Termite diversity in the Abobral region of the Pantanal wetland complex, Brazil

This is the first termite survey using standard protocols in the Abobral region of the Pantanal complex of South America. Abobral, which is primarily composed of four physiognomies: 1) campo , annually flooded grassland; 2) capao , which are islands of semi-deciduous forests; 3) carandazal , annually flooded vegetation composed of a native palm; and 4) paratudal , annually flooded savanna vegetation. Ten species of termites were sampled in the capoes , three in the grasslands, two in the paratudal  and no species in the carandazal . The diversity of termites in the Abobral Pantanal is concentrated in the capoes , which stay above water level during the flood season. In the others physiognomies of the Abobral, the termite fauna is poor. The species composition of termites of the Abobral Pantanal seems to be more related to the Cerrado and Chaco faunas than to the Amazonia and Atlantic Forest faunas.


INTRODUCTION
Termites are social insects that are classified as ecosystem engineers due to the important role they play in ecosystems, such as contributing to the organic matter decomposition, soil formation and aeration, carbon and nitrogen biogeochemical cycles, and nutrient cycling (Jones et al. 1994;Higashi and Abe 1997;Lavelle et al. 1997). These insects are among the most abundant arthropods of tropical soil ecosystems (Black and Okwakol 1997;Davies et al. 1999;Jouquet et al. 2011) and represent 10% of the animal biomass in the tropics (Bignell 2006).
The Pantanal is a seasonally flooded complex in the center of South America, and its fauna and flora are influenced by all of the nearby phytogeographic regions: Amazon Forest, Cerrado, Chaco and Atlantic Forest (Alho 2005). The flood dynamics are linked to the rain season, which normally occurs from October to March (Cadavid-Garcia 1984), and to the plain's regional topography (Alvarenga et al. 1984). Almost 60% of the soils in the Pantanal are hydromorphic, with low drainage and a tendency for flooding and with discontinuous portions of clay and sand (Orioli et al. 1982).
The Pantanal complex is normally subdivided into 11 regions according to the relief and flood pattern (Silva and Abdon 1998;Alho 2005). The Abobral region is composed of different physiognomies, mostly periodically flooded grasslands (native pastures for cattle), with highlands or capões (the plural of capão), which are islands of semi-deciduous forest that remain above water level during the flood season (Allem and Valls 1987). The flooded grasslands are one of the first regions to flood during the rainy season and are composed of the floodplains that are common to the Abobral, Miranda and Negro Rivers (Cunha et al. 1986). The termite fauna of the Pantanal is poorly known , and the few studies published (e.g. Polatto and Alves Jr. 2009;Plaza et al. 2014) do not use standard protocols for comparisons with adjacent environments such as the Cerrado, Chaco or Amazonia. However, these studies did not have the principal objective of evaluating termite richness. The aims of this study were to compare the termite fauna from different physiognomies in the Abobral region of the Pantanal complex, to provide a first check list for the species of this singular environment. The study areas were characterized based on the physical-chemical properties of the soil.

Study site
This study was conducted in the Abobral region of the Pantanal complex, west of Mato Grosso do Sul, Brazil ( Figure 1). The weather is tropical sub-humid Aw, with 1,100 mm of annual precipitation and an average temperature of 26°C (Cadavid-Garcia 1984). The following physiognomies can be found in the Abobral region ( Figure 1): (a) "Campo", flooded grasslands, lowland areas with grass and sedges; (b) "Capões", also called mounds and "murundus", are islands between grasslands with semi-deciduous forests and 8-20 m high canopies, that stay above water level during the flood season; (c) "Carandazal" formations with native palms ("carandá", Copernicia alba Morong.) that are 8-20 m high in periodically flooded areas; and (d) "Paratudal", savanna formations in flooded areas near rivers with a dominance of the "paratudo" tree (Tabebuia aurea (Manso) B. & H.) and 5-16 m high canopies. The sampling was performed in five areas of four physiognomies: A1 (Campo) (19°30′39″ S, 057°02′32″ W); A2 (Carandazal) (19°15′15″ S, MS. Soil samples were analyzed to determine pH in CaCl 2 , organic matter content, available P by the Mehlich-1 method, exchangeable Al, H, K, Ca and Mg, exchangeable acidity and fraction of sand, clay and silt. With the above parameters, was possible to infer, the sum of bases (sum of Ca, Mg e K), base saturation (CEC proportion that is occupied by bases) and cation exchange capacity (the quantity of cations-Al, H, Ca, Mg e K-remain in the soil) at pH 7.0.

Data Analysis
The sampling effort was evaluated using a species accumulation curve, constructed using the observed richness and number of samples for each study area. The termite richness was estimated by Jackknife, a nonparametric method that estimates the richness based on the incidence. The estimated richness is obtained by the sum of the observed richness and of the parameter calculated from the number of species that occurs in one (Jack1) or two (Jack2) samples (Magurran 2004). It is calculated using the software EstimateS version 7.0 (Colwell 2004), with 50 randomizations without replacement.

RESULTS
In the four physiognomies of the Abobral region, 13 species of termites belonging to the following families and subfamilies were sampled: Rhinotermitidae (1); Termitidae, Apicotermitinae (4), Nasutitermitinae (3), Syntermitinae (3) and Termitinae (2) ( Table 1). The total observed richness (13 ± 1.36) corresponded to 82% of the expected richness predicted by the Jackknife1 estimator (15.94 ± 1.66) and to 77% by the Jackknife2 estimator (16.94 ± 0.68) (Figure 2). The areas with higher species richness are: Capões (A4 and A5, with 10 species each), Campo (A1, 3 species) and Paratudal (A3, 2 species). No species were found in the Carandazal (A2), and from the total of 50 plots, 29 had no termites (Table 1). A high diversity and similarity of species were found in Capão: eight species in common between A4 and A5 and nine species unique to this physiognomy were sampled (see Table 1). The observed richness relative to the expected richness predicted by Jackknife2 estimator, corresponded to 37% to A1 and A3, 68% to A4 and 72% to A5 (Table 1). More than 50% of the species have underground nests, in the soil, and nearly the same percentage is xylophagous (Table 1).

Termite sampling
The sampling was performed in July 2012. In each area, the termites were sampled during 1 hour/collector in 10 plots of 5 × 2 m, 10 m distant from each other. Termites were sought in all possible places inside the plots, including in nests, galleries, wood, leaf litter, and soil and under cattle dung. Samples from all colonies were identified using the appropriate literature and/or comparison with the Termitological Collections of the Museu de Zoologia of the Universidade de São Paulo (MZUSP) and of the Laboratório de Pesquisa Ecológica e Educação Científica of the Universidade Estadual de Goiás (Lab-PEEC/UEG). The collections had Sisbio Authorization number 15976-1 (13/05/2008). Voucher specimens from 2987 to 3030 were deposited in the collection of Lab-PEEC/ UEG, Goiás, Brazil.
According to field observations and literature information (Mathews 1977;Gontijo and Domingos 1991;De Souza and Brown, 1994), the species were classified in four feeding groups: xylophagous (wood feeder species), humivorous (species that feed on humus and organic matter on soil), grass/ litter feeders (species that forage on surface and feed on litter and/ or grass), and intermediate (species that feed of organic matter in high decomposed state or do not fit within any of the other groups).

Soil sampling
In each of the five areas, one soil sample of 25 cm 2 and 30 cm in depth were collected, preserving the soil profile to ensure that the quantity of soil to be analyzed is the same both on the surface and 30 cm depth. At each point, the surface vegetation was removed as well as stones and other materials that would not be part of the analysis. The sampling sites were located away from nests, termite mounds, fences and carriers, in order to avoid: changes in the chemical and physical composition of soil caused by insect bioturbation; contamination by feces and urine of cattle over the carrier. Soil samples were labeled and sent for physical-chemical analysis to Laboratório de Análises de Solo e Consultoria Ltda. de Campo Grande, The physical and chemical parameters of soil for each study areas are presented in Table 2. The soil of the five areas has sandy texture with more than 70% sand. A2, A3, A4 and A5 have eutrophic soil, with more than 50% base saturation, indicates soils with high fertility. A1 have dystrophic soil, which indicates soils with medium fertility. A1, A3 and A4 have acidic soil, while A2 and A5 have alkaline soil. A5 has the highest CEC and content of organic matter, while A2 has the lowest CEC and content of organic matter. Comparing the two Capões, the soil of A5 has more organic matter than that of A4.

DISCUSSION
This is the first termite survey in the Abobral region of the Pantanal complex. The observed richness was equivalent to 77% of the total richness estimated for the entire region by the Jackknife2 estimator, the most conservative one. In each physiognomy, the observed richness was 40% to 70% of the estimated richness (see Table 1, except for the Carandazal, where no species were recorded). Whereas that were sampled 10 plots in each area, 70% of the total richness can be considered a relatively well sampled area. Other termite surveys had similar completeness using Jackknife estimator in other biomes, but with higher sampling efforts (e.g. Reis and Cancello 2007). Nasutitermes ephratae was the only species recorded in all four study physiognomies; this species is xylophagous and builds cartons nests, and has a wide distribution, going until to Panama, in Central America (Thorne 1980).
No species were found in the Carandazal, which is dominated by palm trees in hydromorphic soil, whose physicochemical analysis revealed eutrophic soil, alkaline pH, little organic matter and a low cation exchange capacity (CEC) (see Table  2). In Paratudal, only species that build arboreal nests were    found (Nasutitermes ephratae and Microcerotermes strunckii). The absence of termites that build nests in the ground or underground can be because this area is located on the banks of the Miranda River, and suffers frequent flooding, which results in a very acidic soil and a low organic matter content (see Table 2).
The Pantanal fauna is considered to be influenced by all surrounding biomes (Alho 2005); however, the termite fauna seems to be more related to the Cerrado and Chaco. Excluding the species of Nasutitermes and Microcerotermes, which have wide distributions and occur in many biomes, most of the species found in the Abobral region located in the Pantanal complex, can also be found in the Cerrado and Chaco. This is the case for the species Labiotermes laticephalus, Rhynchotermes nasutissimus and Procornitermes triacifer (Roisin and Leponce 2004;. Additionally, the species Heterotermes longiceps and Diversitermes diversimilis occur in the Cerrado and Chaco, but are also distributed across the Atlantic Forest region (Constantino 2000;Cancello et al. 2014).
Studying the inquiline fauna of Cornitermes silvestrii, Plaza et al. (2014) found a different termite fauna in the Pantanal region of Cáceres, north of the Pantanal complex. In the Abobral region, we did not find any epigeal nest, but in the Cáceres region we found three species that can build epigeal nest (C.

silvestrii, C. bequaerti and Silvestritermes euamignathus).
Based on the highest number of species in capões, we conclude that the diversity of termites in the Abobral Pantanal is concentrated in that physiognomy, which normally stay above the water level during the flood season. Additionally, the termite species composition of the Abobral Pantanal seems to be more related to the Cerrado and Chaco fauna, while different regions of the Pantanal have a completely different termite fauna. Similar studies should be performed in other regions of the Pantanal to forge a better understanding of the diversity pattern of the complex as a whole.