Termite (Insecta, Isoptera) assemblage of a gallery forest relic from the Chaco province (Argentina): taxonomic and functional groups

Abstract

Termite (Insecta, Isoptera) assemblage of a gallery forest relic from the Chaco province (Argentina): taxonomic and functional groups
Termite fauna of the gallery forest in the Colonia Benitez Reserve (Chaco province, Argentina) were analyzed using the rapid diversity assessment protocol (100 x 2 m transects). Twelve species, 10 genera and two families (Kalotermitidae and Termitidae), were detected, comprising the four feeding groups recognized for termites. True soil–feeders (IV) showed the highest species richness, and dead wood and grasses feeders (II) had the highest relative abundance. The most frequently occupied microhabitats were dead wood pieces lying on the ground. These results indicate that the Reserve harbors a diverse termite community similar to the ‘monte fuerte’ isopteran fauna (91.6% shared species). Our findings also support the Reserve´s value as a well–preserved fragment of the original gallery forest and emphasize the need to promote its conservation.

Key words: Termite community, Neotropical region, Feeding groups

Resumen

Comunidad de termitas (Insecta, Isoptera) de un relicto de selva en galería de la provincia de Chaco (Argentina): grupos taxonómicos y funcionales
Se analizó la termitofauna de la selva en galería en la Reserva Colonia Benítez (provincia del Chaco, Argentina) mediante el protocolo de estimación de la diversidad de isópteros (transectos de 100 x 2 m). Se detectaron 12 especies incluidas en 10 géneros y dos familias (Kalotermitidae y Termitidae), pertenecientes a los cuatro grupos alimentarios de termitas con mayor riqueza de las alimentadoras de suelo (IV) y mayor abundancia relativa de las alimentadoras de madera muerta y hierbas (II). Los microhábitats más frecuentes fueron piezas de madera muerta húmeda depositadas sobre el suelo. Los resultados indicaron que la Reserva alberga una comunidad taxonómica y funcionalmente diversa de termitas, similar a la del “monte fuerte” (91,6% de especies comunes). Además, apoyan el valor del área como un fragmento bien preservado de la selva en galería original y enfatizan la necesidad de promover su conservación.

Palabras clave: Comunidad de termitas, Región Neotropical, Grupos tróficos

Resum

Comunitat de tèrmits (Insecta, Isoptera) d’un relicte de selva en galeria del Chaco (Argentina): grups taxonòmics i funcionals
Es va analitzar la termitofauna de la selva en galeria de la Reserva Colonia Benítez (província del Chaco, Argentina) mitjançant el protocol d’estimació de la diversitat d’isòpters (transsectes de 100 x 2 m). Es van detetcar 12 espècies incloses en 10 gèneres i dues famílies (Kalotermitidae i Termitidae) pertanyents als quatre grups de tèrmits establerts en funció de l’alimentació, amb més riquesa dels que s’alimenten a partir del sòl (IV) i més abundància relativa dels que s’alimenten de fusta morta i herbes (II). Els microhàbitats més freqüents van ser peces de fusta morta humida dipositades sobre el sòl. Els resultats van indicar que la Reserva acull una comunitat taxonòmica i funcionalment diversa de tèrmits, similar a la del “monte fuerte” (91,6% d’espècies comunes). A més a més, confirmen el valor de l’àrea com a fragment ben preservat de la selva en galeria original i la necessitat de promoure’n la conservació.

Paraules clau: Comunitat de tèrmits, Regió neotropical, Grups tròfics

Introduction

Termites are involved in plant material degradation processes and play an important ecological role as ‘ecosystem engineers’. The type of food consumed by each species varies from living plants to organic matter within mineral soil (Wood & Sands, 1978; Bignell & Eggleton, 2000; Eggleton & Tayasu, 2001; Bignell, 2006). Besides decomposition, the ecosystem services provided by termites include carbon and nitrogen cycling, modification of physical and chemical soil properties, and microbial diversity enhancement (Lobry de Bruyn & Conacher, 1990; Ackerman et al., 2007; Jouquet et al., 2011).

In addition, these insects are considered good indicators of environmental perturbations because of the changes seen in the composition and structure of their assemblages due to habitat fragmentation and agricultural land use (DeSouza & Brown, 1994; Davies et al., 1999, 2003; Barros et al., 2002; Davies, 2002; Eggleton et al., 2002; Sena et al., 2003; Roisin & Leponce, 2004; Attignon et al., 2005). Analysis of their communities can thus provide clues about the conservation status of fragmented natural areas, such as that in the Chaco Reserve analyzed in this study.

It is therefore interesting to characterize the Isoptera fauna from diverse environments and determine the processes in which they participate (Dawes–Gromadzki, 2008). This is especially significant in South American subtropical and semi–arid biomes where such surveys are still scarce. Only a few studies have been conducted to date in Argentina (Domingos et al., 1986; Martius et al., 1999; Laffont et al., 2004; Roisin & Leponce, 2004; Constantino, 2005; Torales et al., 2007; Vasconcellos et al., 2010; Jones & Eggleton, 2011; Palin et al., 2011).

With regard to ecosystems in protected areas of Eastern Chaco, previous termite surveys correspond to xerophytic forests in Chaco and Pilcomayo National Parks and the Pampa del Indio Reserve (Laffont et al., 2004; Roisin & Leponce, 2004; Torales et al., 2007, 2009), but the termite fauna from the Colonia Benitez Reserve (Chaco province) are unknown.

The aim of this study was to analyze the Isoptera assemblage in the Colonia Benitez Strict Nature Reserve and determine the taxonomic and functional group composition in order to help evaluate its conservation status.

Material and methods

Study site

The Colonia Benitez Strict Nature (27º 19′ 10” S, 58º 57′ 09” W, 10 ha) is situated in the Chaco province (NE Argentina), about 20 km N from Resistencia city. It is managed by the National Parks (APN, 2013).

The Reserve has a humid mesothermal climate with little winter rainfall, and the average annual temperature is above 18ºC. Phytogeographically, the area belongs to the Eastern District of the Humid Chaco, characterized by grasslands, floating islands (‘embalsados’), gallery forests and xerophytic forests (‘monte fuerte’) (Cabrera, 1976; Cabrera & Willink, 1980).

Although the Reserve is situated in the area with the highest population density of the Chaco province (Argentina), it has retained samples of the natural environments of the Chaco biogeographical region. This Reserve is considered to be of high biological and educational value despite its small size (Chébez et al., 1998, 2005; Soria, 2000; INTA, 2013). While its ecosystems are apparently little altered, the area shows signs of isolation because it is surrounded by environments mostly dedicated to farming. The flora has been extensively surveyed, but with respect to wildlife, its small size prevents the development of large vertebrate populations (Heinonen Fortabat & Chébez, 1997; Chébez et al., 1998, 2005; Soria, 2000). Only a few groups of invertebrate fauna have been surveyed (Gomez Lutz & Godoy, 2010; Lazzeri et al., 2011).

The study was conducted in one of the physiognomic units of the Reserve, a gallery forest relict (3 ha) with large arboreal vegetation on an old bank of the Negro river. The upper stratum of the gallery forest is formed by trees such as Peltophorum dubium, Enterolobium contortisiliquum, Tabebuia heptaphylla, Tabebuia pulcherrima, and Astronium balansae.

Sampling protocol

We used the standardized protocol for rapid assessment of termite diversity (Jones & Eggleton, 2000). This consisted of 100 x 2 m transects, divided into 20 successive sections of 5 x 2 m. Each section was intensively searched for one man–hour period. The search included all microhabitats (trees, shrubs, stumps, branches, fallen logs, grasses, and herbaceous vegetation), as well as litter and the underlying humus layer. At each section, five randomly distributed excavations (12 x 12 x 10 cm) were also performed to detect termites in the upper soil layers. Epigeal and arboreal nests up to a height of 2 m were measured and dissected. ​​Complementary sampling was made around transects.

Two transects (T1 and T2) were conducted at the gallery forest during the warm season (spring–summer) 2010–2011. This number of strips was due to the small size of the forest in the Reserve and the need to locate the strips 50 m away from the limits (to avoid border effects) and between them.

Sample identification and classification

Termite samples were identified to species or morphospecies level with the help of identification keys and specialized literature (Mathews, 1977; Fontes, 1985, 1992; Constantino, 1991, 1999, 2002, 2012). The specimens were compared with samples from previous studies conducted in the region (Laffont et al., 2004; Laffont et al., 2004, 2009).

The material (annex 1) was deposited in the Isoptera Collection of the Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Corrientes, Argentina (FACENAC).

Annex 1. List of collected samples of termites from Colonia Benitez Reserve with information on field and FACENAC numbers, collection (date, microhabitat, collector) and taxonomic determination. Anexo 1. Lista de muestras de termitas recolectadas en la Reserva Colonia Benitez, con información de los números de registro de campo y FACENAC, datos de recolección (fecha, microhábitat, recolector) y determinación taxonómica.

Termites were also classified according to the ecological or functional groups proposed by Donovan et al. (2001) and Eggleton & Tayasu (2001). Six morphological characters were analyzed: shape of pronotum in side view, development of the molar plate ridges of the right mandible, number and attachment of the Malpighian tubules, development of enteric valve ridges, and ornamentation of the enteric valve wall between and beyond ridges (Godoy, in prep.).

Data analysis

The software Estimates 8.2.0 (Colwell, 2006) was used to determine α diversity through S (richness expressed as the number of species), to build the species accumulation curve, and to calculate the nonparametric estimators (first–order and second–order Jackknife).

The software Statistica (Statsoft, 1999) was used to assess the quality of sampling. The species accumulation curve was adjusted to the Clench function by nonlinear estimation with the Simplex & Quasi Newton algorithm. This function has proved a good fit for many situations and taxa (Jiménez–Valverde & Hortal, 2003).

All tests were performed with a significance α = 0.05. As usual for social insects, we considered the number of occurrences of each species (encounters) instead of the total number of individuals (Leponce et al., 2004).

Results

A total of 30 Isoptera encounters were recorded from the gallery forest. Thirty–one termite samples were obtained, four of which were composed of two species. The sections that were positive to termites were 30% (T1) and 80% (T2), respectively.

Twelve species (S = 12), representing 10 genera and two families, were identified (table 1). Termitidae was the dominant family both in species richness (83.3%) and relative abundance (90%), while Kalotermitidae was represented by only two species (fig. 1).

Table 1. Termites from Colonia Benitez Reserve: species list, number of encounters, feeding groups, microhabitats occupied and nesting habits. Tabla 1. Termitas de la Reserva Colonia Benítez: lista de especies, número de encuentros, grupos establecidos según su alimentación, microhábitats ocupados y tipos de nidos.

Fig. 1. Taxonomic groups of the termite assemblage: richness and relative abundance based on number of encounters. Fig. 1. Grupos taxonómicos de la comunidad de termitas: riqueza y abundancia relativa según el número de encuentros.

Within Termitidae, Apicotermitinae was the most species–rich subfamily with four species, but Nasutitermitinae dominated the community, representing 46.6% of encounters. The most common termite species were Diversitermes diversimiles with seven encounters, and Nasutitermes nordesnkioeldi with six.

The estimated species richness ​​(Jackknife 1 and 2) were 17.8 and 21.7, respectively (fig. 2), indicating that the sampling effort allowed capture of between 55 and 67% of the gallery forest species. Moreover, the species accumulation curve fitted the Clench function (fig. 3) with R2 = 0.999; the value of the curve slope was 0.12, and the asymptote (estimated species) was 19.8, with an estimated capture success of 60%.

Fig. 2. Termite species richness: observed and estimated by first–order and second–order Jackknife.
Fig. 2. Riqueza de especies de termitas observada y estimadas mediante Jackknife de primer y segundo orden.

Fig. 3. Termite species accumulation curves: observed and prediction of the Clench model.
Fig. 3. Curva de acumulación de especies de termitas: observadas y predicción mediante el modelo de Clench.

The termite assemblage comprised the four feeding groups recognized by Donovan et al. (2001) for termites (fig. 4). The true soil–feeders (group IV) showed the highest species richness (five), comprising the soldierless Apicotermitinae and Dihoplotermes inusitatus that consume ligno–cellulose substrates in an extremely amorphous and refractory form. Nevertheless, the litter– and wood– feeders Termitidae (group II) had the highest relative abundance (60% of the encounters), comprising the Nasutitermitinae species and Microcerotermes strunckii, feeding mainly on dead wood. No–Termitidae wood–feeders (group I) were recorded: Tauritermes triceromegas and Rugitermes rugosus. Only one species that consumes the organic–rich upper layers of the soil (group III) was recorded (Neocapritermes opacus).

Fig. 4. Feeding groups (I–IV) of the termite assemblage: richness and relative abundance based on number of encounters. (For the abbreviations of feeding groups see Results.)
Fig. 4. Grupos tróficos (I–IV) de la comunidad de termitas: riqueza y abundancia relativa según el número de encuentros. (Para las abreviaturas de los grupos tróficos, ver Resultados.)

The microhabitats most frequently occupied by termites (50% of the encounters) were pieces of dead wood (fallen branches and trunks), generally with high humidity content, lying on the ground of the gallery forest (fig. 5). We verified a close relationship between the colonized microhabitats and the nesting and feeding habits of each species. Thus, the wood–nesting and xylophagous kalotermitids were found inside galleries excavated in fallen trunks and branches. The three species with arboreal nests and wood–eating habits (feeding group II) (Nasutitermes aquilinus, N. nordenskioeldi and M. strunckii) were detected inside their nests and covered runways on living and dead trees. Arboreal nests of N. aquilinus (two) and M. strunckii (one) were detected in the surroundings of the strips, built on living trees.

Fig. 5. Microhabitats occupied by termites in the Reserve, as a proportion of total termite encounters. (For abbreviations of microhabitats see table 1.)
Fig. 5. Microhábitats ocupados por termitas en la Reserva, en proporción al número total de encuentros. (Para las abreviaturas de los microhábitats, ver tabla 1.)

The other species, with hypogeal nests or frequent inhabitants of other Termitidae nests (inquilines), were detected in highly degraded pieces of dead wood, such as hollow branches filled with mineral soil (D. diversimiles, Grigiotermes sp. a and D. inusitatus), or inside the soil (N. opacus and the remaining Apicotermitinae).

Discussion

The current study is the first systematic survey of termites in a gallery forest relict of the Humid Chaco. Previous studies have been performed in semideciduous xerophytic forests (‘quebrachal’ or ‘monte fuerte’) (Laffont et al., 2004; Roisin & Leponce, 2004; Torales et al., 2007). Despite the floristic differences between gallery forests and ‘monte fuerte’, the termite fauna showed high similarity, with 11 (91.6%) shared species. The morphospecies Grigiotermes sp. b, previously detected at the Paranaense biogeographical region (Torales et al., 2005) is reported for the first time from Chaco. This record increases the number of termite species within this region to 79 (Torales et al., 2009).

These results indicate that the Colonia Benitez Reserve harbors a taxonomically and functionally diverse subsample of termites, having 18.7% of the 64 species previously reported for the Humid Chaco District (Torales et al., 2009). The presence of soil–feeding termites, which contribute to soil fertility and appear to be more affected by anthropogenic disturbances in humid forests, is particularly significant (Eggleton et al., 1995, 1996, 2002; Davies et al., 2003; Jones et al., 2003; Hemachandra et al., 2010). The diversity and abundance of this feeding group in Colonia Benitez provides evidence that the Isoptera assemblage was not severely affected by these processes.

In addition to soil feeding, other termite activities such as litter and dead wood consumption and decomposition, nest building and tunneling on vegetation were recorded in the area. The participation of these insects in diverse processes in the Reserve contributes to the provision of essential ecosystem services such as organic matter decomposition and recycling (Jouquet et al., 2011).

Besides the need to increase the sampling effort, the lower number of species collected may be because only one physiognomic unit of the Reserve was analyzed or because the area of the Reserve was small. In fact, termite communities, like those of other insects such as ants and crickets, are reported to have lower species richness in smaller forests remnants than in large undisturbed areas. This is mainly due to mechanisms of deterioration that act in isolated fragments, such as restriction of population size and immigration, deforestation —related disturbance and edge effects (De Souza & Brown, 1994; Turner & Corlett, 1996; Davies, 2002; Ribas et al., 2005; Nichols et al., 2007).

Several studies, however, have confirmed the value of small fragments of undisturbed or partially altered environments such as habitats for a significant number of plant, invertebrate and small vertebrate species whose populations can persist for long periods of time (Shafer, 1995; Oertli et al., 2002; Miller & Hobbs, 2002).

Our results support the importance of the Colonia Benitez Reserve as a well–preserved fragment of the original gallery forest and also emphasize the need to promote conservation of this area and similar small fragments of the Chacoan Region due to their natural and educational value. Additional studies of other plant and animal groups should be performed to enable accurate evaluation of the regions conservation status and implement effective management and protection strategies.

Acknowledgements

We would like to thank the National Park Administration (APN, Argentina) for permission to conduct research at the Colonia Benitez Reserve, and park wardens Andrés Lanfiutti and Claudio Oneto for their support during field work. We also thank Tiago F. Carrijo, an anonymous referee, and Arxius de Miscel·lània Zoològica editor Francesc Uribe for constructive comments on the manuscript. Funding was provided by the Secretaria General de Ciencia y Técnica (Universidad Nacional del Nordeste).

References

Ackerman, I. L., Teixeira, W. G., Riha, S. J., Lehmann, J. & Fernandes, E. C. M., 2007. The impact of mound–building termites on surface soil properties in a secondary forest of Central Amazonia. Applied Soil Ecology, 37: 267–276.

APN (Administración de Parques Nacionales), 2013. RE Colonia Benitez. http://www.parquesnacionales.gov.ar/_OLD/03_ap/08_cbenitez_RNE/08_cbenitez_RNE.htm [22th February 2013].

Attignon, S., Lachat, T., Sinsin, B., Nagel, P. & Peveling, R., 2005. Termite assemblages in a West–African semi–deciduous forest and teak plantations. Agriculture, Ecosystems and Environment, 110: 318–326.

Barros, E., Pashanasi, B., Constantino, R. & Lavelle, P., 2002. Effects of land–use system on the soil macrofauna in western Brazilian Amazonia. Biology and Fertility of Soils, 35: 338–377.

Bignell, D. E., 2006. Termites as Soil Engineers and Soil Processors. In: Intestinal Microorganisms of Termites and Other Invertebrates: 183–220 (H. König & A. Varma, Eds.). Springer, Berlin.

Bignell, D. E. & Eggleton, P., 2000. Termites in ecosystems. In: Termites: Evolution, Sociality, Symbioses, Ecology: 363–388 (T. Abe, D. Bignell & M. Higashi, Eds.). Kluwer Academic Publishers, The Netherlands.

Cabrera, A., 1976. Regiones fitogeográficas argentinas. In: Enciclopedia argentina de agricultura y jardinería II: 1–85 (W. Kugler, Ed.). Acme, Buenos Aires.

Cabrera, A. & Willink, A., 1980. Biogeografía de América Latina. OEA, Washington.

Chébez, J. C., Rey, N. R., Babarskas, M. & Di Giacomo, A. G., 1998. Las Aves de los Parques Nacionales de la Argentina. LOLA, Buenos Aires.

Chébez, J. C., Rey, N. R. & Williams, J. D., 2005. Reptiles de los Parques Nacionales de Argentina. LOLA, Buenos Aires.

Colwell, R. K., 2006. EstimateS: Statistical estimation of species richness and shared species from samples. 8.2.0. User’s Guide and application [on line]. <http://purl.oclc.org/estimates> [15th March 2012].

Constantino, R., 1991. Notes on Neocapritermes Holmgren, with description of two new species from the Amazon basin (Isoptera, Termitidae). Goeldiana Zoologia, 7: 1–13.

–    1999. Chave ilustrada para a identificação dos géneros de cupins (Insecta: Isoptera) que ocorrem no Brasil. Papéis Avulsos de Zoología, 40(25): 387–448.

–    2002. An illustrated key to Neotropical termite genera (Insecta: Isoptera) based primarily on soldiers. Zootaxa, 67: 1–40.

–    2005. Padrões de diversidade e endemismo de térmitas no bioma cerrado. In: Biodiversidade, Ecologia e Conservação do Cerrado: 319–333 (A. O. Scariot, J. C. Silva & J. M. Felfili, Eds.). Ministério do Meio Ambiente, Brasilia.

–    2012. Online Termite Database. <http://www.unb.br/ib/zoo/catalog.html> [25th May 2012].

Davies, R. G., 2002. Feeding group responses of a Neotropical termite assemblage to rain forest fragmentation. Oecologia, 133: 233–242.

Davies, R. G., Eggleton, P., Dibog, L., Lawton, J. H., Bignell, D. E., Brauman, A., Hartmann, C., Nunes, L., Holt, J. & Rouland, C., 1999. Successional response of a tropical forest termite assemblage to experimental habitat perturbation. Journal of Applied Ecology, 36: 946–962.

Davies, R. G., Hernández, L. M., Eggleton, P., Didham, R. K., Fagan, L. L. & Winchester, N. N., 2003. Environmental and spatial influences upon species composition of a termite assemblage across neotropical forest islands. Journal of Tropical Ecology, 19: 509–524.

Dawes–Gromadzki, T. Z., 2008. Abundance and diversity of termites in a savanna woodland reserve in tropical Australia. Australian Journal of Entomology, 47: 307–314.

De Souza, O. F. & Brown, V. K., 1994. Effects of habitat fragmentation on Amazonian termite communities. Journal of Tropical Ecology, 10: 197–206.

Domingos, D. J., Cavenaghi, T. M., Gontijo, T. A., Drumond, M. A. & Carvalho, R. C., 1986. Composicão em espécies, densidade e aspectos biológicos da fauna de térmitas de cerrado em Sete Lagoas–M. G. Ciencia e Cultura, 38(1): 199–207.

Donovan, S., Eggleton, P. & Bignell, D., 2001. Gut content analysis and a new feeding group classification of termites. Ecological Entomology, 26: 356–366.

Eggleton, P., Bignell, D. E., Sands, W. A., Mawdsley, N. A., Lawton, J. H., Wood, T. G., Bignell, N. C., 1996. The diversity, abundance and biomass of termites under differing levels of disturbance in the Mbalmayo Forest Reserve, Southern Cameroon. Philosophical Transactions of the Royal Society B: Biological Sciences London B, 351: 51–68.

Eggleton, P., Bignell, D. E., Sands, W. A., Waite, B., Wood, T. G. & Lawton, J. H., 1995. The diversity of termites (Isoptera) under differing levels of forest disturbance in the Mbalmayo Forest Reserve, Southern Cameroon. Journal of Tropical Ecology, 11: 85–98.

Eggleton, P., Bignell, D. E., Hauser, S., Dibog, L., Norgrove, L. & Madong, B., 2002. Termite diversity across an anthropogenic disturbance gradient in the humid forest zone of West Africa. Agriculture, Ecosystems and Environment, 90: 189–202.

Eggleton, P. & Tayasu, I., 2001. Feeding groups, lifetypes and the global ecology of termites. Ecological Research, 16 (5): 941–960.

Fontes, L. R., 1985. Potentialities of the appearance of the worker gut in situ for the identification of neotropical genera of Apicotermitinae (Isoptera, Termitidae). Annals of the Entomological Society of America, 3(2): 1–6.

–    1992. Key to the genera of New World Apicotermitinae (Isoptera, Termitidae). In: Insects of Panama and Mesoamerica: 242–248 (D. A. Quintero & A. Aiello, Eds.). Oxford University Press, New York.

Gomez Lutz, M. & Godoy, M. C., 2010. Diversidad y grupos funcionales de Formicidae (Insecta, Hymenoptera) de la Reserva Natural Educativa Colonia Benitez (Provincia del Chaco, Argentina). FABICIB, 14: 180–195.

Heinonen Fortabat, S. & Chébez, J. C., 1997. Los Mamíferos de los Parques Nacionales de la Argentina. LOLA, Buenos Aires.

Hemachandra, I. I., Edirisinghe, J. P., Karunaratne, W. A. & Gunatilleke, C. V., 2010. Distinctiveness of termite assemblages in two fragmented forest types in Hantane Hills in the Kandy District of Sri Lanka. Ceylon Journal of Science (Biological Sciences), 39(1): 11–19.

INTA Colonia Benitez, 2013. Reserva Natural Educativa Colonia Benitez. <http://www.inta.gov.ar/benitez/info/reserva/reserva.htm> [20th February 2013].

Jiménez–Valverde, A. & Hortal, J., 2003. Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Revista Ibérica de Aracnología, 8: 151–161.

Jones, D. & Eggleton, P., 2000. Sampling termite assemblages in tropical forest: testing a rapid biodiversity assessment protocol. Journal of Applied Ecology, 37: 191–203.

–    2011. Global biogeography of termites: a compilation of sources. In: Biology of Termites: A Modern Synthesis: 477–498 (D. E. Bignell, Y. Roisin & N. Lo, Eds). Springer, Dordrecht.

Jones, D., Susilo, F. X., Bignell, D. E., Hardiwinoto, S., Gillison, A. N. & Eggleton, P., 2003. Termite assemblage collapse along a land–use intensification gradient in lowland central Sumatra, Indonesia. Journal of Applied Ecology, 40: 380–391.

Jouquet, P., Traoré, S., Choosai, C., Hartmann, C. & Bignell, D. E., 2011. Influence of termites on ecosystem functioning. Ecosystem services provided by termites. European Journal of Soil Biology, 47: 215–222.

Laffont, E. R., Torales, G.J., Coronel, J. M., Arbino, M. O. & Godoy, M. C., 2004. Termite (Insecta, Isoptera) Fauna from National Parks of the Northeast Region of Argentina. Scientia Agricola, 61(6): 665–670.

Lazzeri, M. G., Núñez–Bustos, E. & Damborsky, M. P., 2011. Nuevos registros de Archaeoprepona demophon thalpius (Hübner, 1814) en las provincias de Corrientes y Chaco, Argentina (Lepidoptera: Nymphalidae, Charaxinae, Preponini). SHILAP Revta. lepid., 39(156): 1–5.

Leponce, M., Theunis, L., Delabie, J. & Roisin, Y., 2004. Scale dependence of diversity measures in a leaf–litter ant assemblage. Ecography, 27: 253–267.

Lobry de Bruyn, L. & Conacher, A. J., 1990. The role of termites and ants in soil modification: a review. Australian Journal of Soil Research, 28: 55–93.

Martius, C., Tabosa, W. A., Bandeira, A. G. & Amelung, W., 1999. Richness of termite genera in a Semi–Arid Region (Sertão) in NE Brazil (Isoptera). Sociobiology, 33 (3): 357–365.

Mathews, A. G., 1977. Studies on termites from Mato Grosso State, Brazil. Academia Brasileira de Ciencias, Rio de Janeiro.

Miller, J. R. & Hobbs, R. J., 2002. Conservation where people live and work. Conservation Biology, 16(2): 330–337.

Nichols, E., Larsen, T., Spector, S., Davis, A. L., Escobar, F., Favila, M. & Vulinec, K., 2007. The Scarabaeinae research network. Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and metaanalysis. Biological Conservation, 137: 1–19.

Oertli, B., Joye, D. A., Castella, E., Juge, R., Cambin, D. & Lachavanne, J. B., 2002. Does size matter? The relationship between pond area and biodiversity. Biological Conservation, 104: 59–70.

Palin, O. F., Eggleton, P., Malhi, Y., Girardin, C. A. J., Rozas–Dávila, A. & Parr, C. L., 2011. Termite diversity along an Amazon–Andes elevation gradient, Peru. Biotropica, 43: 100–107.

Ribas, C. R., Sobrinho, T. G., Schoereder, J. H., Sperber, C. F., Lopes–Andrade, C. & Soares, S. M., 2005. How large is large enough for insects? Forest fragmentation effects at three spatial scales. Acta Oecologica, 27: 31–41.

Roisin, Y. & Leponce, M., 2004. Characterizing termite assemblages in fragmented forest: A test case in the Argentinian Chaco. Austral Ecology, 29: 637–646.

Sena, J. M., Vasconcellos, A., Gusmão, M. A. B. & Bandeira, A. G., 2003. Assemblage of termites in a fragment of cerrado on the coast of Paraiba State, northeast Brazil (Isoptera). Sociobiology, 42: 753–760.

Shafer, C. L., 1995. Value and shortcomings of small reserves. Bioscience, 45: 80–88.

Soria, A., 2000. Especies de valor especial de los parques nacionales chaqueños: guía para la identificación de vertebrados de registro prioritario. Administración de Parques Nacionales. Delegación Regional Nordeste Argentino, Puerto Iguazú.

StatSoft, Inc., 1999. STATISTICA for Windows <http://www.statsoft.com> [10th March 2012].

Torales, G. J., Coronel, J. M., Laffont, E. R., Godoy, M.C. & Fontana, J. L., 2007. Termite (Insecta, Isoptera) faunal composition in natural forests of the humid Chaco (Argentina). Sociobiology, 50(2): 419–433.

Torales, G. J., Coronel, J. M., Laffont, E. R., Fontana, J. L. & Godoy, M. C., 2009. Termite associations (Insecta, Isoptera) in natural or semi–natural plant communities from Argentina. Sociobiology, 54(2): 383–437.

Turner, I. M. & Corlett, R. T., 1996. The conservation value of small, isolated fragments of lowland tropical rain forest. Tree, 1(8): 330–333.

Vasconcellos, A., Bandeira, A. G., Moura, F. M., Araújo, V. F., Gusmão, M. A. B., Constantino, R., 2010. Termite assemblages in three habitats under different disturbance regimes in the semi–arid Caatinga of NE Brazil. Journal of Arid Environments, 74: 298–302.

Wood, T. G. & Sands, W. A., 1978. The role of termites in ecosystems. In: Production ecology of ants and termites: 245–292 (M. Brian, Ed.). Cambridge Univ. Press, London.