First report of a nest of Ceratina (Ceratinula) fioreseana Oliveira (Hymenoptera: Apidae)

Primeiro registro de um ninho de Ceratina (Ceratinula) fioreseana Oliveira (Hymenoptera: Apidae)

ABSTRACT.

We provide herein the first report of a nest of Ceratina (Ceratinula) fioreseana Oliveira, 2020, a species that was recently described for the Cerrado domain. The nest was collected in a Passiflora edulis Sims (Passifloraceae) plantation in Minas Gerais State, Brazil and was built in a trap nest, a dry petiole of Cecropia pachystachya Trécul (Urticaceae). Within the nest there was a living female and a brood cell without partition containing a pupa, whose adult female emerged 28 days after pupation. Pollen analysis revealed the dominance of Emilia fosbergii Nicolson (Asteraceae) pollen grains, a weed recorded a few meters from the nest. The record of an adult female within the nest with a pupa and the absence of nest partition might suggest social behavior in this bee species.

KEYWORDS.
Brazilian Savanna; Ceratinula ; pollen; trap nest

RESUMO.

Primeiro registro de um ninho de Ceratina (Ceratinula) fioreseana Oliveira (Hymenoptera: Apidae). É fornecido o primeiro registro de um ninho de Ceratina (Ceratinula) fioreseana Oliveira, 2020, uma espécie que foi recentemente descrita para o domínio do Cerrado. O ninho foi coletado em um cultivo de Passiflora edulis Sims (Passifloraceae) no estado de Minas Gerais, Brasil e foi construído em um ninho-armadilha, um pecíolo seco de Cecropia pachystachya Trécul (Urticaceae). Dentro do ninho havia uma fêmea e uma célula de cria sem partição contendo uma pupa, a qual a fêmea adulta emergiu 28 dias após pupação. A análise polínica revelou a dominância de grãos de pólen de Emilia fosbergii Nicolson (Asteraceae), uma espécie ruderal observada a poucos metros do ninho. O registro de uma fêmea adulta dentro do ninho juntamente com uma pupa e a ausência de partição na célula de cria podem sugerir comportamento social nesta espécie de abelha.

PALAVRAS-CHAVE.
Cerrado; Ceratinula ; ninho-armadilha; pólen

Ceratina Latreille, 1802 (Apidae) is represented by approximately 380 species (Oliveira et al., 2020; Ascher & Pickering, 2022; Moure & Melo, 2022) classified in 23 subgenera with a worldwide distribution but absent in Ireland, Iceland, New Zealand, and some small islands (Michener, 2007; Ascher & Pickering, 2022). Females nest in pithy twigs or dead branches where they excavate a burrow and construct unlined brood cells (Michener, 2007). Despite the high diversity found in the Neotropical region, more than 100 species recorded (Moure & Melo, 2022), most of the studies on the nest biology of Ceratina species were conducted in Asia, Australia, Europe, and North America (Sakagami & Maeta, 1987; Malaipan & Orostrirat, 1992; Maeta & Sakagami, 1995; Rehan et al., 2009; Rehan & Richards, 2010; Vickruck et al., 2011; Ali et al., 2016; Kaliaperumal, 2019; Mikát et al., 2019; Udayakumar & Shivalingaswamy, 2019; Mikát et al., 2021, 2022; Oppenheimer & Rehan, 2021; Rauf et al., 2022). In contrast, the information on nests of Neotropical Ceratina species is still scarce (Schrottky, 1914; Michener & Eickwort, 1966; Sakagami & Laroca, 1971; Gonzalez et al., 2004; Rehan et al., 2015).

Here, it is reported for the first time a nest of Ceratina (Ceratinula) fioreseanaOliveira, 2020 constructed in a trap nest in Minas Gerais State, south-eastern Brazil. This species was recently described from Goiás State from an area distant about 500 km from our study site (Oliveira et al., 2020). It belongs to the subgenus C. (Ceratinula) Moure, 1941, which comprises 40 minute species of up to 6 mm distributed from southern United States to northern Argentina (Oliveira et al., 2020; Ascher & Pickering, 2022; Moure & Melo, 2022). The records of nest biology or mentions of built nests of C. (Ceratinula) species were documented by Schrottky (1914) for C. gomphrenae Schrottky, 1909 in Paraguay, Michener & Eickwort (1966) for C. rectangulifera Schwarz & Michener, 1954 in Costa Rica, Sakagami & Laroca (1971) for C. muelleri Friese, 1910 and C. oxalidis Schrottky, 1907 in southern Brazil, and Rehan et al. (2015) for four species from Panama.

MATERIAL AND METHODS

The nest was collected in a farm (18°34’10.1”S, 48°01’06.2”W) located north-eastern the city of Araguari, Minas Gerais State, south-eastern Brazil. The area lies at the Brazilian Savanna domain and consist of a small familiar property where 0.8 hectares were occupied by a plantation of yellow passionfruit, Passiflora edulis Sims (Passifloraceae), which were replaced with soybean, Glycine max (L.) Merr (Fabaceae), by the end of 2021. The area was visited once a month since August 2019 to sample trap-nesting solitary bees and wasps (Rocha-Filho et al., in prep.). The sampling station consisted of a wooden frame (30 cm height, 30 cm width, 20 cm depth) attached to a tree 1.5 m above ground and located in front of the passionfruit crop. Twenty bamboo canes, Bambusa vulgaris Schrad. (Poaceae), from 1.4 to 2.4 cm diameter and 15 cm length were inserted horizontally in metal screens screwed to the wooden frame and were used to attract nesting females of Xylocopa (Neoxylocopa) frontalis (Olivier, 1789) (Apidae). Additionally, five PVC tubes (20 cm length and 10 cm diameter) containing each 24 bamboo canes (0.5 to 2 cm diameter and 9 to 25 cm length) were attached below the wooden frame to attract nesting females of trap-nesting wasps and bees. Beside each side of the wooden frame, two dry petioles of Cecropia pachystachya Trécul (Urticaceae), cut straight in both ends, were attached with nails to attract nesting females of Ceratina species.

On November 10^th, 2021, one dry petiole containing a small hole at its border was collected and taken to the laboratory for the emergence of adults. The 23.4 cm-length and 0.59 cm-diameter petiole was carefully open the next day with a cutter to check if there was a Ceratina nest or if it was occupied by ants such as Pseudomyrmex gracilis (Fabricius, 1804) (Formicidae), which can use this kind of substrate to nest (Rocha-Filho et al., in prep.). The emerging bees were identified with the key provided by Oliveira et al. (2020) and are deposited as voucher specimens at the collection of Laboratório de Ecologia e Comportamento de Abelhas (LECA) of Universidade Federal de Uberlândia.

The faeces found within the nest were collected, stored in 70% ethanol, and then transferred to absolute acetic acid for at least 24 hours to be acetolysed according to the protocol described by Erdtman (1960). The acetolysed pollen grains were glued with small glycerine gelatine cubes and placed on microscopic slides.

RESULTS

The nest contained a sinuous tunnel of 9.1 cm length (Fig. 1) and a living female, which tried to hide at the bottom of the nest, where there was a pupa surrounded by faeces. No signs of nest partitions were observed. The adult female (Fig. 2) left the nest on November 12^th. Another female (Fig. 3) emerged from the nest on December 7^th. Three pollen samples were used for identification and counting of all grains found in the microscopic slides. A total of 1,057 pollen grains were counted and 95.27% belonged to the weed species Emilia fosbergii Nicolson (Asteraceae) (Fig. 4), which had some individuals located one to three meters from the sampling station. Other pollen types, such as P. edulis, type Bidens (Asteraceae), and Mesosphaerum suaveolens (L.) Kuntze (Lamiaceae) accounted 1.42%, 1.42%, and 0.76%, respectively, while other four types represented less than 1.5% of the total amount counted.

Figs 1-4:
1, Dry petiole of Cecropia pachystachya used as nesting substrate by a female of Ceratina fioreseana; 2, living female found in the nest; 3, emerging female; 4, polar view of Emilia fosbergii pollen grain. Figs 2, 3, Scale bars: 2 mm; 4, Scale bar: 50 μm.

DISCUSSION

Most of the studied nests of Ceratina species were observed on natural substrates such as pithy stems or twigs (Rehan & Richards, 2010; Rehan et al., 2015; Ali et al., 2016; Kaliaperumal, 2019; Mikát et al., 2019; Udayakumar & Shivalingaswamy, 2019; Oppenheimer & Rehan, 2021). However, Mikát et al. (2021) used sheaves of cut twigs attached to rods and fixed to the ground as artificial substrates for Ceratina (Euceratina) nigrolabiata Friese, 1896 in Czechia. Rauf et al. (2022) obtained nests of Ceratina (Pithitis) smaragdula (Fabricius, 1787) built in bamboo canes, a cardboard tube and a log of Ziziphus mauritiana Lam. (Rhamnaceae) in Pakistan. In Japan, Sakagami & Maeta (1987) employed glass tubes in which it was inserted the pithy core of Kerria japonica (L.) DC. (Rosaceae) that had already been partly excavated by a female. Dry petioles of C. pachystachya used herein are commonly found in different Brazilian biomes and have been demonstrated to be a useful artificial substrate for nesting Ceratina females, both larger species such as Ceratina (Crewella) maculifrons Smith, 1854 (Rocha-Filho et al., 2021) and minute as C. fioreseana. We also encourage the use of dead branches of Rosa chinensis Jacq. (Rosaceae) as trap nests to attract nesting females since nests of Ceratina species are often recorded in such substrates and this plant species is ubiquitous in several gardens in Brazil.

Differently from what was observed in other C. (Ceratinula) spp. (Michener & Eickwort, 1966; Sakagami & Laroca, 1971; Rehan et al., 2015), there was no evidence of partition in the C. fioreseana nest. According to Michener & Eickwort (1966), nest partitions of C. rectangulifera were thin but resistant, composed of bits of pith compactly cemented together. Possibly, the soft pith of C. pachystachya petioles may not be hard enough to build nest partitions, which could be reinforced by the fact that no partitions were detected in nests of C. maculifrons constructed in the same nesting substrate (L. C. Rocha-Filho, pers. comm.). The lack of partitions can be due to failure in constructing them, when the last brood cell is not sealed and the immature is guarded by the mother, as observed in C. (Rhysoceratina) volitans Schrottky, 1907 (Sakagami & Laroca, 1971). Another cause for the absence of partitions is later removal by the mother, which is often observed between brood cells containing old larvae or pupae, as noted in one nest of C. oxalidis containing older immature (Sakagami & Laroca, 1971).

The C. fioreseana growth lasted longer than what was reported by Michener & Eickwort (1966) for C. rectangulifera. The period between pupation to the emergence of adult took approximately 11 days for C. rectangulifera while the C. fioreseana female emerged 28 days since the nest collection in the field, when it was in pupal stage. This longer period of pupation was also observed in C. volitans in Brazil, which was estimated as 28 to 30 days (Sakagami & Laroca, 1971). The discrepancy of developmental period between the two C. (Ceratinula) species could be related to differences of climate variables between the studied areas.

The lone brood cell containing a pupa found in the C. fioreseana nest was also observed in one of the seven nests of C. rectangulifera, but the latter had no adult bee inside the nest (Michener & Eickwort, 1966). However, the authors found one nest with one cell containing a large larva and a living adult in the external part of the nest tunnel. Because of this small number of brood cells observed in the nests of C. rectangulifera, Michener & Eickwort (1966) conjectured that a nesting female must construct two or more nests. It could be wondered the same hypothesis for C. fioreseana because of the single brood cell found in the nest, but other three dry petioles were available in the sampling station and no signs of excavation were observed on them.

Only one adult female was found in the C. fioreseana nest. On the other hand, Sakagami & Laroca (1971) observed two females in one nest of C. oxalidis containing old brood cells and it was assumed that they were elder sister of the pupa and larva found within that nest. The authors also found two nests of this species without brood cells, but only two females with swollen ovaries in one of them and six individuals (three females and three males) in the other nest. Ceratina oxalidis has an inactive period in the year and it was presumed that both nests were on stage of hibernation (Sakagami & Laroca, 1971). Rehan et al. (2015) found nests with two females in three of the four C. (Ceratinula) studied species but always in a much lower proportion when compared to nests with a single female. The authors observed reproductive division of labor in these multifemale nests, in which the larger female was a reproductive forager and the smaller female a non-reproductive guard, providing thus the first evidence for social behavior of three C. (Ceratinula) species.

One important aspect to be highlighted herein is the putative social behavior of C. fioreseana. Despite the record of only one nest, the fact that an adult female (possibly the mother) was inside the tunnel with a pupa and the absence of nest partition indicates that this species is not solitary, as also observed in other Ceratina species belonging to different subgenera (Rehan et al., 2009, 2015; Rehan & Richards, 2010; Oppenheimer & Rehan, 2021). Our data suggest that the living female in the nest may be long-lived and performing nest protection and maternal care, which are recurrent characteristics of several Ceratina species (Rehan et al., 2009).

The high prevalence of E. fosbergii pollen grains found in the residual content of the C. fioreseana nest suggests that this bee species might be oligolectic, but a single sample would not be appropriate to conclude about its diet. The C. fioreseana specimens studied and described by Oliveira et al. (2020) were collected on flowers of peppermint, Mentha piperita L. (Lamiaceae), which could be either a pollen and/or a nectar source. Flower records of eight C. (Ceratinula) species in São Paulo State showed associations with 34 plant species belonging to 22 families, which indicates that some of these species could be polylectic given the high number of species visited (Imperatriz-Fonseca et al., 2011). Indeed, C. oxalidis females containing pollen loads were collected on several flowers belonging to various plant species of different families in southern Brazil (Sakagami & Laroca, 1971). Additionally, in five nests of C. maculifrons collected in an urban area, the residual content had pollen from four plant families, confirming the polylecty of this bee species (Müller & Kuhlmann, 2008; Rocha-Filho et al., 2021). Hence, it is plausible to assume that the use of E. fosbergii pollen for brood cell provisioning may be associated to the very short distance of plant individuals from the nest, likewise P. edulis and M. suaveolens, which were located one to three meters away from the sampling station, ensuring the host female short-distance flights for foraging.

Acknowledgments.

The authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for providing scholarships to the first and third authors, to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the scholarship provided to the second author and by the financial support from project Programa de Pesquisas Ecológicas de Longa Duração - Triângulo Mineiro e Sudeste de Goiás (PELD/TMSG) (441225/2016-0 and 441142/2020-6). We also would like to thank Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) (APQ 04815-17) for the financial support provided and the owners of the farm that allowed our fieldwork in the area.

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Publication Dates

• Publication in this collection
  12 Dec 2022
• Date of issue
  2022

History

• Received
  28 May 2022
• Accepted
  10 Oct 2022