001

Axis 1 (x) Cecropia Presence 0.01 0.01 0.04

Axis 2 (y) Cecropia Presence -0.18 3.24 <0.001

Axis 2 (y) Bamboo Presence 0.12 1.44 0.009

Axis 2 (y) Strangler Fig Presence -0.21 4.41 <0.001

Axis 1 (x) No. of Fruit Species 0.16 2.56 0.001

Appendix D. Table 1 Continued

79 s 2 Factor 1 Factor 2 r Rs P Axis 2 (y) No. of Fruit Species 0.26 6.76 <0.001

Axis 1 (x) No. of Flower Species 0.22 4.84 <0.001

Axis 2 (y) No. of Flower Species 0.23 5.29 <0.001

Axis 2 (y) Balsa Presence 0.25 6.25 <0.001

Appendix D: Table 2. Significant Correlations (with coefficient of determination) between ordination axis 1 and 2 and the habitat data for plots with suitable termitaria only.

80 2 Factor1 Factor2 rs Rs P

Axis 1 (x) Size of termitaria (rank) 0.32 10.24 0.014

Axis 1 (x) Total litres (l) 0.33 10.89 0.011

Axis 1 (x) Average tree girth (cm) -0.78 60.84 <0.001

Axis 2 (y) Average tree girth (cm) -0.67 44.89 <0.001

Axis 1 (x) Fallen Trees -0.53 28.09 <0.001

Axis 2 (y) Fallen Trees -0.58 33.64 <0.001

Axis 1 (x) Gradient of slope -0.35 12.25 0.007

Axis 2 (y) Gradient of slope -0.33 10.89 0.013

Axis 1 (x) Width of path (cm) -0.76 57.76 <0.001

Axis 2 (y) Width of path (cm) -0.59 34.81 <0.001

Axis 1 (x) Numbers of palms >5m -0.69 47.61 <0.001 (rank) Axis 2 (y) Numbers of palms > 5m -0.73 53.29 <0.001 (rank) Axis 1 (x) Volume of Active Termitaria 0.35 12.25 <0.001 (l) Axis 2 (y) Volume of Active Termitaria 0.35 12.25 <0.001 (l) Axis 1 (x) Volume of Inactive 0.63 39.69 <0.001 Termitaria (l) Axis 1 (x) No. Suitable Active 0.63 39.69 <0.001 Termitaria Axis 1 (x) No. Suitable Inactive 0.60 36.00 <0.001 Termitaria Appendix D. Table 2 Continued.

s 2 Factor 1 Factor 2 r Rs P Axis 1 (x) Height of Suitable Active 0.56 31.36 <0.001 Termitaria (cm)

81 Axis 1 (x) Height of Suitable 0.63 39.69 <0.001 Inactive Termitaria (cm) Axis 1 (x) No. of Species Fruit -0.42 17.64 0.001

Axis 2 (y) No. of Species Fruit -0.33 10.89 0.01

Axis 1 (x) No. of Species Flowers -0.38 14.44 <0.001

Axis 2 (y) No. of Species Flowers -0.47 22.09 <0.001

Acknowledgements

Thank you to Phil Wheater for the support, advice and time. All the people involved with the Las Piedras Biodiversity Station thank you for persevering. Thank you to Stuart Marsden and Alan Lee for their support during the field course. A special thank you to my parents and Georgina Ralston.