Print version ISSN 1519-566X
Neotrop. entomol. vol.38 no.5 Londrina Sept./Oct. 2009
ECOLOGY, BEHAVIOR AND BIONOMICS
Eufriesea violacea (Blanchard) (Hymenoptera: Apidae): an orchid Bee apparently sensitive to size reduction in forest patches
Eufriesea violacea (Blanchard) (Hymenoptera: Apidae): uma abelha das orquídeas aparentemente sensível à redução no tamanho dos fragmentos florestais
Douglas C Giangarelli; Gabriele A Freiria; Olavo P Colatreli; Karen M Suzuki; Silvia H Sofia
Depto. Biologia Geral, CCB, Univ. Estadual de Londrina, C. postal 6001, 86051-990, Londrina, PR; email@example.com
Eufriesea violacea (Blanchard) is a very seasonal euglossine species, more frequently found in the southern and southeastern regions of Brazil. A number of studies have revealed large variations in the abundance of males of this species present in Atlantic Forest remnants throughout both regions. In this paper, we report variations in the abundance of E. violacea males sampled in several forest patches of different sizes (ranging from 10 to 580 ha), and we propose that this species is possibly sensitive to the reduction in size of forest remnants. Surveys were carried out in nine forest remnants of Atlantic rainforest located in northern Paraná State, southern Brazil. Male euglossine bees were collected with an entomological net when visiting scent-baits, between 10:00 am and 1:00 pm, from October to December of 2001 and 2006. A total of 360 E. violacea males were captured in the nine forest fragments studied. The number of bees attracted to scent baits in each forest patch varied from zero to 261. A very high association (r = 0.993) was detected between the forest patch size and the visitation rate of E. violacea males at different sites, with the highest mean number of males visiting baits/sampling (43.5) being observed for bees from the largest forest remnant. Although alternative hypothesis should not be discharged for the decline in the abundance or absence of E. violacea in small forest patches, our results indicate that populations of this euglossine species need larger forest areas for existing.
Key words: Brazilian Atlantic rainforest, euglossine bee, Euglossini, bee abundance, Neotropics
Eufriesea violacea (Blanchard) é uma espécie de Euglossini bastante sazonal, de ocorrência mais frequente no Sul e Sudeste do Brasil. Vários estudos revelaram grandes variações na abundância de machos de E. violacea em remanescentes de Mata Atlântica dessas duas regiões brasileiras. Neste artigo, relatamos variações na abundância de machos de E. violacea de vários fragmentos florestais de tamanhos distintos (variando de 10 a 580 ha), e sugerimos que a espécie seja provavelmente sensível à redução no tamanho da área do fragmento florestal. As amostragens foram realizadas em nove remanescentes florestais de Mata Atlântica, localizados no Norte do Paraná, Sul do Brasil. Machos euglossíneos foram coletados com rede entomológica durante suas visitas às iscas-odores, entre 10:00h e 13:00h, de outubro a dezembro de 2001 e 2006. O total de 360 machos de E. violacea foi coletado nos fragmentos estudados. O número de abelhas atraídas às iscas em cada área variou de zero a 261 indivíduos. O tamanho do fragmento foi proporcionalmente relacionado (r = 0,993) à taxa de visitação de machos de E. violacea nas diferentes áreas, sendo que o maior número médio de machos (43,5) por amostragem foi observado para abelhas do fragmento florestal maior. Embora hipóteses alternativas para o declínio na abundância ou ausência de E. violacea em fragmentos florestais menores não devam ser descartadas, esses resultados indicam que populações de E. violacea necessitam de áreas florestais maiores para sua sobrevivência.
Palavras-chave: Floresta Atlântica, abelha euglossina, Euglossini, abundância de abelhas, neotrópico
Orchid bees (Apidae: Euglossini) are shy, fast-flying they are visitors of a large number of plant families including bees, rarely collected at flowers (Dressler 1982, Nemésio Orchidaceae (Dressler 1982, Roubik & Hanson 2004). The & Silveira 2007a), and are considered elusive pollinators group is primarily native from Mexico to northern Argentina throughout the American tropics (Cameron 2004), where (Dressler 1982, Roubik & Hanson 2004), but occurrence of euglossine bees have also been reported to USA (Minckley & Reyes 1996, Pemberton & Wheeler 2006).
There is evidence indicating that forest fragments can undergo a decline in the number of males in some euglossine species (Powell & Powell 1987, Morato 1994, Sofia & Suzuki 2004). Recently, Parra-H & Nates-Parra (2007) suggested that it is possible to determine habitat quality using data obtained from orchid bee array.
Eufriesea violacea (Blanchard) is a robust, medium-size bee (ca. 16 mm long), with a metallic integument, predominantly green with violet parts in males and violet colour in females. Considered an endemic species to the Atlantic Forest (Nemésio & Silveira 2007b), the occurrence of E. violacea has been documented mainly to the southern and southeastern regions of Brazil (Peruquetti & Campos 1997, Rebêlo & Garófalo 1991, Sofia & Suzuki 2004, Wittmann et al 1989). While females of E. violacea exhibit solitary nesting behaviour and nest in natural and man-made cavities, frequently constructing nests in aggregations (Peruquetti & Campos 1997), males are usually attracted to scent-baits of eucalyptol, vanillin and others chemicals during the wet-warm season (Wittmann et al 1989, Sofia & Suzuki 2004, Uehara & Garófalo 2006). This species has one generation per year (Wittmann et al 1989), with males usually emerging in September and females after October (Peruquetti & Campos 1997). Like other Eufriesea species, E. violacea spend most of the annual cycle as diapausing prepupae (Dressler 1982, Kimsey 1982, Uehara-Prado & Garófalo 2006).
Although several authors have usually considered species of Eufriesea as rare (e.g., Kimsey 1982, Nemésio & Silveira 2004, Nemésio 2005), a number of studies carried out in Atlantic Forest remnants in Brazil have revealed surprisingly high frequencies of males of E. violacea (Wittmann et al 1989, Sofia et al 2004), representing above 50% of the euglossine samples in these studies. This fact attracted the attention of Nemésio & Silveira (2007b), who pointed out the variation in abundance of this species in different studies (Wittmann et al 1989, Rebêlo & Garófalo 1997, Nemésio 2004, Sofia et al 2004). Comparing the euglossine fauna from three forest remnants in southern Brazil, Sofia & Suzuki (2004) detected that a reduction in fragment size negatively affected the frequency of E. violacea males, suggesting that this species could be a possible bioindicator of habitat quality.
According to Roubik (2001), population studies of bees allow for a graphic understanding of trends or possible decline in pollinator abundance, and perhaps more fundamentally, the kinds of abundance variations that can be expected. In this paper, we report the variation in the abundance of E. violacea males sampled in nine forest patches of different sizes and suggest that this species is sensitive to reduction of forest remnant size.
Material and Methods
Study sites. This study was conducted in nine forest fragments located in northern Paraná State, in southern Brazil (Fig 1). The dominant vegetation in the region is the semi-deciduous forest, a tropical seasonal forest that represents an ecosystem of the Atlantic Forest (Morellato & Haddad 2000). The local climate is classified as Cfa, humid subtropical with warm summer, with a mean annual temperature of 21ºC. The mean annual rainfall is 1,600 mm (Mendonça 2000), where rain is distributed in all the seasons, with a decline in rainfall in the winter (June, July and August).
Of the nine sites studied, five constitute areas on privately owned ranches, showing different sizes, as follows: two large forest fragments (> 100 ha), named sites A and B; one medium-size fragment (86 ha), site C; and two small forest fragments (10-15 ha), corresponding to sites D and E (Table 1). These fragments are areas where a minimum of 20% of the land must be preserved as wooded areas on private properties, established by a Brazilian Federal law. The vegetation of these fragments has been selectively logged for many decades.
Two forest fragments constitute governmental reserves: Parque Estadual Mata dos Godoy - GF (site F) and Parque Municipal Arthur Thomas (site G). GF is a governmental reserve that includes an area of 580 ha of very well preserved native vegetation. It has a wooded area that is more or less connected with other native forest fragments situated outside the protected area of the park, constituting a forest fragment with a total area of around 2800 ha (Sofia et al 2005). Parque Municipal Arthur Thomas consists of 66 ha and is situated within the urban area of Londrina, a city of around 500,000 inhabitants. The last two forest patches are also located inside an urban area: one of them corresponding to 13.4 ha is situated at the campus of the Universidade Estadual de Londrina (site H) and a forest patch of around 18 ha surrounding an urban stream (site I) (Fig 1 and Table 1). All forest fragments exhibit signs of past and present anthropogenic disturbance and most part of them are surrounded by crop and pasture areas.
Methods and analysis. Male euglossine bees were collected with an entomological net after they were attracted to scent-baits of eugenol, eucalyptol and vanillin, between 10:00 am and 1:00 pm (2h of sampling/site), from November to December of 2001 and from October to December of 2006, which is the period of higher activity of E. violacea in the northern part of Paraná State (Sofia & Suzuki 2004, Sofia et al 2004).
To make the census more effective and minimize sampling error caused by weather, only clear and warm days were chosen for samplings (Powell & Powell 1987). The baits were placed in the shade, hung on strings tied to vegetation in the border of the fragment. Chemicals were replenished on the baits every half hour, in order to maintain a high and homogeneous attractiveness (Uehara-Prado & Garófalo 2006). Only one site per forest fragment was established for samplings. After being collected at the baits, the easily identifiable E. violacea males were marked with a dot of paint (Posca: Mitsubishi Pencil Co., Ltd.) on the thorax and released. The procedure of marking the bees was employed to avoid counting the same bee more than once. Only a few individuals of E. violacea were collected and voucher specimens were deposited at the Zoology Museum of the Universidade Estadual de Londrina (MZUEL).
Visitation rate (mean number of bees/sampling) was used to compare possible variation in E. violacea abundance in different forest patches. The statistical analyses included the chi-square test (one-sample) and the Kruskall-Wallis test (which was based on the median values of number of males attracted to chemical baits) (Siegel & Castellan 1988). Also, the association between mean number of bees captured per sampling and fragment size data was examined for significance using a correlation coefficient test. All values were considered significantly different if P < 0.05.
Results and Discussion
A total of 360 E. violacea males were captured in the nine forest fragments studied. The number of bees attracted to scent baits in each forest patch varied from zero (sites D, H and I) to 261 at site F, which showed the highest mean number of males visiting baits/sampling (43.5) amongst all forest fragments (Table 1). Despite variation in the number of samplings per area (ranging from n = 3 to n = 6), there was an obvious wide variation between some forest fragments in the number of individuals collected (χ2 = 202. 144, P < 0.0001; H = 31.380, P < 0.001, df = 8). The three larger forest fragments (A, B and F) showed some variation in the number of bees attracted to scent baits among the different samplings (Fig 2). However, a high correlation (r = 0.993) was detected between forest patch size and visitation rate of E. violacea males surveyed at baits at different sites (Fig 3).
Euglossine bees have been extensively recognized as strong fliers, especially the larger euglossine species (Janzen 1971, Dressler 1982). As a medium-sized and robust bee E.violacea is potentially able to fly long distances. However, in a fragmented landscape, the matrix has strong infl uence on fragmented populations, such as precluding the movement of some species (Laurence et al 2002). On the other hand, the movement of euglossine bees between forest fragments, crossing open areas, has been reported by different authors (Raw 1989, Murren 2002, Tonhasca et al 2003).
In the present study, it is possible that the geographic proximity of site F (the largest and best preserved site surveyed) favours small forest patches located in the vicinity, such as sites C and E, located respectively 1.3 km and 4.2 km from the site F fragment. Thus, site F could be functionally acting as a "mainland" and a source of visitors to small fragments located in close proximity (Nol et al 2005). According to Castro & Fernandes (2004), although large forest fragments may be a potential source of colonizers and/or immigrants, these events should be much more frequent among fragments due to the much shorter
distances that separate them from each other. Assuming that E. violacea from a large forest fragment (site F) are moving among small fragments in the vicinity, it means that the well-preserved conditions of this forest patch, compared other eight fragments surveyed, are not preventing E. violacea males to exploit other forest patches. It has been suggested that the density of male euglossine bees may be higher at sites with greater resource availability, but the local concentration of resources does not prevent bees to access to all nearby areas (Tonhasca et al 2002a). Also, Murren (2002) attributed the reproductive success of island populations of Catasetum viridiflavum Hooker (Asparagales, Orchidaceae), a euglossine bee-pollinated orchid species, to mainland populations of Eulaema cingulata (Fabricius) (Hymenoptera, Apidae), which were found to fly across water to reach bait traps available on the island. According to this author, males of E. cingulata are probably not island residents, but rather transient visitors from larger continuous forest areas.
Assessing the genetic structure of E. violocea males in three forest remnants of the Atlantic Forest in the study region of the current work, Sofia et al (2005) reported the occurrence of a single panmitic population among three forest fragments studied, attributing this finding to reduced history of fragmentation in the region (around 80 years) and to the potential ability of males to move among nearby forest patches. However, to better understand the foraging behaviour of E. violacea males, concerning movement between forest patches, future studies using marking and recapture methods must be considered (Raw 1989, Murren 2002, Tonhasca et al 2003).
In opposition to the above, the short distance between sites D and F was not sufficient to explain the absence of E.violacea at site D, which is also located close (around 2.5 km away) to the large fragment, site F (Fig 1). However, in a fragment containing a small population of inhabiting bees or occasionally visited by bees from the "neighbourhood", the limited number of samplings per site could explain the failure in surveying bees at baits, but other fragmentation effects on local fauna cannot be ignored in this case.
Also, the high association detected between forest fragment size and visitation rate of euglossine males suggests that it is a potential area-sensitive species. Area-sensitive species by definition are species that prefer to breed in large tracts of forest; however, species may still be considered area-sensitive if their probability of occurrence increases with habitat patch size (Fraser & Stutchbury 2004). Even thought population dynamics in unprotected habitats are less predictable or more compromised by exotic organisms (Roubik 2001), the abundance pattern observed for E.violacea in the present study makes this euglossine bee a possible area-sensitive species, corroborating the idea that euglossine bees are possible bioindicator of quality of environmental conditions (Peruquetti et al 1999, Tonhasca et al 2002b, Parra & Nates-Parra 2007).
While forest fragmentation is associated with population decline of euglossine bees (Powell & Powell 1987, Morato 1994, Sofia & Suzuki 2004), a higher euglossine bee abundance in 10 ha and 100 ha fragments compared to a continuous forest is reported in the literature, with a significant reduction in euglossine bees visiting baits occurring only in very small forest patches (1 ha) (Becker et al 1991). In a very long-term study of orchid-bees carried out in a protected tropical moist forest in Panama, Roubik (2001) demonstrated that even though populations of bees varied considerably between years, no decline in euglossine bees in the study area occurred over 20 years. They concluded that long-term studies substantially clarified results taken on a small temporal scale.
An alternative explanation for the absence or low number of males of E. violacea visiting baits at some forest patches may be the availability of alternative scent sources in these areas, such as a high concentration of resources (displayed as "hot spots") (Armbruster 1993), reducing the chance of bees being attracted to baits. As males do not collect fragrances everyday, but do feed frequently, it seems logical to suppose nectar distribution as a main, but not sole, causal factor of capturing frequencies (Otero & Sandino 2003).
Our results indicate that populations of E. violacea need larger forest areas for existing. Therefore, the absence of E. violacea in some forest patches could indicate a high degree of disturbance, demonstrating the need for their better management. It is worth noting that in northern Paraná State these forest patches are among the last remains of the Brazilian Atlantic rainforest and as such probable reservoirs of local biodiversity.
To Dr Solange C Augusto who provided very helpful comments on manuscript draft and to Dr A Leyva who provided English editing of the manuscript. The authors also thank IBAMA (Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis), IAP (Instituto Ambiental do Paraná) and the owners of private forest areas for permission to collect bees. This study was supported by grants from Fundação O Boticário de Proteção à Natureza (FBPN), Fundação Araucária and Klabin S.A. D.C. Giangarelli and G.A. Freiria received fellowships from PIBIC-CNPq and PROPPG-UEL. The authors are also grateful to the anonymous referees, which deeply contributed with valuable comments and suggestions.
Armbruster W S (1993) Within-habitat heterogeneity in baiting samples of male euglossine bees: possible causes and implications. Biotropica 25: 122-128. [ Links ]
Becker P, Moure J S, Peralta F J A (1991) More about Euglossine bees in Amazonian forest fragments. Biotropica 23: 586-591. [ Links ]
Cameron S A (2004) Phylogeny and biology of Neotropical orchid bees (Euglossini). Ann Rev Entomol 49: 377-404. [ Links ]
Castro E V, Fernandes F A S (2004) Determinants of differential extinction vulnerabilities of small mammals in Atlantic forest fragments in Brazil. Biol Conserv 119: 73-80. [ Links ]
Dressler R L (1982) Biology of orchid bees (Euglossini). Annu Rev Ecol Syst 13: 373-394. [ Links ]
Fraser G S, Stutchbury B J M (2004) Area-sensitive forest birds move extensively among forest patches. Biol Conserv 118: 377-387. [ Links ]
Janzen D H (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171: 203-204. [ Links ]
Kimsey L S (1982) Systematics of bees of the genus Eufriesea. Univ California Publ Entomol 95: 1-97. [ Links ]
Laurence W F, Lovejoy T E, Vasconcellos H L, Bruna E M, Didham R K, Stouffer P C Gascon C, Bierregaard R O, Laurence S G, Sampaio E (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv Biol 16: 605-618. [ Links ]
Mendonça F A (2000) A tipologia climática: gênese, características e tendências, p.21-62. In Stipp N M F (ed) Macrozoneamento ambiental da bacia hidrográfica do rio Tibagi (PR). Londrina, Editora UEL, 196p. [ Links ]
Minckley R L, Reyes S G (1996) Capture of the orchid bee, Eulaema polychroma (Friese) (Apidae: Euglossini) in Arizona, with notes on northern distributions of other Mesoamerican bees. J Kansas Entomol Soc 69: 102-104. [ Links ]
Morato E F (1994) Abundância e riqueza de machos de Euglossini (Hymenoptera: Apidae) em mata de terra firme e áreas de derrubada, nas vizinhanças de Manaus (Brasil). Bol Mus Para Emilio Goeldi ser Zool 10: 95-105. [ Links ]
Morellato L P C, Haddad C F B (2000) Introduction: the Brazilian Atlantic Forest. Biotropica 32: 786-792. [ Links ]
Murren C J (2002) Effects of habitat fragmentation on pollination: pollinators, pollinia viability and reproductive success. J Ecol 90: 100-107. [ Links ]
Nemésio A (2004) Composição e riqueza em espécies e abundância de machos de Euglossina (Hymenoptera: Apidae: Apini) de remanescentes florestais de Mata Atlântica no estado de Minas Gerais. Dissertação de mestrado, Universidade Federal de Minas Gerais, Belo Horizonte, xii + 153p. [ Links ]
Nemésio A (2005) Description of the male Eufriesea nigrohirta (Friese, 1899) (Hymenoptera: Apidae: Euglossina) with comments on the holotype, species biology and distribution. Lundiana 6: 41-45. [ Links ]
Nemésio A, Silveira, F A (2004) Biogeographic notes on rare species of Euglossina (Hymenoptera: Apidae: Apini) occurring in the Brazilian Atlantic Rain Forest. Neotrop Entomol 33: 117-120. [ Links ]
Nemésio A, Silveira F A (2007a) Orchid bee fauna (Hymenoptera: Apidae: Euglossina) of Atlantic Forest fragments inside an urban area in southeastern Brazil. Neotrop Entomol 36: 186-191. [ Links ]
Nemésio A, Silveira F A (2007b) Diversity and distribution of orchid bees (Hymenoptera: Apidae) with a revised checklist of species. Neotrop Entomol 36: 874-888. [ Links ]
Nol E, Francis C M, Burke D M (2005) Using distance from putative source woodlots to predict occurrence of forest birds in putative sinks. Conserv Biol 19: 836-844. [ Links ]
Otero J T Sandino J C (2003) Capture rates of male euglossine bees across a human intervention gradient, Chocó Region, Colombia. Biotropica 35: 520-529. [ Links ]
Parra-H A, Nates-Parra G (2007) Variación de la comunidad de abejas de las orquídeas (Hymenoptera: Apidae) en tres ambientes perturbados del piedemonte llanero colombiano. Rev Biol Trop 55: 931-941. [ Links ]
Pemberton R W, Wheeeler G S (2006) Orchid bees don't need orchids: evidence from the naturalization of an orchid bee in Florida. Ecology 87: 1995-2001. [ Links ]
Peruquetti R C, Campos L A O (1997) Aspectos da biologia de Euplusia violacea (Blanchard) (Hymenoptera, Apidae, Euglossini). Rev Bras Zool 14: 91-97. [ Links ]
Peruquetti R C, Campos L A O, Coelho C D P, Abrantes C V M, Lisboa L C O (1999) Abelhas Euglossini (Apidae) de áreas de Mata Atlântica: abundância, riqueza e aspectos biológicos. Rev Bras Zool 16: 101-118. [ Links ]
Powell A H, Powell G N N (1987) Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica 19: 176-179. [ Links ]
Raw A (1989) The dispersal of euglossine bees between isolated patches of eastern Brazilian wet forest (Hymenoptera, Apidae). Rev Bras Entomol 33: 103-107. [ Links ]
Rebêlo J M M, Garófalo C A (1991) Diversidade e sazonalidade de machos de Euglossini (Hymenoptera, Apidae) e preferências por iscas-odores em um fragmento de floresta no Sudeste do Brasil. Rev Bras Biol 51: 787-799. [ Links ]
Rebêlo J M M, Garófalo C A (1997) Comunidades de machos de Euglossini (Hymenoptera: Apidae) em matas semidecíduas do nordeste do estado de São Paulo. An Soc Entomol Brasil 26: 243-255. [ Links ]
Roubik D W, Hanson P H (2004) Abejas de orquídeas de la América tropical. Biología y guía de campo. Heredia, INBio Press, 370p. [ Links ]
Siegel S, Castellan J D (1988) Nonparametric statistics for behavioural sciences. New York, McGraw-Hill Company, 399p. [ Links ]
Sofia S H, Paula F M, Santos A M, Almeida F S, Sodré L M K (2005) Genetic structure analysis of Eufriesea violacea (Hymenoptera, Apidae) populations from southern Brazilian Atlantic Forest remnants. Gen Mol Biol 28: 479-484. [ Links ]
Sofia S H, Santos A M, Silva C R M (2004) Euglossine bees (Hymenoptera, Apidae) in a remnant of Atlantic Forest in Paraná State, Brazil. Iheringia 94: 217-222. [ Links ]
Sofia S H, Suzuki K M (2004) Comunidades de abelhas Euglossina (Hymenoptera, Apidae) em fragmentos florestais no Sul do Brasil. Neotrop Entomol 33: 693-702. [ Links ]
Tonhasca Jr A, Albuquerque G S, Blackmer J L (2003) Dispersal of euglossine bees between fragments of the Brazilian Atlantic Forest. J Trop Ecol 19: 99-102. [ Links ]
Tonhasca Jr A, Blackmer J L, Albuquerque G S (2002a) Within-heterogeneity of euglossine bee populations: a re-evaluation of the evidence. J Trop Ecol 18: 929-933. [ Links ]
Tonhasca Jr A, Blackmer J L, Albuquerque G S (2002b) Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic Forest. Biotropica 34: 416-422. [ Links ]
Uehara-Prado M, Garófalo C A (2006) Small-scale elevational variation in the abundance of Eufriesea violacea (Blanchard) (Hymenoptera: Apidae). Neotrop Entomol 35: 446-451. [ Links ]
Wittmann D, Radtke R, Blochtein B (1989) Seasonality and seasonal changes in preferences for scent baits in Euplusia violacea in Rio Grande do Sul/Brazil. Entomol Gen 14: 217-221. [ Links ]
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