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Revista chilena de entomología

versión impresa ISSN 0034-740Xversión On-line ISSN 0718-8994

Rev. chil. entomol. vol.46 no.3 Santiago set. 2020

http://dx.doi.org/10.35249/rche.46.3.20.02 

Scientific Note

Notes on the nest architecture of Centris (Centris) caxiensis Ducke (Hymenoptera: Apidae) in an urban dry forest fragment in northeastern Brazil

Notas sobre la arquitectura del nido de Centris (Centris) caxiensis Ducke (Hymenoptera: Apidae) en un fragmento urbano de bosque seco en el noreste de Brasil

Herbeson Ovidio De Jesus Martins1  2 

Felipe Vivallo3 

Vinina Silva Ferreira1 

1Universidade Federal do Vale do São Francisco, Colegiado de Ciências Biológicas, Petrolina, Brazil.

2Programa de Pós-Graduação em Entomologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil.

3HYMN Laboratório de Hymenoptera, Departamento de Entomologia, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão 20940‒040 Rio de Janeiro, RJ, Brazil.

Abstract

We described the nest architecture and the brood cell morphology of the oil-collecting bee Centris caxiensis. The nest is a single and unbranched tunnel measuring between 37 and 49 cm in length slant obliquely into the ground. There were one or two brood cells at the end of the gallery oriented vertically. The brood cells are urn-shaped with a plug containing a central hollow process. The nest morphology and the brood cells followed a similar pattern to the other ones reported for species of the subgenus Centris s. str.

Key words: Caatinga; ground-nesting; oil-collecting bee; solitary bee

Resumen

Describimos la arquitectura del nido y la morfología de las celdillas de cría de la abeja recolectora de aceite Centris caxiensis. El nido corresponde a un túnel único no ramificado que mide entre 37 y 49 centímetros de largo dispuesto oblicuamente en el suelo. Al final del túnel se encuentran una o dos celdillas de cría orientadas verticalmente. Las celdillas de cría tienen forma de barril con una proyección central en forma de chimenea. La morfología, tanto del nido como de las celdillas de cría, siguen un patrón similar a otros encontrados en especies del subgénero Centris s. str.

Palabras clave: Abeja recolectora de aceite; abeja solitaria; Caatinga; nidificación en suelo

The solitary bee genus Centris Fabricius, 1804 consists of approximately 230 species, grouped in 12 subgenera (Moure et al. 2007; Vivallo 2019). These oil-collecting bees have a mutualistic relationship with plants that offer oil from specialized glands (elaiophores) (e.g. Malpighiaceae, Krameriaceae, Plantaginaceae, etc.) (Buchmann 1987; Neff and Simpson 2017). Most females of Centris have morphological structures, elaiospathes, that allow them to collect this floral resource promoting the plant pollination (Vogel 1974; Neff and Simpson 2017). Females use this floral oil to feeding their offspring and/ or to waterproof their brood cells (Vogel 1974; Neff and Simpson 2017).

Bees of the genus Centris have different nesting habits (Coville et al. 1983). Species of the subgenera Centris s. str. Fabricius, C. (Melanocentris) Friese, C. (Paracentris) Cameron, C. (Penthemisia) Moure, C. (Trachina) Klug, and C. (Wagenknechtia) Moure construct their nests in the flat ground or earth banks (Coville et al. 1983; Aguiar and Gaglianone 2003; Sabino et al. 2020). On the other hand, species of C. (Ptilotopus) Klug nest in termitaria (Gaglianone 2001), and those of the subgenera C. (Hemisiella) Moure, C. (Heterocentris) Cockerell and C. (Xanthemisia) Moure build their nests in pre-existing cavities such as wooden galleries made by other insects or abandoned nests of other bee and wasp species (Frankie et al. 1993; Camillo et al. 1995; Aguiar et al. 2005). The nesting habits of the species of C. (Aphemisia) Ayala and C. (Ptilocentris) Snelling remain unknown. Despite the advances in the researches on cavity-nesting bees (Costa and Gonçalves 2019), the studies on the nesting biology of most Centris species remain unknown, mainly those ground nesting due to the difficulty in finding their nests.

Centris (Centris) caxiensis Ducke, 1907 is a Neotropical species found mainly in the Brazilian coastal sand dune (Restinga) (Madeira-da-Silva and Martins 2003). It was also recorded in the dry forest (Caatinga) (Aguiar and Zanella 2005) and in the Brazilian Cerrado (Albuquerque and Mendonça 1996). As far as we know, there is only one study that mentions the nest excavation of C. caxiensis to study trophic ecology, but it did not report the nest architecture (Ribeiro et al. 2008). Here we described the nest architecture and the morphology of the brood cells of C. caxiensis, providing additional information about its reproductive nesting biology.

We carried out this study at the Campus de Ciências Agrárias of the Universidade Federal do Vale do São Francisco (CCA / UNIVASF) (9°19'44.2”S, 40°33'30.1”W), in Petrolina, Pernambuco state, northeastern Brazil. The climate of the region is dry and hot semi-arid (BShw) according to the Köpen classification (1948), with the annual average temperature of 24.8°C (Alvares et al. 2013).

In May 2017, we recorded five females of C. caxiensis digging nests in an earth bank under shrubs (Fig. 1a). We discovered the other seven old nests, but four of them were abandoned by the females before their completion. We excavated five nests and used three for the architecture description. We used a liquid plaster to filling the burrow while we excavated (Fig. 1b). We took the brood cells to the laboratory and measured it using a caliper rule. In addition, we did the chemical and physical analyzes of the soil from the nesting sites. We removed the nest structures and took them to the Laboratório de Entomologia of the Universidade Federal do Vale do São Francisco (UNIVASF), Petrolina, Pernambuco state, Brazil. Voucher specimens are deposited in the Coleção Entomológica of the Museu Nacional Rio de Janeiro, Brazil (MNRJ).

The nests were not aggregated, with their entrances from seven to 30 meters away, approximately. The soil was classified as quartzarenic neossol, with two defined layers. The upper part consisted of earth banks, composed of loose soil deposited artificially, being the layer where we found the nests. The lower part contained a vertical soil (ravine type), which was exposed through excavation. The sand content of the composite nest substrate was high (87.95%) followed by silt (8.15%) and clay (3.90%). In addition, the upper layer was classified as acid (pH = 5.20).

The nests had an entrance ranging from circular to oval measuring between 1 cm and 1.5 cm (n= 5). When females were active, we observed the sand tumuli as a result of the excavation processes. The nest entrance was closed by the females upon completion (Fig. 2a). Following the entrance, we identified a simple gallery measuring between 37 cm and 49 cm in length (from the entrance to the first brood cell). The main tunnel descended vertically to a maximum depth from 21 cm to 28 cm below the surface. At the end we found one (Fig. 2a) or two (Fig. 2c) brood cells oriented vertically. We visualized some nests with the brood cells opened and/or partially provisioned, which suggest 366

that these nests were abandoned (Fig. 2b). Two nests showed a curvature in the tunnel, probably formed to deflect a rock (Fig. 2b-2c). The brood cells were urn-shaped with a plug containing a central hollow process (Fig. 2d). This orifice connected the inner side of the brood cell with the external environment. The brood cells measured 16.78 18.83 mm in length, 10.86-12.16 in maximum diameter, and 10.32-11.03 in minimum diameter.

We also observed the female's activities to build their nests. The first day was intended for excavation of the nest (Fig. 1d). The second day the female transported pollen what means that she was provisioning her brood cells. The third day the female ended her activities in the morning, suggesting that these bees take just a couple of days to build, provisioning and laying their eggs. Moreover only one male emerged after 58 days from the brood cells that we took to the laboratory. The other two brood cells contained a dead larva and a mass of dry pollen.

Figure 1 Main characteristics of the nesting habits of Centris caxiensis. (a) General view of nest site; (b) Excavated nest; (c) Females cleaning nest entrance; (d) Females digging the nest (arrow 1: brood cell; arrow 2: nest entrance). 

The ground-nesting habit is considered plesiomorphic for the centridine bees, occurring in most species of the genus (Coville et al. 1983). In addition, most species of Centris have the habit of digging their nests on flat surfaces (see Coville et al. 1993). The females of C. caxiensis nested in sandy soil, which might have facilitated the excavation of the tunnel. Excluding C. aenea Lepeletier that nests in clay soil (Aguiar and Gaglianone 2003), species of the subgenus Centris s. str. seem to prefer to dig their nests in sandy surfaces (see Coville et al. 1983). Ribeiro et al. (2008) reported the presence of nests of C. caxiensis in sand dunes, which strengthens the hypothesis that the species nests in areas with earth banks.

The shape of the brood cells of C. caxiensis was similar to that observed for other species of Centris, being urn-shaped and with a rounded base (see Coville et al. 1983; Rozen and Buchmann 1990; Aguiar and Gaglianone 2003). In addition, the brood cell closure of C. caxiensis had a central process in the operculum such as other species of the subgenus. In spite of connecting the inner side of the brood cell with the external environment, it is unlikely that external materials such as dust or water will enter the brood cell. The central process morphology, with the upper part usually folded at the base or at its end, may acts as a barrier protecting the inner of the cell. Similar observations were made by Coville et al. (1983) in C. varia (Erichson), cited as C. segregata Crawford one of its junior synonyms. Furthermore, Rozen and Buchmann (1990) suggested that the presence of a hollow central process probably facilitates the exchange of gases between the internal and external environment since the brood cells of these species are lined at the beginning of construction and the waterproofing layer would probably make it difficult to exchange gases through the brood cell wall. However, different brood cell shapes have been reported for C. pallida Fox (Alcock et al. 1976; Rozen and Buchmann 1990) and C. burgdorfi Friese (Sabino et al. 2020), in which the top of the operculum does not have a hollow central process.

Nests of C. caxiensis are deep when compared to other species of Centris that generally have shallow nests [e.g., at depths of 11.8 cm in C. rhodopus Cockerell; 8.3 in C. cockerelli Fox; 10.5 in C. pallida (Alcock et al. 1976); 12 cm in C. collaris Lepeletier; 3.8 4.9 in C. fuscata Lepeletier (Camillo et al. 1993); 5.0-9.5 in C. heithausi Snelling (Coville et al. 1986); and 8.4-14.5 in C. aethyctera Snelling (Vinson and Frankie 1977)]. Nests with similar depth to those observed for C. caxiensis were also observed in other species of the subgenus, such as C. flavofasciata Friese (Vinson and Frankie 1999; Rozen et al. 2011) and C. flavifrons (Fabricius) (Vinson and Frankie 1988; Rêgo et al. 2006; Martins et al. 2014). In addition, the nests of C. caxiensis were formed by a simple tunnel ending in one or two brood cells. Coville et al. (1983) suggested that this type of structure is plesiomorphic for Centris species, being reported in C. pallida (Alcock et al. 1976; Rozen and Buchmann 1990), C. cockerelli, C. rhodopus (Alcock et al. 1976), C. flavifrons (Vinson and Frankie 1988; Rêgo et al. 2006), C. flavofasciata (Vinson and Frankie 1999; Rozen et al. 2011), and C. aethiocesta Snelling (Vinson and Frankie 1988). The construction of nests with a single brood cell, although uncommon in Centris, is frequently seen in Epicharis Klug, 1807 species, such as E. nigrita Friese (Gaglianone 2005), E. bicolor Smith (Rocha-Filho et al. 2008), and E. dejeanii Lepeletier (Dec and Vivallo 2019). This type of architecture appears to be energetically inefficient when compared to a multicelled nest since females spent a lot of energy in the digging process to construct a single brood cell. However, Coville et al. (1983) suggested that this type of architecture is associated with the soil composition, which is generally sandy and easy to excavate, and the presence of natural enemies. In this sense, the construction of nests containing a single brood cell would spread the pressure of these natural enemies that have the capacity to memorize the entrance of the nests. Despite this, no natural enemies were observed visiting the nest sites during the development of the study.

This study allows understanding the structural aspects related to the nests of C. caxiensis, an important species to the maintenance of plant populations from sand dunes, dry forest, cerrado, and agrosystems. Also, it can increase the knowledge of bionomic aspects of ground-nesting Centris due to the difficulty of finding nests in natural areas.

Figure 2 Nest features of Centris caxiensis. (a) Nest with a single brood cell; (b), Unfinished nest; (c) Nest with two brood cells; (d) Brood cell: 1-sand filling tunnel; 2- nest entrance; 3-curvature in the tunnel; 4-unfinished cell; 5- central process. 

Acknowledgements

We thank Dr. José Jorge Sousa Carvalho and Mirelly Ferreira Tenório for carrying out soil analysis. The first author thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting the scholarship 134121/2019-8. This paper is part of the SIGMA project Nº21565 MN/UFRJ and the contribution number 46 from the HYMN.

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Received: June 13, 2020; Accepted: July 06, 2020

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