767 Morphometric Characterization of a Population of Tetrapedia diversipes in Restricted Areas in Bahia, Brazil (Hymenoptera: Apidae) by Cynthia Maria de Lyra Neves1; Carlos Alfredo Lopes de Carvalho1; Adriane Vieira Souza1 & Cristovam Alves de Lima Junior1 ABSTRACT Tetrapedia species are solitary bees which collect floral oils, being restricted to tropical regions of the Americas. Information on forms of nesting has been little researched in the literature, requiring studies on the diversity and vari- ability of species to obtain better management and conservation strategies for their populations. Morphometry is a efficient technique and has been used to detect variation and for identification of species of bees in order to detect changes in quantitative traits within and among populations of bees. This study aimed to compare the variability of the population of Tetrapedia diversipes in artificial nests located in orchards and their surroundings (other fruit) of acerola in a restricted area of the Reconcavo region of Bahia, Brazil. Right wings were extracted from 155 individuals of the T. diversipes species, to perform the morphometric analysis. In conventional morphometry, 9 variables contributed significantly to the sexual dimorphism in the study areas (α = 0.05). The geometric morphometric analysis revealed low gene flow in populations of T. diversipes demonstrating loss of genetic diversity, requiring proper management of this bee for its conservation and maintenance of the associated flora. KEY WORDS: Solitary Bees, Tetrapediini, Morphometry. INTRODUCTION Solitary bees represent approximately 330 species in the Neotropical re- gion (Michener 2000) including the genus Tetrapedia (Tetrapediini) with 18 1 Insecta Research Group; Center of Agricultural, Environmental and Biological Sciences, Federal University of Bahia Reconcavo (UFRB), 44380-000, Cruz das Almas-BA, Brazil. E-mail: cmlneves@ msn.com; insecta@ufrb.edu.br 768 Sociobiolog y Vol. 59, No. 3, 2012 described species in Brazil (Silveira et al. 2002), presenting different morpho- logical and behavioral characters in their nesting (Cordeiro et al. 2010). The Tetrapedia species use preexisting cavities as nesting sites which allows the sampling of these bees by means of trap-nests or artificial nests (Camillo 2005), and this solitary behavior is another hallmark of the Tetrapediini tribe characterized by independence of the female in the construction and supply their nest (Alves-dos-Santos et al. 2007). The study of oil-collecting bees and their importance in the pollination of many plant groups is an important tool to contribute to the knowledge of their ecolog y, economic importance (Imperatriz-Fonseca 2010) and morpho- logical variation of bee populations in their natural environment (Francoy & Imperatriz-Fonseca 2010). Research for the evaluation of morphological diversity is important in ecological and genetic studies, and one of the tech- niques used in these studies are morphometric tools (Rohlf 1990). In morphometric analysis variation is studied through the covariation between pairs of linear measurements, and geometric morphometry is able to more clearly describe and locate the regions of changes and rebuild and reconstruct these differences graphically (Francoy et al. 2011). Morphometry has been widely applied in many studies with social bees using tools to detect or describe genetic patterns in colonies, species identi- fication, geographical variations and phylogenetic relationships among and within populations of bees (Peruquetti 2003, Mendes et al. 2007; Nunes et al. 2008, Souza et al. 2009, Carvalho et al. 2011; Ferreira et al. 2011; Francoy et al. 2011, Souza et al. 2010), and variability in shape and size of wings of social bees (Nunes et al. 2007; Quezada-Euán et al. 2007). However, there are few morphometric studies on solitary bees (Bosch 2008), with the exception of a study on the patterns of wing venation and geographical differences between populations of the Centris genus (Ferreira et al. 2011) and one study on the morpholog y of Tetrapedia diversipes applying linear morphometric analysis to length and width of the wings, head width and cephalic and mouth ap- pendages (Smith et al. 2011). In this context, considering the importance of morphometric studies in populations of bees, it is necessary to collect data on solitary bees and offer suggestions for future research aimed at the morphological variability within and among populations, diversity and biolog y of nesting. The study aimed to compare the degree the morphological variability of Tetrapedia diversipes 769 Neves, C. et al. — Morphometric Characterization of Tetrapedia diversipes residing in artificial nests located in orchards and their surroundings (other fruit) of acerola in a restricted area in the Bahia Reconcavo region, Brazil. MATERIAL AND METHODS The experiment was conducted in Embrapa (Brazilian Agricultural Research Corporation) Cassava and Tropical Fruits in the period between March/2008 and August/2009 in the Municipality of Cruz das Almas (12 ° 40’12 “S, 39 º 06’07” W, 220 m), located in the Reconcavo of Bahia, Brazil. The nests were installed in four areas: Area I - Active Germplasm Bank of Malpighia emarginata DC; Area II - Other Orchards (Citrus spp., Spondias sp., Musa spp. and Mangifera indica); Area III - Transition area (the area between the forest and other orchards) and Area IV - Forest Fragment. The artificial nests were made of colored paper timber of 5 mm in diameter with a length of 15 cm (Machado 2011), and the species collected from the Tetrapediini tribe was Tetrapedia diversipes. The sealed nests were transferred to the Laboratory of the Center for the Study of Insects (INSECTA) of the Federal University of Bahia Reconcavo (UFRB), and placed in BOD (Biologic Oxygen Demand) chambers at a tem- perature of 25 ± 1 ° C, humidity 80% ± 1% with a photoperiod of 12 hours. Right wings of T. diversipes were removed and placed between two plates to capture images using the program Motic 2.0 ML with a digital camera coupled to a stereomicroscope, with 7.5 X magnification (Carvalho et al. 2011). The veins and cells wings were classified according to the methodolog y described by Silveira et al. (2002), and biological material has been identified, and stored in Eppendorf tubes of 1.5 mL and deposited in the collection of the Laboratory of the Center for the Study of Insects (Núcleo de Estudos dos Insetos-INSECTA), at the Center of Agricultural, Environmental and Bio- logical Sciences (Centro de Ciências Agrárias, Ambientais e Biológicas) of the Federal University of Bahia Reconcavo (UFRB). Geometric Morphometric Analysis 18 landmarks were defined and recorded using intersections of the veins of the forewings of Tetrapedia diversipes specimens (Fig. 1) using software tpsDig2 version 2.12 (Rohlf 2008a). The alignment of the x and y coordinates of each line of the wings (alx aly) and the centroid size of the wings can be 770 Sociobiolog y Vol. 59, No. 3, 2012 used as a data matrix (matrix W) in order to perform multivariate analysis (Rohlf 2008b). The coordinates of the landmarks of the wings and centroid size were used in principal component analysis (PCA), the matrix W was used in multi- variate analysis of variance (MANOVA) and cluster analysis by UPGMA (Unweighted Pair-Group Method using Arithmetic Average). Conventional Morphometric Analysis In this analysis we used 24 linear measurements in the right wings (Figs. 2, 3) of 155 individuals measured by Motic software 2.0 ML. Measurements of the veins and cells were applied according to the methodolog y of de Souza et al. (2010), which used 17 measures on the forewing (length - C and Width - L of the wing, width and length of 1st, 2nd and 3rd submarginal cells, and 1st and 2nd Medial cells (M), length of the Subcostal veins + Radial (Sc + R) and Anal-1 vein; length of the cells: Marginal (M) and the 2nd cubital (Cu); distance from the intersection of the Anal-1 vein with Cubital-anal (Cu-a) until the intersection of the Cubital vein with 1st Middle-Cubital (m-Cu) and the hindwings with 7 measurements (length and width of the wing ; length of the ribs sector Radial (R), Anal-1 and Cubital-anal veins; distance from the intersection of the rib Anal -1 with cubital-anal until the intersection of the median-Radial sector (Rs-m) with the Radial sector (Rs) and Radial (R) cell width. Fig. 1 – Landmarks used for geometric morphometric analysis of the forewing Tetrapedia diversipes. 771 Neves, C. et al. — Morphometric Characterization of Tetrapedia diversipes The differences between the sexes of the individuals of the species T. diversipes were analyzed by multivariate variance (MANOVA), canonical variables (AVC), principal components (PCA) and cluster analysis by the UPGMA method. RESULTS AND DISCUSSION Conventional Morphometrics For the multivariate analysis of variance (MANOVA), there was a significant difference between groups of individuals (Wilk’s λ = 0.65109, p <0.00001), Fig. 2 – Linear measurements of morphological characters of the forewing (A) and hindwing (B) female Tetrapedia diversipes by conventional morphometric. Legend: Length (L), width (W), Radial + Subcostal veins (Sc + R), Cubital vein (Cu), Cubital-anal (Cu-a), Middle-Cubital or median-Cubital (m-Cu), Radial (R), Radial sector (Rs), median-Radial sector (m-Rs). 772 Sociobiolog y Vol. 59, No. 3, 2012 with only 10 variables contributing significantly to the separation of individu- als (α = 0.05), confirming the existence of sexual dimorphism of this species in relation to the size of the wings. This separation is represented graphically by principal component analysis (Fig. 4). In principal component analysis (PCA) performed to test the existence of sexual dimorphism of T. diversipes the first three variables explained 74.40% of the variation, with the first component explained 63.28%, the second and the third 6.70%, and 4.42% (Table 1), and the variables that contributed most to the first component were length and width of forewings (Table 2). Fig. 3 – Linear measurements of morphological characters of the forewing (A) and hindwing (B) male Tetrapedia diversipes by conventional morphometric. Legend: Length (L), width (W), Radial + Subcostal veins (Sc + R), Cubital vein (Cu), Cubital-anal (Cu-a), Middle-Cubital or median- Cubital (m-Cu), Radial (R), Radial sector (Rs), median-Radial sector (m-Rs). 773 Neves, C. et al. — Morphometric Characterization of Tetrapedia diversipes To evaluate the differences between the areas another PCA was performed (Fig. 5), where an overposition between the three areas of the population occurred, demonstrating the existence of low morphometric divergence be- tween individuals of the three areas. This can be explained by the vicinity of the sampled areas, which contributes to gene flow between the population and therefore, maintains a similar phenotypic pattern. The analysis of canonical variables showed morphometric differences between individuals in Area I and II, and area III formed a group with characteristics that are similar to areas I and II (Fig. 6). Multivariate analysis of variance (MANOVA) for the three areas showed a significant difference between individuals collected in areas I, II and III (Wilk’s λ = 0.57864, p <0.00001), where only 9 variables corresponding to the forewings contributed significantly to the separation of individuals in each area (α = 0.05). Considering the Mahalanobis D2 distances (Table 3) between the areas, it appears that individuals of the areas I (Active Germplasm Bank of M. emar- Fig. 4 - Graphic dispersion between males and females Tetrapedia diversipes in relation to Cartesian axes established by the first two principal components (PC1, PC2). 774 Sociobiolog y Vol. 59, No. 3, 2012 ginata) and II (Other Orchards) showed highly significant morphological differences (p <0.00001). However, comparing areas I and III (Transition area: between the forest and other orchards), and II and III there was no significant difference between the total sample, demonstrating morphometric similarity, which can be attributed to the similarity of available resources between these areas. Table 1 - Eigenvalues, Total Variation (%), Proportion (%) and Cumulative Proportion of the 24 variables obtained with principal component analysis of Tetrapedia diversipes wings in the areas studied, Bahia of Reconcavo region, Brazil. Principal Component Eigenvalue Total Variation (%) Proportion (%) Cumulative Proportion 1 15.1888 63.2868 15.1888 63.2868 2 1.6056 6.6901 16.7944 69.9769 3 1.0622 4.4257 17.8566 74.4026 4 0.8999 3.7494 18.7565 78.1520 5 0.6954 2.8976 19.4519 81.0497 6 0.6015 2.5064 20.0535 83.5560 7 0.5423 2.2597 20.5958 85.8158 8 0.4739 1.9747 21.0697 87.7905 9 0.4454 1.8560 21.5152 89.6465 10 0.4061 1.6922 21.9213 91.3387 11 0.3427 1.4279 22.2640 92.7666 12 0.2890 1.2041 22.5530 93.9706 13 0.2375 0.9898 22.7905 94.9604 14 0.2114 0.8809 23.0019 95.8413 15 0.1979 0.8245 23.1998 96.6659 16 0.1609 0.6702 23.3607 97.3361 17 0.1494 0.6224 23.5101 97.9586 18 0.1162 0.4840 23.6262 98.4425 19 0.0985 0.4103 23.7247 98.8528 20 0.0695 0.2896 23.7942 99.1424 21 0.0636 0.2651 23.8578 99.4075 22 0.0609 0.2537 23.9187 99.6612 23 0.0464 0.1935 23.9651 99.8547 24 0.0349 0.1453 24.0000 100.00 775 Neves, C. et al. — Morphometric Characterization of Tetrapedia diversipes Table 2. Principal component analysis between males and females of Tetrapedia diversipes, Bahia of Reconcavo region, Brazil. Variable Principal Component PC01 PC02 L1 0.6028 0.0439 L2 0.7141 0.0823 L3 0.8419 0.0173 L4 0.8128 0.1221 L5 0.7525 0.3258 L6 0.7385 0.3392 L7 0.7719 0.3525 L8 0.7364 0.2207 L9 0.9338 0.1445 L10 0.8580 0.2261 L11 0.7232 0.1663 L12 0.8485 0.3841 L13 0.8553 0.3358 L14 0.7541 0.1905 L15 0.7733 0.3139 L16 0.9335 0.1209 L17 0.9340 0.1748 L18 0.8054 0.1504 L19 0.7467 0.3711 L20 0.8668 0.1418 L21 0.4813 0.6517 L22 0.8023 0.0295 L23 0.7515 0.2033 L24 0.8975 0.0174 Legend: L1: Width of 1st submarginal cell; L2: Length of the 1st submarginal cell; L3: length of mar- ginal cell; L4: width of the 2nd submarginal cell: L5: length of the 2nd submarginal cell; L6: width of the 3rd submarginal cell; L7: length of the 3rd submarginal cell, L8: width of the 1st Medial cell; L9: length of the 1st Medial cell; L10: width of the 2nd Medial cell; L11: length of the 2nd medial cell; L12: Intersection of anal 1 vein with Cu-a (anal 1-Cubital) until intersection of Cu (Cubital vein) with 1st m-Cu (1st median-Cubital); Ll3: length of the 2nd Cubital cell; L14: length of Sc + R (Subcostal + Radial); L15: length of anal 1; L16: length of forewing ; L17: width of the forewing ; L18: length of the radial sector (Rs); L19: radial cell width; L20: width of the hindwing ; L21-length of the Cu-a; L22: Intersection of anal 1 with Cu-a until intersection of m-Rs (median-Radial sector) with Radial sector (Rs); L23: the length of the anal 1 vein; L24: length of hindwing. 776 Sociobiolog y Vol. 59, No. 3, 2012 Fig. 5 - Graphic dispersion of the population Tetrapedia diversipes in relation to Cartesian axes established by the first two principal components (PC1, PC2). Table 3 - Mahalanobis D2 distances (superior part) and statistical significance (p) for each distance (inferior part) between areas, by conventional morphometry analysis: I - Active Germplasm Bank of Malpighia emarginata; II - Other Orchards (Citrus spp., Spondias sp., Musa spp. and Mangifera indica) and III - Transition area (the area between the forest and other orchards). Area I II III I - 2.646967 2.137111 II 0.00001 - 5.670577 III 0.758967 0.086292 - 777 Neves, C. et al. — Morphometric Characterization of Tetrapedia diversipes Fig. 6 - Graphic dispersion of the population Tetrapedia diversipes in relation to Cartesian axes established by canonical variables (CV1, CV2) obtained from morphological characteristics of wings. Table 4 - Mahalanobis D2 distances (superior part) and statistical significance (p) for each distance (inferior part) between areas, by geometric morphometry analysis: I - Active Germplasm Bank of Malpighia emarginata; II - Other Orchards (Citrus spp., Spondias sp., Musa spp. and Mangifera indica) and III - Transition area (the area between the forest and other orchards). Area I II III I - 3.83154 6.76865 II 0.00001 - 10.84870 III 0.239981 0.017491 - 778 Sociobiolog y Vol. 59, No. 3, 2012 Ferreira et al. (2011) studied the degree of differentiation of populations in areas of Centris aenea in acerola orchards, where they observed significant morphometric differences between individuals, corroborating the present study. It is very important to consider that there are fluctuations of trophic resources over time, and the phenotypic expression of the bees may vary ac- cording to availability of resources. Geometric Morphometrics Multivariate analysis of variance (MANOVA) with the matrix W to observe the difference between the areas, also found significant differences (Wilk’s λ = 0.459, p <0.0001) between individuals of T. diversipes collected in the three areas, and all variables of the matrix W contributed significantly (α = 0.05) to discriminate between the groups in the areas. With the triangular matrix of Mahalanobis D2 distances from the data coming from the matrix W, we found again significant differences between Fig. 7 - Graphic dispersion between the bees T. diversipes in each area, in relation to Cartesian axes established by canonical variables (CV1, CV2). 779 Neves, C. et al. — Morphometric Characterization of Tetrapedia diversipes area I and areas I and II. However, among areas I and III, there was no sig- nificant difference (Table 4). Ghaderi et al. (1984) found that when several characteristics are analyzed at once, the squared Mahalanobis distances can be used as estimates of genetic diversity among the groups or areas where this variability is the result of morpho-physiological characteristics and ecological differences. The analysis of canonical variables produced a difference between individuals in areas I, II and III (Fig. 7). The individuals of T. diversipes in areas I and III showed similar morphometrics, so there is probably a greater genetic interac- tion between the bees in these two areas. This similarity can be attributed to a low level of gene flow, with the assumption of the occurrence of inbreed- ing. According to Breda et al. (2004) inbreeding occurs among individuals related by descent, or is the union of individuals more closely related than the average population, increasing the homozygosity and phenotypic effect of expressing the recessive genes. It is possible that the fragmentation of the environment caused by anthropogenic activities and is mainly favoring the isolation of the population of T. diversipes, increasing the rate of inbreeding, weakening the genetic diversity and therefore favoring the disappearance of bees in these areas. Similar data were found by Mendes et al. (2007). Analyzing the popula- tion Nannotrigona testaceicornis collected in two urban areas and an area of natural vegetation, they found that in urban areas there were more similarities when compared with areas of natural vegetation, affecting gene flow of these bees. However, Gonçalves (2010) noted that the geometric morphometry of wings was not sensitive enough to separate samples of Frisieomelita varies in natural and disturbed areas and diverged from the present work. The conservation of native flora and reducing human disturbance around natural and agricultural areas can contribute to the maintenance of intrapo- pulation genetic material of T. diversipes, increasing their genetic variability and ensuring survival, demonstrating the need for further studies on the evolutionary variations of this species. CONCLUSION A conventional morphometric analysis revealed the existence of sexual dimorphism of the species Tetrapedia diversipes. However, geometric mor- 780 Sociobiolog y Vol. 59, No. 3, 2012 phometrics indicated the existence of low levels of gene flow, facilitating the isolation and weakening of the genetic diversity in the population. The study of morphometric characterization has provided important data on the degree of intrapopulational differentiation of T. diversipes, facilitating future research on other species of Tetrapedia, supporting strategies for the conservation and maintenance of this bee. ACKNOWLEDGMENTS The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. 303237/2010-4 and Proc. 506290/2010-7), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarships, Embrapa Mandioca e Fruticultura Tropical for providing the study areas and PhD. João Paulo Morselli for the wing study design. REFERENCES Alves-dos-Santos, I., I.C. Machado & M.C. Gaglianone. 2007. História natural das abelhas coletoras de óleo. Oecologia Brasiliensis 11: p. 544-557. Bosch, J. 2008. Production of undersized offspring in a solitary bee. Applied Animal Behavior Science 75: p. 809-816. Breda, F.C.; R.F. Euclydes, S.P. Carmen, A.T. Robledo, L.S.C. Paulo, R.S. José Lindenberg, A.T.F. Rodolpho & K.F.M. Antonia. 2004. Endogamia e limite de seleção em populações selecionadas obtidas por simulação. Revista Brasileira de Zootecnia 33: p. 2017-2025. Camillo, E. 2005. 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