doi:10.12741/ebrasilis.v8i2.502 e-ISSN 1983-0572 Publicação do Projeto Entomologistas do Brasil www.ebras.bio.br Distribuído através da Creative Commons Licence v4.0 (BY-NC-ND) Copyright © EntomoBrasilis Copyright © do(s) Autor(es)
Termite Communities in Sugarcane Plantations in Southeastern Brazil: an Ecological Approach Luciane Kern Junqueira, Edmilson Ricardo Gonçalves & Lucas Manuel Cabral Teixeira
Pontifícia Universidade Católica de Campinas, e-mail: [email protected] (Autor para correspondência), [email protected], [email protected]. ______
EntomoBrasilis 8 (2): 105-116 (2015) Abstract. Termites are key components of soil fauna, playing an essential role in organic matter decomposition and nutrient cycling. However, they can cause significant economic losses in commercial plantations, such as sugar cane. Therefore, the correct identification of termite species is critical for pest control. Here, we evaluated the species richness, abundance and functional groups of termites in sugarcane plantations in 53 cities throughout the state of São Paulo, southeastern Brazil. We also analyzed the influence of macroclimatic variables on termite species distribution and functional groups. We found 22 taxa of two families, of which the most frequent species were Termitidae (96.51%). Within this family, Apicotermitinae had the highest frequency of occurrence (37.12%), followed by Termitinae (30.57%), Syntermitinae (27.95%), and Nasutitermitinae (0.8 %). The other family, Rhinotermitidae, had the lowest frequency (3.5%), being represented only by Heterotermes sulcatus Mathews. We classifiedNeocapritermes opacus Hagen (29.26%), Apicotermitinae sp.2 (24.89%), Cornitermes cumulans Kollar (13.10%), and Apicotermitinae sp.1 (6.99%) as common taxa. The remaining 18 species were classified as rare. The most common functional group was humus-feeders (37%), followed by wood-feeders (34%), grass- litter feeders (25%), and intermediate feeders (4%). Climate influenced the distribution of common species, humus-feeders and grass-litter feeders. Regarding the pest status of termites in sugar cane plantations, we suggest that the exasperated use of pesticide in the last decades has reduced the abundance of species considered pests (e.g. Heterotermes) and reinforce the importance of ecological approaches for determining the best pest control methods.
Keywords: Functional groups; Heterotermes sp.; Isoptera.
Comunidades de Cupins em Cultivos de Cana-de-Açúcar no Estado de São Paulo: Uma Abordagem Ecológica
Resumo. Os cupins são importantes componentes da fauna de solo, atuando na decomposição da matéria orgânica e ciclagem de nutrientes. Porém, em cultivos de cana-de-açúcar, podem provocar perdas econômicas significativas. A correta identificação das espécies de cupins é um ponto crítico para o controle daquelas que adquiriram e/ou que podem atingir o status de praga. Este trabalho objetivou identificar a riqueza, a abundância e os grupos funcionais destes insetos em canaviais de 53 municípios do estado de São Paulo. Paralelamente, avaliou se as variáveis macroclimáticas influenciam a distribuição das comunidades de cupins e dos grupos funcionais. A riqueza obtida foi de 22 táxons. Da família Termitidae (96,51%), a maior frequência Ecologia de ocorrência foi da subfamília Apicotermitinae (37,12%), seguindo-se Termitinae (30,57%), Syntermitinae (27,95%) e Nasutitermitinae (0,8%). A família Rhinotermitidae (3,5%) esteve representada apenas por Heterotermes sulcatus Mathews. Quatro táxons foram considerados comuns em canaviais, Neocapritermes opacus Hagen (29,26%), Apicotermitinae sp.2 (24,89%), Cornitermes cumulans Kollar (13,10%) e Apicotermitinae sp.1 (6,99%) e os 18 restantes foram classificados como raros. O grupo funcional mais frequente foi o dos humívoros (37%), seguido por xilófagos (34%), comedores de serrapilheira (25%) e intermediários (4%). O clima influenciou a distribuição das espécies comuns, bem como dos grupos funcionais dos humívoros e dos comedores de serrapilheira. Sugere-se que o uso intensivo de pesticidas nas últimas décadas reduziu a abundância de espécies até então consideradas praga em cana-de-açúcar (ex. Heterotermes), o que reforça a importância dos estudos ecológicos para a definição de métodos de controle mais adequados.
Palavras-chave: Grupos funcionais; Heterotermes sp.; Isoptera.
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ermite communities are usually species rich systems, population dynamics should be encouraged, to improve control with different feeding and nesting strategies. Termites agents, and species-specific management techniques (Mi r a n d a et are the main group involved in the intake and processing al. 2004). of organic and mineral matter (La v e ll e et al. 1997; Jo n e s 2000; Ga t h o r n e -Ha r d y et al. 2001), also playing a key role in the carbon On the other hand, xylophagous termites do not seem to be decomposition and mineralization, changing the soil structure influenced by agricultural practices (De So u z a & Br o w n 1994; (Bi g n e ll & Eggl e t o n 2000; Ac k e r m a n et al. 2007). Some species Eggl e t o n et al. 1997, 2002; Ba n d e i r a & Va s c o n c e ll o s 2002; Ba n d e i r a seem to be more sensitive to land use than others. For example, et al. 2003). Xylophagous are key components of the soil fauna geophagous are vulnerable to agricultural activities, which in native forests, playing an essential role in the decomposition reduces species richness and abundance of this group. The decline of organic matter, nutrient cycling, aeration, drainage, and the in geophagous species is often harmful to vegetation (Ba n d e i r a establishment of new soil in eroded areas (Co ll i n s 1981; Be r t i - & Va s c o n c e ll o s 2002; Ba n d e i r a et al. 2003). Geophagous Fi l h o 1995; Ju n q u e i r a et al. 2008). However, some species may are associated with the increase in nitrogen and phosphorus become pests in planted forests. For example, they are known release, drainage and aeration of the soil and humidification and to cause significant economic damages inEucalyptus plantations stabilization of organic matter (La v e ll e et al. 1997; Di b o g et al. (Wa r d e ll 1987; La ff o n t et al. 1998). More recently this group has 1999; Ju n q u e i r a et al. 2008). However, given the importance also been mentioned as pests in sugarcane plantations (Ba t i s t a - of termites in maintaining the fertility, aeration, and porosity of tropical soils, studies on their reproductive biology and Financial support: Pontifícia Universidade Católica de Campinas
www.periodico.ebras.bio.br 106 C and ethanol other products, such as animal food of and liters billion 25 about produced remainder the while industry, sugar the in used was this of Half tons. 612 million about producing 2010, and 2009 between sugarcane cultivated with were ha million 7.5 Around century. sixteenth early Sugarcane has been an economically important crop in Brazil since eotd 4 emt seis n uacn pattos n the in plantations while county, sugarcane the of part in southeastern species termite 14 reported arciai vrals eg, eprtr ad precipitation) and temperature (e.g., variables if if the macroclimatic tested we Finally, pests. literature potential are scientific species the common most in investigated also We southeastern Paulo, Brazil. São insugarcane of state the in oftermites cities 53 of species plantations rare and common define to distribution abundance species used and termites of species of Here, we identify the richness, abundance and functional groups in SãoPaulo,duetoitswidedistributionandhighabundance. considered in productivity( increase the to contributed that practices farming efficient more of adoption the promoting is crop this in interest The years. 30 use of sugarcane to produce biofuels increased globally in the past production (I production with 33% of world production, and India, concentring 23% of the Brazil, were 2007 in sugarcane producing countries top two The Figure 1.Distribution ofcitiesinthestateSãoPaulo inwhichtermitesweresampled insugarcaneplantations. P ih erdcie ilg ad ouain yais f several insect species (M of dynamics population and biology reproductive with might become pests, there is a growing body of literature dealing species some that concern the to Due forest. planted and crops sugarcane on termites of effect the in interest growing a is There ptnil et (M pest potential a nordestinus (Amitermes another while nordenskioeldi (Cylindrotermes damage causing was one only but Brazil northeastern northeastern in plantation sugarcane a in plantations genera Neocapritermes the sugarcane of incidence high in a with Brazil, pest major are & D diinly ohr tde (e.g., studies other Additionally, soil. the in matter organic of amount the and biomass root the by influenced mainly were species these of distribution spatial tgs f h cn (C cane the growth of different stages damage can which termites, subterranean of occurrence the favor factors Those soils. sandy and fertility low including Brazil, in area large a occupies plantation Sugarcane a r i e r e e v a e h Termite CommunitiesinSugarcanePlantationsin… h e i l g etal.2004). 2008,2010; i t t a Heterotermes tenuis Heterotermes -G n o t t o n a i f a m r o C . A previous study found four termite species in species termite four found study previous A . a d n a r i e v a e h a d n a r i E A etal. m a n a m r e k c s c i m o n o c
g et al. i t t a p s o
t al. et 2011).
-G 98. o eape termites example, For 1988). al. et 2004; o t t o n a i etal.2009). /FNP 04 ad h audne and abundance the and 2004) Hagen as the main pest species pest main the as Hagen J N a r i e u q n u etal.2011). S i t t e r a v o h t u o Mélo & Fontes) could be could Fontes) & Mélo A cachaça l a d i e m A
et al. 2008; and Heterotermes a c i r e m F & & (CONAB 2009; A s e t n o 2009). The 2009). Holmgren), l s e v (1999) M 1998) e z n e l
C 1998, 1999, 2001, 2002a, 2002b, 2014), 92 1995), 1992, ape trie y pnn to urw (,0 cm (2,500 burrows two opening by termite sampled Defining common and rare species. rare and common Defining feeders, andintermediatefeeders. grass-litter humus-feeders, wood-feeders, as groups functional and workers of intestinal contents. Thus, we morphology followed this classification to define jaw on based species Termitidae s rprd ih iig o a e patn (D planting new sugarcane a for the liming with soil of prepared the Then, is roots. end its with along the harvested, is after it when cycle, 2011 in occurred Sampling Technology, Piracicaba, Sugarcane São Paulo state) for (collection license SISBIO #12205-1). (Center Canavieira” Tecnologia de “Centro the by selected were Plantations Brazil. state, Paulo São the of 1) Appendix 1, (Figure cities 53 in plantations sugarcane identification. and Sampling cm depth) per hectare in sugarcane tussocks (following tussocks sugarcane in hectare per depth) cm R and vertebrate corpses). manure lichens, algae, fungi, on feed that (species groups xylophagous, leaf-litter dweelers, grass-eaters, and other feeding and geophages between intermediaries xylophagous, geophages, & n hc te uvtr cag. pce o te et ie were side left the on Species change. curvature thepoint the i.e., which curve, in rank abundance a in point inflection the al. et (1983), A including species, termite identify to keys and catalogs used We with 80%ethanol. glazing entomological in stored were termites Collected harvest. the after month one performed was sampling Each 1998). al. et species andfunctionalgroups. termite of distribution the influence distance geographical and (B defined based on species feeding guilds (M guilds feeding species on definition. based defined group Functional for LifeSciences,PontificalCatholicUniversityofCampinas. Collection of Isoptera, Department of Biological Sciences, Center the in housed are specimens collected The acknowledgements). (see specialists by confirmed was identification Species 2012b). 1997; o n i t n a t s n o ú a r e d n e z e D i g n i m o e n j (2012) to define common and rare species based on species rare and common define to (2012) o L L J (1977), s e n o R (2012) classified the feeding habits of South American South of habits feeding the classified (2012) & g a h c o s o E 1991; & B & L G G K & Material andethods C a n h s i r C n o t e C e c n a a v r a e d n e r e c n a D e 2000) defined functional groups as follows: as groups functional defined 2000) S L L l & o h L L L L a z u o o (1986, 1989), (1986, o 98 J 1998; (2011), A (2009), and (2009), ú a r & B & j o n w o r (1968), E s e n o n o s r e m 1994 e ape trie in termites sampled We
ucinl rus were groups Functional R 00. peiu study previous A 2000). C C a h c o o n i t n a t s n o o n i t n a t s n o e-ISSN 1983-0572 15) F (1952), M ; We followed We s w e h t a E s w e h t a
L G G et al. et Junqueira s a t n a n o t e 1977; G 1977; (2011, 2012a, (2011, (1977),
et al. s e t n o (1994, 1995, (1994,
01. We 2011). et al. et 2 ih 30 with A S (2006), et al. (1985, i r r a r i e u q i i t n o 1995, M g i n o i j L L o
Maio - Agosto 2015 - www.periodico.ebras.bio.br EntomoBrasilis 8 (2) defined as common and those on the right side as rare. This which 229 (92%) could be identified. Total species richness was is a straightforward visual method that uses untransformed 22 taxa (Table 1). The majority of the taxa (96.51%) belonged to abundances, stressing the real differences between common and Termitidae, with higher occurrence frequency of Apicotermitinae rare species. (37.12%) with four morphospecies, followed by Termitinae (30.57%) with the genera Neocapritermes and Cylindrotermes, Climatic data. We obtained the altitude and macroclimatic and Syntermitinae (27.95%) with the genera Cornitermes, variables (Appendix 2) from WorldClim (Hi j m a n s et al. 2005). As Syntermes, Embiratermes, Proconitermes, and Silvestritermes. they are highly correlated, we performed a Principal Component The lowest occurrences (0.87%) were recorded for the Analysis (PCA) to reduce the dimensionality. We used the broken Nasutitermitinae genera Parvitermes and Velocitermes. There stick model to select meaningful principal components (PC, was only one species of Rhinotermitidae (3.49%), Heterotermes Le g e n d r e & Le g e n d r e 2012), which resulted in the retention of sulcatus Mathews. two PCs that together explained 85% of the variation of the data. Then, we calculated the Euclidean distance between PC 1 and PC Our sampling method was efficient to collect species, since the 2 that will be entered in a Mantel test (see below). species accumulation curve tended to an asymptote (Figure 2). The species abundance distribution is best fitted by the Zipf- Data Analysis Mandelbrot model (Figure 3).
Spatial variables. We translated the matrix of site coordinates Common and rare species. We considered four taxa (latitude and longitude) into spatial predictors using distance- as common: Neocapritermes opacus Hagen (29.26%), based Moran Eigenvector Maps (dbMEM), formally called Apicotermitinae sp.2 (24.89%), Cornitermes cumulans Kollar Principal Coordinates of Neighbor Matrices (PCNM, Dr a y et (13.10%), and Apicotermitinae sp.1 (6.99%). The remaining 18 al. 2006, 2012). From a Euclidean pair-wise distance matrix taxa were considered rare (Figure 4). between sampled sites, we computed the threshold value and constructed a truncated distance matrix. This matrix kept Functional groups. The most frequent functional group was distances lower than the threshold unchanged and multiplied humus-feeder (37%), followed by wood-feeder (34%), grass- those higher by four times the threshold. We then performed a litter feeder (25%), and intermediate feeders (4%) (Table 1). Principal Coordinate Analysis (PCoA) on the truncated distance We mapped the occurrence frequency of the two most frequent matrix to obtain eigenvectors that were transformed to a distance groups by city, showing those that had a frequency of occurrence ≥ matrix to be used as spatial predictors in Mantel tests. 50% in each city (Figure 5, Appendix 3). Of the 53 cities sampled, 16 had predominant occurrence of humus-feeder species and 18 Rank-Dominance curves and species abundance distribution wood-feeder species. (SADs). We calculated a species accumulation curve (SAC) using the random method, which finds the mean SAC and its standard Climatic variables. We found a positive correlation between deviation from random permutations of the data (Go t e ll i & climate and species composition, independent on the geographic Co l w e ll 2001). We built a Species Abundance Distribution distance (r = 0.13, P <0.01, Figure 6). Additionally, climate (SAD) curve using Whittaker plots, by ranking species (from influenced the distribution of common (r = 0.11, P <0.01), but most to least abundant) in the x-axis and their raw abundances not rare species (r = 0.074, P = 0.089). in the y-axis. Several theoretical models have been suggested to fit observed SADs (reviewed in To k e s h i 1999; Ma g u r r a n 2004; We found a low and marginally significant correlation between McGi ll et al. 2007). Here, we used the following models: broken climate and functional group composition (r = 0.10, P = 0.079). stick, Motomura’s geometric series, lognormal, Zipf, and Zipf- However, the composition of humus-feeders (r = 0.277, P = 0.002) Mandelbrot. We used generalized linear (lognormal and Zipf) and grass-litter feeders (r = 0.158, P = 0.03) are correlated with and nonlinear models (Zipf-Mandelbrot and geometric series) the climate when tested separately, contrarily to wood-feeders (r along with the Akaike Information Criteria (AIC) to select the = 0.02, P = 0.395). theoretical model that best fitted the observed SAD (Wi l s o n 1991). Discussion
Partial Mantel test. To test if macroclimatic variables explain Termite occurrence in sugarcane plantations. We the variation in termite species composition, we used a partial found that the Apicotermitinae (37%) was the most frequent Mantel test, which tests the effect of macroclimatic variables subfamily of Termitidae, followed by Termitinae (30.57%), and (predictor) on species composition while controlling for the effect Syntermitinae (27.95%). The only species from another family of spatial variables. A partial Mantel test was used to control (Rhinotermitidae) was H. sulcatus (3.49%). for the effect of spatial autocorrelation on species distribution, . Subfamily Apicotermitinae: Taxa of this little known i.e., the phenomenon by which sites closer to each other have subfamily had the highest frequency of occurrence, more similar species composition than further ones, regardless including Apicotermitinae sp. 1 and 2, which was among the of environmental variation (Dr a y et al. 2006, 2012; Le g e n d r e & four most common taxa. Most species of this subfamily are Le g e n d r e 2012). Here, we transformed the species composition humus-feeders that do not build epigean or arboreal nests into a dissimilarity matrix using the Bray-Curtis distance against (Co n s t a n t i n o 1999). Members of this subfamily can be usually macroclimatic dissimilarity obtained above, while controlling for found cohabiting nests of other termites species, promoting the effect of spatial distance (Euclidean distance) (Le g e n d r e & organic matter decomposition and nutrient cycling (Di e h l et Le g e n d r e 2012). The significance of the correlation was estimated al. 2005; Cu n h a & Mo r a i s 2010). There are only five genera by 999 permutations of rows and columns of the species of this subfamily in South America (Co n s t a n t i n o 2002a), dissimilarity matrix (Le g e n d r e & Le g e n d r e 2012). We also made of which only Anoplotermes pacificus Müller is considered separate Partial Mantel tests using each functional group: wood- a pest of Eucalyptus. Also, species of Aparatermes and feeder, humus-feeder, and grass-litter feeder. We could not run Grigiotermes are considered pests of rice crops (reviewed partial Mantel tests for the intermediate group because we found in Co n s t a n t i n o 2002b). However, most species of this group only two species. Analyses were conducted in R (R Co r e Te a m , helps in nutrient cycling and soil aeration, acting as primary 2013) packages vegan (Ok s a n e n et al. 2013) and labdsv (Ro b e r t s consumers and decomposers (La v e ll e et al. 1997; Bi g n e ll &
2013). 107 Eggl e t o n 2000; Ho l t & Le p a g e 2000; Da v i e s 2002). Thus, Results the occurrence of Apicotermitinae in sugarcane plantations seems to be important for the maintenance of soil quality, Richness and abundance. We obtained 247 samples, of and the use of insecticides is unnecessary. e-ISSN 1983-0572 108
Table 1: Termite species recorded, with functional group, and nesting in sugarcane plantations of 53 cities in the state of São Paulo, Brazil. Termite CommunitiesinSugarcanePlantationsin…
Family Subfamily Species Sampling units Frequency Functional group* Pest Status ** Crops **
Rhinotermitidae 8 3.49
Heterotermes sulcatus Mathews 8 3.49 wood low unknown
Termitidae 221 96.51
Apicotermitinae 85 37.12
Apicotermitinae sp. 8 3.49 humus unknown various
Apicotermitinae sp.1 16 6.99 humus unknown various
Apicotermitinae sp.2 57 24.89 humus unknown various
Apicotermitinae sp.3 4 1.75 humus unknown various
Nasutitermitinae 2 0.87
Parvitermes sp. Emerson (in Snyder) 1 0.435 wood unknown unknown
Velocitermes sp. Holmgren 1 0.435 grass-litter unknown soybean, cassava
Syntermtinae 64 27.95
Embiratermes heterotypus Silvestri 7 3.06 intermediate unknown eucalyptus
Cornitermes bequaerti Emerson 7 3.06 grass-litter very low pasture
Cornitermes cumulans Kollar (in Pohl) 30 13.10 grass-litter major pasture, sugarcane
Cornitermes sp. Wasmann 1 0.44 grass-litter major pasture, sugarcane
Procornitermes triacifer Silvestri 4 1.75 grass-litter major sugarcane, rice, cofffe, eucalyptus, maize
Silvestritermes euamignathus Silvestri 1 0.44 intermediate unknown unknown
Syntermes dirus Burmeister 1 0.44 grass-litter unknown unknown
Syntermes molestus Burmeister 1 0.44 grass-litter very low sugarcane,rice
Syntermes nanus Constantino 4 1.75 grass-litter major eucalyptus, rice
Syntermes insidians Silvestri 2 0.87 grass-litter very low eucalyptus
Syntermes sp. Holmgren 5 2.18 grass-litter unknown unknown
Syntermes sp.1 1 0.44 grass-litter unknown unknown e-ISSN 1983-0572
Termitinae 70 30.57 Junqueira
Cylindrotermes caata Rocha & Cancello 1 0.44 wood very low sugarcane, eucalyptus
Cylindrotermes sp. Holmgren 2 0.87 wood unknown unknown
Neocapritermes opacus Hagen 67 29.26 wood major eucalyptus et al.
TOTAL 4 22 229 100
* Following Re z e n d e (2012) **Following Co n s t a n t i n o (2002b) Maio - Agosto 2015 - www.periodico.ebras.bio.br EntomoBrasilis 8 (2)
Figure 2. Mean (± standard deviation) species accumulation curve of Figure 3. Species abundance distribution curve showing a Mandelbrot termite species collected in sugarcane plantations of 53 cities in the state model distribution of termite species collected in sugarcane plantation in of São Paulo, Brazil. 53 cities of the state of São Paulo, Brazil.
Figure 4. Occurrence of termites (number of samples) in sugarcane plantations in 53 cities of the state of São Paulo. Observed and expected values according to Zipf-Mandelbrot model for the 22 taxa collected. The dashed arrow indicates the inflection point of the curve. Species at the left side were classified as common, and those at the right side were classified as rare.
. Subfamily Termitinae: N. opacus (29.26%) was the most 12 possible options chemicals to control this species in frequent among the common species. This species occurs sugarcane plantations. from Ecuador to eastern Argentina and southern Brazil (Kr i s h n a & Ar a u j o 1968; Co n s t a n t i n o 1998), it feeds on wood . Subfamily Syntermitinae: C. cumulans was common, with on the floor (Co n s t a n t i n o 1999) and is considered a pest in frequency of occurrence of 13.10%. The genus Cornitermes Eucalyptus (reviewed in Co n s t a n t i n o 2002b; Co n t a n t i n o is widely distributed in South America, occurring from the 109 2014) and sugarcane plantations (Ch e a v e g a t t i -Gi a n o t t o Amazon basin to southern Brazil, extending to Paraguay et al. 2011). Thus, the Brazilian System of Phytosanitary and northeastern Argentina (Em e r s o n 1952; Co n s t a n t i n o Agrochemicals (AGROFIT 2012) recommends up to 1998). Most species build epigean nests, but some live in e-ISSN 1983-0572 110 Figure 6:Correlationbetweenbioclimaticandspeciesdissimilarity (PartialMantelTestr=0.13;P<0.01). wood-feeders andhumus-feeders. of 50% ≥ with termites, of groups functional of distribution the showing Paulo São state the in sampled cities of distribution Geographical 5. Figure Termite CommunitiesinSugarcanePlantationsin… C (C are usually a homogeneous environment with no competitors w ohr eea f hs subfamily, this of genera other Two material and it is often found in pastures (C negon nss (C nests underground 1998). However, other studies (C C in (reviewed plantations sugarcane in pest a considered is they do not reduce the grazing area. Nonetheless, this genus since harmful, not are nests epigean their that found 2007) f i Gad d Sl (D Sul do Grande Rio of state Brazilian the in livestock for areas grazing reduce to whose chemical control is recommended by recommended is control chemical whose o n i t n a t s n o a h n u a h n u
et al. & M 2006;
s i a r o 2002b; 2010). V a C l o i r é e v a e h o n i t n a t s n o h e i Cornitermes 2006; g l i t t a
t al. et -G e z C 99. t ed o plant on feeds It 1999). i r r a p o t t o n a i k a 2005;
et al. j Procornitermes o a be suggested been has
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ae on ta te mgt e et n te cultures. (C other Argentina northern to Bolivia and Brazil in Central pest be might Procornitermes they that found have Syntermes, (C Andes the of east Argentina, northeastern and northern to America South northern from occurs It study. this in rare genus and uh as such some species of this genus are considered pests in sugarcane, G 96 ad t ocrec ses o e iie b climatic by limited factors in be northern South to America (E seems occurrence its and 1986) o t t o n a i o n i t n a t s n o Proconitermes striatus Proconitermes Syntermes
t al. et rcntre triacifer Proconitermes were rare in this study, although some authors some although study, this in rare were 98 ad ed mil o lte, being litter, on mainly feeds and 1998) 2011; cus rm oten mzn across Amazon, southern from occurs f h sm sbaiy a considered was subfamily same the of AGROFIT (Hagen) (AGROFIT (Hagen) 2012; e-ISSN 1983-0572 n o s r e m ivsr (C Silvestri C o n i t n a t s o Junqueira 1952). However, 2012). The 2012). e v a e h 2002b) et al. e c n a g i t t a L L o -
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considered a pest in sugarcane, Eucalyptus, rice plantations, grass-litter feeders were affected when we tested the influence and pastures (reviewed in Co s n t a n t i n o 2002b). A previous of climatic variables on functional groups. Wood-feeders were study (Mi r a n d a et al. 2004) recorded Syntermes nanus not affected and intermediates were not tested due to low sample Constantino in sugarcane plantations in northeastern size. Brazil. However, the frequency of leaves attack does not cause significant losses. There are many controversies about functional group classification of N. opacus. It was considered here a wood-feeder, but it has been . Family Rhinotermitidae: The only Rhinotermitidae species defined as intermediate feeder by Co n s t a n t i n o (2002), wood- recorded by us was H. sulcatus, which had a low occurrence feeder by Re z e n d e (2012), and wood/humus-feeder by So u z a et frequency and was considered rare. The genus Heterotermes al. (2012). This species has been found feeding on trees, trunks occurs from southern Mexico, including the Bahamas and and roots, with soil nests in the Brazilian Cerrado (Ma t h e w s West Indies, to northern Argentina, but H. tenuis has a 1977). Some authors (e.g., Sl e a f o r d et al. 1996; Do n o v a n et al. wide distribution throughout South America (Co n s t a n t i n o 2001) suggest that termite diet is distributed along a gradient of 1998, 2001). It feeds on living or dead plant material, having humification, from living timber to humus. This could explain the been considered pest in several crops, mainly sugarcane and assignment of N. opacus to different functional groups, especially timber (Ha i f i g et al. 2008). A previous study in São Paulo because the species behavior in some studies cited was based (Al m e i d a & Al v e s 1999) considered H. tenuis as the main pest on field observations. Additionally, this would explain why the in sugarcane plantations due to its wide distribution and high distribution of this species here was influenced by environmental abundance. The estimated damage caused by this species variables, when tested along with rare species, when the reverse can reach US$ 500/ha (Ga r c i a 2004), including chemical was true when tested clumped with wood-feeders. control, for which up to 42 possible options chemicals can be used (AGROFIT 2012). The low occurrence frequency of A previous study (Ac k e r m a n et al. 2009) found a high frequency H. sulcatus we found (3.5%) may indicate a decline in its of occurrence of humus-feeders (57%) in less diverse agroforests abundance due to the continuous use of insecticides over and primary forests in Central Amazonia, suggesting that the the last decade, which is interesting for commercial crops. ability of agroforests to support populations of humus-feeders could potentially have a positive effect on soil fertility in The remaining 18 taxa of termites collected in the sugarcane agroecosystems. Conversely, Mi r a n d a et al. (2004) did not record plantations of São Paulo and to samples were categorized as humus-feeders in a sugarcane plantation in Northeastern Brazil. rare. However, we suggest that termite regional fauna should be maintained. According to Ol i v e i r a & De l -Cl a r o (2005) and Another study (Pa l i n et al. 2011) along an Amazon-Andes De l -Cl a r o (2008) interspecific ecological relationships and altitudinal gradient in Peru found that the diversity declined overlapping of niches are important for the maintenance of with increased elevation. However, functional groups responded populations at low levels. Ca r r i j o et al. (2009) showed that differently to the upper distribution limit. For example, the habitat simplification in the “Cerrado” led to extinction of distribution limit for humus-feeders was between 925 and 1,500 termite populations as well as other members of the fauna and m asl, while for wood-feeders it was between 1,550 and 1,850 flora for the loss of specific features due to the application of m asl. This pattern suggested that energy requirements of each pesticides. According to Si n g h & Si n g h (2001) the abundance group are a key factor shaping species occurrence associated with and composition of termite’s community respond differently to altitude and temperature. environments and insecticide use. The model that best fitted the species abundance distribution The influence of climatic variables on termite occurrence was Zipf-Mandelbrot. Following Wi l s o n (1991) the presence of a in sugarcane plantations. Environmental variables, such species in this model depends on the previous physical condition as altitude, temperature, and rainfall, besides local vegetation and previous species presence. Specifically, pioneer species, structure and complexity influence termite communities (Co ll i n s requiring little previous conditions. Late successional species 1980; Ga t h o r n e -Ha r d y et al. 2001; Da v i e s 2002; In o u e et al. 2006; need more energy, time, and organization of the ecosystem Jo n e s & Eggl e t o n 2011). However, it is difficult to generalize before they can invade, justifying why these species are rare. distribution patterns of termites in South America (Jo n e s & These differences between pioneer and late successional species Eggl e t o n 2011), because collections and studies are concentrated give a Zipf-Mandelbrot distribution. on a few regions of Guyana and Brazil, especially Amazonia, São Finally, it seems that continued use of insecticides had possibly Paulo, and Mato Grosso. Furthermore, a previous study (Di e h l reduced the abundance of some pest species, which are now rare, et al. 2014) suggests a positive relationship between species such as those of the genus Heterotermes. Contrarily to other occurrence and altitude in different geomorphological regions studies, our results suggest that most termite species recorded of Rio Grande do Sul state in southern Brazil. However, their is potentially beneficial for sugarcane plantations, given the high results were inconclusive due to the low number of collections incidence of humus-feeders. We then reinforce the importance in the state. of associating ecology research to agricultural systems and Here, climate variables influenced the distribution of four pest control methods and suggest an in-depth Integrated Pest common taxa: N. opacus (wood-feeder), Apicotermitinae sp. Management (IPM) analysis based on data on damage/injury 1 and 2 (humus-feeder), and C. cumulans (grass-litter feeder), coupled with cost/benefits of control. but none of the 18 rare taxa. However, only humus-feeders and 111
e-ISSN 1983-0572 112 Appendix 2.ListofmacroclimaticvariablesobtainedfromWorldClim( Appendix 1.GeographiccoordinatesofthecitieswithsugarcaneplantationssampledinstateSãoPaulo. City Altinópolis Araras Areiópolis Bariri Barra Bonita Barrinha Bebedouro Boraceia Botucatu Brodósqui Cajuru Chavantes Cordeirópolis Cravinhos Dois Córregos Guariba Guatapará Iacanga Icém Igaraçu doTietê Ilha Solteira Ipaussu Iracemápolis Itapura Jaú Leme Lençóis Paulista Termite CommunitiesinSugarcanePlantationsin… BIO10 BIO18 BIO19 BIO16 BIO14 BIO12 BIO13 BIO15 BIO17 BIO11 BIO8 BIO6 BIO4 BIO9 BIO2 BIO3 BIO5 BIO7 BIO1 Annual MeanTemperature Temperature AnnualRange(BIO5-BIO6) Min TemperatureofColdestMonth Max TemperatureofWarmestMonth Temperature Seasonality(standarddeviation*100) Isothermality (BIO2/BIO7)(*100) Mean DiurnalRange(Meanofmonthly(maxtemp-mintemp)) Mean TemperatureofWettestQuarter Mean TemperatureofDriestQuarter Precipitation ofColdestQuarter Precipitation ofWarmestQuarter Precipitation ofDriestQuarter Precipitation ofWettestQuarter Precipitation ofDriestMonth Annual Precipitation Mean TemperatureofColdestQuarter Mean TemperatureofWarmestQuarter Precipitation Seasonality(CoefficientofVariation) Precipitation ofWettestMonth Geographic coordinates 21°01’33”S; 47°22’26”W 22°21’25”S; 47°23’02”W 22°40’04”S; 48°39’54”W 22°04’26”S; 48°44’24”W 22°29’42”S; 48°33’28”W 21°11’38”S; 48°09’50”W 20°56’56”S; 48°28’44”W 22°11’34”S; 48°46’44”W 22°53’09”S; 48°26’42”W 20°59’27”S; 47°39’32”W 21°16’30”S 47°18’14”W 23°02’20”S; 49°42’32”W 22°28’55”S; 47°27’25”W 21°20’24”S; 47°43’44”W 22°21’57”S; 48°22’48”W 21°21’36”S; 48°13’40”W 21°29’49”S; 48°02’16”W 21°53’24”S; 49°01’30”W 20°20’31”S; 49°11’42”W 22°30’32”S; 48°33’28”W 22°30’32”S; 48°33’28”W 23°03’25”S; 49°37’33”W 22°34’51”S; 47°31’08”W 20°38’45”S; 51°30’32”W 22°17’45”S; 48°33’28”W 22°11’09”S; 47°23’24”W 22°35’56”S; 48°48’00”W Macroclimatic variables City Luís Antônio Mineiros doTietê Motuca Nova Europa Ourinhos Paulo deFaria Pederneiras Pereira Barreto Piracicaba Pitangueiras Pradópolis Pratânia Quatá Rancharia Ribeirão Preto Rincão Rio Claro Santa CruzdoRioPardo Santa RosadoViterbo Santo AntôniodaAlegria São Manuel São PedroTurvo São Simão Serra Azul Serrana Tabatinga http://www.worldclim.org) Geographic coordinates 21°33’18”S; 47°42’14”W 22°24’32”S; 48°27’03”W 21°30’28”S; 48°09’03”W 21°46’40”S; 48°33’39”W 22°58’44”S; 49°52’15”W 20°01’51”S; 49°22’58”W 22°21’07”S; 48°46’30”W 20°38’16”S; 51°06’32”W 22°43’30”S; 47°38’56”W 21°00’32”S; 48°13’19”W 21°21’32”S; 48°03’57”W 22°48’28”S; 48°39’57”W 22°14’52”S; 50°41’52”W 22°13’44”S; 50°53’34”W 21°10’40”S; 47°48’36”W 21°35’13”S; 48°04’15”W 22°24’39”S; 47°33’39”W 22°53’56”S; 49°37’58”W 21°28’22”S; 47°21’46”W 21°05’13”S; 47°09’03”W 22°43’51”S; 48°34’15”W 22°44’49”S; 49°44’24”W 21°28’44”S; 47°33’03”W 21°18’39”S; 47°33’57”W 21°12’39”S; 47°35’45”W 21°43’01”S; 48°41’16”W e-ISSN 1983-0572 Junqueira et al. Maio - Agosto 2015 - www.periodico.ebras.bio.br EntomoBrasilis 8 (2)
Appendix 3. Cities in the states of São Paulo, Brazil, whose sugarcane plantations had a frequency of occurrence ≥ 50% for humus-feeders and wood- feeders. Frequency of occurrence of functional groups of termites ≥ 50% humus-feeders ≥ 50% wood-feeders Altinópolis
Bariri Areiopólis
Botucatu Bebedouro
Chavantes Brodósqui
Iacanga Cajurú
Icem Dois Córregos
Igaraçú do Tietê Guariba
Ilha Solteira Guatapara
Itapura Luis Antônio
Lençóis Paulista Ourinhos
Mineiros do Tietê Piracicaba
Paulo de Faria Pitangueiras
Pederneiras Ribeirão Preto
Pereira Barreto Rincão
Pratânia Rio Claro
Santa Cruz do Rio Pardo Santo Antônio da Alegria
Santa Rosa do Viterbo Serra Azul
Tabatinga
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e-ISSN 1983-0572 116 Sleaford, F., D.E. Bignell & P. Eggleton, 1996. A pilot analysis of analysis pilot A 1996. Eggleton, P. & Bignell D.E. F., Sleaford, for insecticide of Application 2001. Singh, N.B. & M. Singh, Siqueira, T., L.M. Bini, F.O. Roque, S.R.M. Couceiro, S. Trivinho- Multivariate and Ordination labdsv: 2013. D.W., Roberts, oeh, . 19. pce Ceitne eooia and ecological Coexistence: Species 1999. M., Tokeshi, Souza, H.B. de A., W de F. Alves & A. Vasconcellos, 2012. Termite Available in: Ecological an Brazil: Southeastern Approach EntomoBrasilis,8(2):105-116. in Plantations Sugarcane in Communities Termite 2015. Teixeira, L.M.C. & Gonçalves E.R. L.K., Junqueira, Suggested citation: Termite CommunitiesinSugarcanePlantationsin… j.1365-2311.1996.tb01245. Cameroon. Ecological Entomology, 21: 279-288. doi: Reserve, Forest Mbalmayo the from termites in contents gut in sugarcane.SugarTech,3:146-153. contributing characters on yield termite controlanditseffect doi: j.1600-0587.2011.06875. 183–192. macroinvertebrate 35: in Ecography, processes species metacommunities. rare niche and similar Common to 2012. respond Cottenie, K. & Strixino