Long-term ecology of euglossine orchid-bees (Apidae: Euglossini) in Panama

Summary Abundance patterns during 6–7 years and orchid visitation were determined for 51 species of the 57 local euglossine bees. Male bees were counted at 3 chemical attractants presented in the same manner each month. Sites were separated by 75 km but included wet Atlantic forest at 500 m elevation, moist forest at 180 m near Barro Colorado Island, and cloud forest at 900 m near the Pacific ocean. 1. From 15 to 30 euglossine species of 4 genera were active in each month and site; monthly species number and general bee abundance were positively correlated. Many species had 3 annual abundance peaks (range 1–4) and were active throughout the year, but peak annual abundances rarely occurred during late wet or early dry seasons. In contrast, Eufriesea generally were present as adults only 1–2 months in a year. 2. Euglossine populations were exceptionally stable. Species at each site were more stable than any known insect population, and stability and abundance were positively associated. However, year-to-year population stability and the degree of seasonality were not correlated. Among the three sites, the more diverse (species rich) bee assemblages displayed lower stability; these were the wetter and upland sites. 3. The most abundant bees visited more orchid species. Eg. and El. each visited and average of 4 orchid species (range 0–13); Ex. and Ef. visited 0–3. Stable populations did not visit more or fewer orchid species than did unstable populations. 4. Less than 68% of species at each site visited orchid flowers; less than a few dozen of the 100–800 bees counted in a day carried orchid pollinaria. Over 20% of the euglossine species never were seen with pollinaria at any site and probably seldom visit orchids in central Panama. 5. Most bee species visited 1 or no fragrance orchids in a given habitat. Orchids tended to utilize common pollinators that seldom included more than 1 species, and they utilized stable or unstable, seasonal or aseasonal bees. However, the most stable and abundant bee, Eg. imperialis, rarely pollinated orchids; fewer than 10 of ca. 20000 bees carried pollinaria. 6. Orchids may interact primarily with discrete seasonal bee population peaks-probably the emerging adults. Although specialized orchid preferences are implicated for species that visit few or no local orchids but pollinate other species and carry pollinaria in other areas, euglossine bees do not need orchids to survive or reproduce.     

Diploid Male Frequencies in Colombian Populations of Euglossine Bees

Some studies have recently reported high diploid male frequencies in euglossine bees indicating possible population declines. We estimated the genetic variability and frequency of males that are diploid in five Colombian species of euglossine bees using allozyme markers. Expected heterozygosities ranged from 0.10 to 0.23. Diploid males were found in three species with frequencies ranging from 8 to 32 percent. Our results suggest that some species are more susceptible to environmental changes and anthropogenic pressure.     

Occurrence of Aglae caerulea Lepeletier & Serville (Hymenoptera: Apidae: Euglossini) in the Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil

In a study conducted in the gallery forest of the Vale doVeu de Noiva in the Parque Nacional da Chapada dos Guimar?es, Mato Grosso state, chemical baits were used to attract and sample male orchid bees. From September 2003 to July 2005, male euglossine bees were captured monthly, from 8:00 a.m. to 4:00 p.m. as they arrived at the baits. Of the 264 males captured, eight males belonged to Aglae caerulea Lepeletier & Serville, a cleptoparasitic euglossine species that presumably occurred only in the Amazon basin. Therefore, the occurrence of A. caerulea in this study area extends its geographical distribution range by approximately 2,400 km southwards in South America, as it is now recorded in both the Amazon and Platina basins.     

Diversity and distribution of orchid bees (Hymenoptera: Apidae) with a revised checklist of species

The aim of this study was to investigate the diversity and distribution patterns of orchid bees (Euglossina). Cluster and correlation analyses were applied to data extracted from 28 orchid-bee surveys throughout the Neotropical Region. The 28 sampling sites were grouped in three main biogeographic areas that roughly correspond to the Amazonian Basin, the Atlantic Forest and Central America. These three regions, as well as subregions within each of them, correspond approximately to biogeographic components identified through phylogeny-based analyses for other bees and organisms. The Amazonian Forest as a whole has the richest fauna and the highest levels of endemism. The Atlantic Forest, on the other hand, showed the poorest fauna and the lowest levels of endemism. However, a major neotropical biome, in which orchid bees are known to occur, has not been sampled yet, the savanna-like cerrado. At least 30% of the species are endemic to each biome. An updated checklist of the species of Euglossina is provided.     

CONSERVATION GENETICS OF NEOTROPICAL POLLINATORS REVISITED: MICROSATELLITE ANALYSIS SUGGESTS THAT DIPLOID MALES ARE RARE IN ORCHID BEES

Allozyme analyses have suggested that Neotropical orchid bee (Euglossini) pollinators are vulnerable because of putative high frequencies of diploid males, a result of loss of sex allele diversity in small hymenopteran populations with single locus complementary sex determination. Our analysis of 1010 males from 27 species of euglossine bees sampled across the Neotropics at 2–11 polymorphic microsatellite loci revealed only five diploid males at an overall frequency of 0.005 (95% CIs 0.002–0.010); errors through genetic nondetection of diploid males were likely small. In contrast to allozyme‐based studies, we detected very weak or insignificant population genetic structure, even for a pair of populations >500 km apart, possibly accounting for low diploid male frequencies. Technical flaws in previous allozyme‐based analyses have probably led to considerable overestimation of diploid male production in orchid bees. Other factors may have a more immediate impact on population persistence than the genetic load imposed by diploid males on these important Neotropical pollinators.     

EUGLOSSINE BEE POLLINATION OF THE ORCHID,COCHLEANTHES LIPSCOMBIAE: A FOOD SOURCE MIMIC

Cochleanthes lipscombiae is pollinated by large male and female euglossine bees. The flowers lack pollinator rewards, but attract bees searching for nectar. The euglossines extend their long tongues and crawl into the gullet-flower. The bees probe the back-swept lateral sepals for nectar. Pollination occurs as a pollinarium laden bee backs out, deposits pollinia on the stigma, and obtains a new pollinarium load by dislodging the anther. Some related orchid species have similar morphological characteristics as those essential to the pollination mechanism of C. lipscombiae. These features may have taxonomic significance at the generic level. Cochleanthes lipscombiae may be a floral mimic of a sympatric legume, but may also receive exploratory visits by bees searching for food resources. The latter may be young, recently emerged naive bees, or individuals seeking new nectar hosts during a period of rapid host species turnover.     

Specificity and mutual dependency of the orchid-euglossine bee interaction

Seasonal and geographic relationships, and host pollinator specificities are examined for indications of interdependency in the orchid-euglossine bee interaction. The orchids are dependent on the bees for pollination, and their flowering seasonality corresponds well with peak activity of their pollinators. However, there is little evidence that the bees are dependent on these fragrance hosts. The orchids tap the majority of euglossine species and individuals for pollinator services during any given season, but most of those bee species that temporarily lack orchid fragrance hosts persist in the area, continually emerge from nests, and seek floral fragrance compounds. Pollinator specificity occurs in less than half of the orchids, and host specificity is rare. Geographic distributions of nearly all orchid-pollinator pairs are not mutually inclusive. Moreover, nearly a third of the local male euglossine bee species censused are not pollinators of any fragrance orchids in the area. Local alternative fragrance sources occur. The orchid-male euglossine bee interaction does not appear to represent a mutually obligatory relationship. The orchids may have exploited a preexisting behavioural phenomenon of the bees, and reciprocal evolutionary responses may not have occurred.     

Long Tongues and Loose Niches: Evolution of Euglossine Bees and Their Nectar Flowers1

I examined relationships between tongue length of orchid bees (Apidae: Euglossini) and nectar spur length of their flowers in the genera Calathea, Costus, and Dimerocostus using phylogenetically independent contrasts. Long‐tubed flowers have specialized on one or several species of long‐tongued euglossine bees, but long‐tongued bees have not specialized on long‐tubed flowers. Whereas long tongues may have evolved to provide access to a wider variety of nectar resources, long nectar spurs may be a mechanism for flowers to conserve nectar resources while remaining attractive to traplining bee visitors.     

Microsatellite loci for euglossine bees (Hymenoptera: Apidae)

The Neotropical Euglossini (Hymenoptera: Apidae) are important pollinators of many flowering plants, particularly orchids. Lack of highly polymorphic genetic markers for euglossine species has limited the study of their social organization and inbreeding. We therefore developed microsatellite markers for two species, Eulaema nigrita (11 loci) and Euglossa cordata (nine loci), most of which were highly polymorphic in the source species and in a range of related euglossine bees.     

Biotic Resource Needs of Specialist Orchid Pollinators

Orchid pollinators have highly varied life histories with complex biotic resource requirements, about which we have limited knowledge. Among the specialist orchid pollinators are insect predators and parasitoids with specific prey types such as aphids and subterranean scarab larvae; oligolectic bees that collect pollen from limited sources such as bellflowers; euglossine bees and butterflies that collect particular plant chemicals for reproduction and self defense; oil-collecting bees that provision their brood cells with floral oils from a few plants; bees that collect rare floral resins to construct their nest and brood cells; moths and butterflies that require specific larval host plants; mosquitos and horse flies that need blood; and fungus gnats and carrion flies tied to fungi and dead animals. Loss of critical biotic resources and relationships can reduce the abundance of orchid pollinators and/or their effectiveness. Protection of large, plant rich, pesticide-free orchid habitats is key to conserving essential pollinator resources.     

Seasonal cycles,phylogenetic assembly,and functional diversity of orchid bee communities

Neotropical rainforests sustain some of the most diverse terrestrial communities on Earth. Euglossine (or orchid) bees are a diverse lineage of insect pollinators distributed throughout the American tropics, where they provide pollination services to a staggering diversity of flowering plant taxa. Elucidating the seasonal patterns of phylogenetic assembly and functional trait diversity of bee communities can shed new light into the mechanisms that govern the assembly of bee pollinator communities and the potential effects of declining bee populations. Male euglossine bees collect, store, and accumulate odoriferous compounds (perfumes) to subsequently use during courtship display. Thus, synthetic chemical baits can be used to attract and monitor euglossine bee populations. We conducted monthly censuses of orchid bees in three sites in the Magdalena valley of Colombia – a region where Central and South American biotas converge – to investigate the structure, diversity, and assembly of euglossine bee communities through time in relation to seasonal climatic cycles. In particular, we tested the hypothesis that phylogenetic community structure and functional trait diversity changed in response to seasonal rainfall fluctuations. All communities exhibited strong to moderate phylogenetic clustering throughout the year, with few pronounced bursts of phylogenetic overdispersion that coincided with the transition from wet‐to‐dry seasons. Despite the heterogeneous distribution of functional traits (e.g., body size, body mass, and proboscis length) and the observed seasonal fluctuations in phylogenetic diversity, we found that functional trait diversity, evenness, and divergence remained constant during all seasons in all communities. However, similar to the pattern observed with phylogenetic diversity, functional trait richness fluctuated markedly with rainfall in all sites. These results emphasize the importance of considering seasonal fluctuations in community assembly and provide a glimpse to the potential effects that climatic alterations may have on both pollinator communities and the ecosystem services they provide.     

Notes on pollination ecology and floral scent chemistry of the rare neotropical orchid Catasetum galeritum Rchb.f.

The neotropical orchid genus Catasetum embraces about 180 species that produce perfume as reward for pollinators (i.e. male euglossine bees). Among the ca. 1000 perfume‐rewarding plants, Catasetum species are the best studied with respect to their natural history. Nevertheless, the pollination ecology of most species (> 80%) remains unknown. Here, we investigated the pollination ecology and floral scent chemistry of C. galeritum, a rare species endemic to the poorly investigated Brazilian Amazon. Flowers of C. galeritum were visited only by male bees of Eufriesea superba. Its perfume bouquet was composed of six volatiles, with 1,4‐dimethoxybenzene accounting for about 85% of the total scent discharge. Curiously, this compound is a potent attractant of more than 40 euglossine species. The absence of euglossine species other than Ef. superba on flowers of C. galeritum might be, therefore, be mediated by a modifier effect of another compound(s) in its floral scent bouquet.     

Diversity and community composition of euglossine bee assemblages (Hymenoptera: Apidae) in western Amazonia

Tropical forests are known for their diverse insect fauna. We aimed to determine the effect and relative importance of latitude, elevation and climatic factors affecting species richness and turnover in euglossine bee assemblages along a gradient of 18° latitude from tropical rainforests to subtropical, deciduous dry forests in Peru and Bolivia. Sixteen forest sites were sampled during the dry season. Variance partitioning techniques were applied to assess the relative effects of the spatial and environmental variables on species richness and composition. Furthermore, we conducted a Species Indicator Analysis to find characteristic species for the biogeographic zones. There was a significant decrease in species richness towards the subtropical area. The best predictors of species richness were precipitation and its consequences on soil properties as well as temperature seasonality. The abundance of euglossines was most closely related to precipitation and soil-pH, but the causal links of abundance to these factors is unclear since soil-pH itself is correlated to a drastic turnover of vegetation structure. Based on the analysis of assemblage composition we propose three different assemblages with a transitional zone at the southern tropical area. The biogeographical distribution of euglossine bees along our study transect appears to be primarily related to climatic conditions and does not reflect the common subdividion of Amazonia into drainage systems.     

Orchid Bee (Apidae: Euglossini) Communities in Atlantic Forest Remnants and Restored Areas in Paraná State,Brazil

In this study, we compare orchid bee communities surveyed in four forest remnants of the Atlantic Forest and four reforested areas characterized by seasonal semi-deciduous forest vegetation in different successional stages (mature and secondary vegetation), located in southern Brazil. The sizes of forest remnants and reforested areas varied from 32.1 to 583.9 ha and from 11.3 to 33.3 ha, respectively. All reforested areas were located near one forest remnant. During samplings, totaling nine per study area, euglossine males were attracted to eight scent baits and captured with bait trap and entomological nets. Each forest remnant and its respective reforested area were sampled simultaneously by two collectors. We collected 435 males belonging to nine species of orchid bees distributed in four genera. The number of individuals and species did not differ significantly between different areas, except for a reforested area (size 33.3 ha), which was located far from its respective forest remnant. Our findings also revealed an apparent association between an orchid bee species (Euglossa annectans Dressler 1982) and the most preserved area surveyed in our study, suggesting that this bee is a potential indicator of good habitat quality in recuperating or preserved areas. Our results suggest that reforested habitats located near forest remnants have a higher probability of having reinstated their euglossine communities.     

Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: absence of premating barriers?

Pollinator specificity has traditionally been considered the main reproductive isolation mechanism in orchids. Among Mediterranean orchids, however, many species attract and deceive pollinators by mimicking nectar-rewarding plants. To test the extent to which deceptive orchid species share pollinators, we collected and identified hemipollinaria-carrying insects, and used ribosomal sequences to identify the orchid species from which hemipollinaria were removed. We found that social and solitary bees, and also flies, carried hemipollinaria belonging to nine orchid species with different degrees of specialization. In particular, Anacamptis morio, Dactylorhiza romana and Orchis mascula used a large set of pollinator species, whereas others such as Orchis quadripunctata seemed to be pollinated by one pollinator species only. Out of the insects with hemipollinaria, 19% were found to carry hemipollinaria from more than one orchid species, indicating that sympatric food-deceptive orchids can share pollinators. This sharing was apparent even among orchid sister-species, thus revealing an effective overlap in pollinator sets among closely related species. These results suggest varying degrees of pollinator specificity in these orchids, and indicate that pollinator specificity cannot always act as the main isolation mechanism in food-deceptive temperate orchids.     

Euglossine bees as potential bio-indicators of coffee farms: does forest access, on a seasonal basis, affect abundance?

In order to understand the implications of agriculture on the environment, ecosystem health must be measured. Observing the presence of a biological indicator within an ecosystem is one such method. In this study, male euglossine bees were observed using as attractant cineole 1:8, at adjacent organic (La Paz) and conventional (La Carena) coffee farms near the Northern Barranca River, San Ramón, Alajuela, Costa Rica. Simultaneous data collections were conducted on both farms in April 2004 (late-dry season) and June 2004 (early-rainy season) and combined with the findings of August 2004 (mid-rainy season). These observations show that orchid bees are a viable bio-indicator of organic farm health on a seasonal basis. In the dry season there was no significant difference in orchid bee abundance between the two farms. There is a strong tendency for more bees during the rainy season, suggesting that orchid bee abundance is linked to seasonality and forest access.     

Long-distance gene flow and cross-Andean dispersal of lowland rainforest bees (Apidae: Euglossini) revealed by comparative mitochondrial DNA phylogeography

Euglossine bees (Apidae; Euglossini) exclusively pollinate hundreds of orchid species and comprise up to 25% of bee species richness in neotropical rainforests. As one of the first studies of comparative phylogeography in a neotropical insect group, we performed a mitochondrial DNA (mtDNA)-based analysis of 14 euglossine species represented by populations sampled across the Andes and/or across the Amazon basin. The mtDNA divergences within species were consistently low; across the 12 monophyletic species the mean intraspecific divergence among haplotypes was 0.9% (range of means, 0-1.9%). The cytochrome oxidase 1 (CO1) divergence among populations separated by the Andes (N = 11 species) averaged 1.1% (range 0.0-2.0%). The mtDNA CO1 data set displayed homogeneous rates of nucleotide substitution, permitting us to infer dispersal across the cordillera long after the final Andean uplift based on arthropod molecular clocks of 1.2-1.5% divergence per million years. Gene flow across the 3000-km breadth of the Amazon basin was inferred from identical cross-Amazon haplotypes found in five species. Although mtDNA haplotypes for 12 of the 14 euglossine species were monophyletic, a reticulate CO1 phylogeny was recovered in Euglossa cognata and E. mixta, suggesting large ancestral populations and recent speciation. Reference to closely related outgroups suggested recent speciation for the majority of species. Phylogeographical structure across a broad spatial scale is weaker in euglossine bees than in any neotropical group previously examined, and may derive from a combination of Quaternary speciation, population expansion and/or long-distance gene flow.     

At daybreak--reproductive biology and isolating mechanisms of Cirrhaea dependens (Orchidaceae)

Floral biology, reproduction, pollinator specificity, and fruit set of Cirrhaea dependens were recorded in forest areas of Southeastern Brazil. Cirrhaea dependens is a lithophytic or epiphytic herb occurring very sparsely below dense canopies. Nearly all the flowers of a single plant open simultaneously before dawn. They are short-lasting and offer floral fragrances as rewards, which are collected by male euglossine bees. Observations carried out in mesophytic forests at Serra do Japi revealed that Euglossa VIRIDIS is their principal pollinator, with Eufriesea violacea a sporadic co-pollinator. Visitation started soon after flower opening, and attractiveness remained high for about 2 h, decreasing abruptly at sunrise. Flower anthesis with subsequent fragrance release seems to be correlated with bee attraction. Observations using chemical baits were carried out at Serra do Japi, and in the Atlantic Rain Forest of Picinguaba. Three euglossine species were captured with pollinaria of C. dependens in Picinguaba, whereas only E. violacea was attracted in Serra do Japi. In Picinguaba, C. dependens occurs sympatrically with C. saccata and C. loddigesii. Each species attracted different pollinators. The specificity and resulting reproductive isolation are due to the production of different odours by each orchid species. Cirrhaea dependens is self-compatible but pollinator-dependent. The reproductive success was low and appears to result from a combination of factors discussed here, such as the production of short-lived flowers, presence of floral mechanisms avoiding self-pollination, non-synchronization of flower phases among plants, and populations with few and sparsely distributed individuals.     

Abundance and Diversity of Euglossine Bees in the Fragmented Landscape of the Brazilian Atlantic Forest1

Male euglossine bees were sampled with chemical baits every two months from September 1997 to July 1999 at nine sites in the Desengano mountain range, Rio de Janeiro State, Brazil. Four sites were located in Atlantic Forest mature second growth, two sites in disturbed forest, and three sites in forest fragments of 200, 156, and 14 ha, respectively. We collected 3653 male euglossine bees from at least 21 species. Analyses of variance indicated no differences among the three habitat types for total number of bees, and 5 of the 6 dominant species. Bootstrapping indicated significant variation in species richness and diversity for some sites, but there was no clear indication of differences among habitats. Similarity as measured with the Morisita–Horn index was inversely related to distance between sites, but relatively high for most site combinations. These results suggest that the euglossine bee community in the three habitats was essentially the same. Although some species were associated with each habitat type, most appeared to respond to temporal local conditions. Our results do not support the hypothesis that forest fragmentation or habitat alteration reduces abundance and diversity of euglossine bees.     

Evolution and diversity of floral scent chemistry in the euglossine bee-pollinated orchid genus Gongora

•Background and Aims Animal-pollinated angiosperms have evolved a variety of signalling mechanisms to attract pollinators. Floral scent is a key component of pollinator attraction, and its chemistry modulates both pollinator behaviour and the formation of plant–pollinator networks. The neotropical orchid genus Gongora exhibits specialized pollinator associations with male orchid bees (Euglossini). Male bees visit orchid flowers to collect volatile chemical compounds that they store in hind-leg pouches to use subsequently during courtship display. Hence, Gongora floral scent compounds simultaneously serve as signalling molecules and pollinator rewards. Furthermore, because floral scent acts as the predominant reproductive isolating barrier among lineages, it has been hypothesized that chemical traits are highly species specific. A comparative analysis of intra- and inter-specific variation of floral scent chemistry was conducted to investigate the evolutionary patterns across the genus.•Methods Gas chromatography–mass spectrometry (GC-MS) was used to analyse the floral scent of 78 individuals belonging to 28 different species of Gongora from two of the three major lineages sampled across the neotropical region. Multidimensional scaling and indicator value analyses were implemented to investigate the patterns of chemical diversity within and among taxonomic groups at various geographic scales. Additionally, pollinator observations were conducted on a sympatric community of Gongora orchids exhibiting distinct floral scent phenotypes.•Key Results A total of 83 floral volatiles, mainly terpenes and aromatic compounds, were detected. Many of the identified compounds are common across diverse angiosperm families (e.g. cineole, eugenol, β-ocimene, β-pinene and terpinen-4-ol), while others are relatively rare outside euglossine bee-pollinated orchid lineages. Additionally, 29 volatiles were identified that are known to attract and elicit collection behaviour in male bees. Floral scent traits were less variable within species than between species, and the analysis revealed exceptional levels of cryptic diversity. Gongora species were divided into 15 fragrance groups based on shared compounds. Fragrance groups indicate that floral scent variation is not predicted by taxonomic rank or biogeographic region.•Conclusions Gongora orchids emit a diverse array of scent molecules that are largely species specific, and closely related taxa exhibit qualitatively and quantitatively divergent chemical profiles. It is shown that within a community, Gongora scent chemotypes are correlated with near non-overlapping bee pollinator assemblies. The results lend support to the hypothesis that floral scent traits regulate the architecture of bee pollinator associations. Thus, Gongora provides unique opportunities to examine the interplay between floral traits and pollinator specialization in plant–pollinator mutualisms.