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.
1.2Western Lowland Amazon andthe Las Piedras Research Centre
Upper Western Amazonian forests may have the mostdiverse floral and faunal assemblages in the world. TheCocha Cashu site in ManuNational Park, Peru, has the world'slargest 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 surroundingIquitos, 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 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.
1.3Termites- evolution and sociality
The earliest evidence ofeusocial insects in the fossil record is of reproductive termites castes found at a lower cretaceous lithographic limestone site in Spain (Bartz 1979, Delclos and Martinell1995). 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 1994and 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 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 plantmaterial, 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). Estimatesare 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 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 eusocialwith 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 buildingarboreal 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 intoarboreal 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.
1.4Arboreal 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 anegligible 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 forests worldwide (Abe 1978, 1979; Leponce et al. 1997; Dejean et al. 2003; Goncalves et al. 2005).
1.5Cavity Nesting Birds
The structural complexity of tropical lowland forests provides birds with manynesting 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 (Warrenet 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 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 acommunity 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, Beissinger1996)and smaller nestling periods. This is due to the high competition for nests (Eberhard 2002).
1.6Termitaria 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 oftenbased 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 (Brotogeriscyanoptera) parakeets have been published by Brightsmith (2000 and 2004). The Micronesian kingfisher(Todiramphus cinnamominus reichenbachii) has been thefocus 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 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 (Forpuspasserinus passerinus)has also been documented nesting in termitaria cavities (Belcher and Smooker 1936, Friedman and Smith 1950,) although neither studyalludes 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) andJuniper and Parr (1998) describe their observationsin 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. InJullien & 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 (Marmosacanescens), 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.
Adegree of commonness in arboreal nesting may exist that has yetto 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.
1.7Habitat 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 andsize of termitaria. Habitat will also influence avian presencein termitaria due to the specific dimensions all cavity nesting birds require (>9 litres in volume and > 5metres in height) (Brightsmith 2000, 2004). Threat from predation is a factor that will influence the height at which termitaria are built. This defensive strategyis limited primarily by resource availability and therefore habitat.
Termites that build arboreal nestsrequire 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.
1.8Flood Plain (FP) and TerraFirmeForests (TF)
The lowland tropical forests of Amazonia resemble ahomogenous-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 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, Pitmannet 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) influencestree species diversity and the structure of the FP forests (Junk et al. 1989b), resulting in a clearzonation 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.