Influence of landscape context on the abundance of native bee pollinators in tomato crops in Central Brazil

Evidence shows that pollinator abundance has declined and, consequently, so has their services, which has possible negative impacts on ecosystem functioning. The goal of this study was to evaluate the influence of landscape context at multiple spatial scales on the abundance of bee pollinators of tomato crops in Brazil. Pollinator abundance was obtained from tomato crops grown in a conventional system in the Cerrado region. Around each tomato field circular buffers of 0.75, 1, 1.5, 2, and 3 km radius were defined. Inside each buffer the landscapes were manually classified into native and non-native cover and, the proportion of native vegetation, the relative largest patch size, and the distance of the nearest native vegetation to each field were calculated. Pollinator species were categorized into five groups: Exomalopsis, Centris, Bombus/Eulaema, Halictidae, and all buzz pollinators combined (Buzzers). The results showed that the landscape context influenced the abundance of the five groups of tomato pollinators. Bees with a smaller body size, such as Exomalopsis spp., responded at smaller scales, while bees with a larger body size, such as the Centris and Bombus/Eulaema groups, responded at larger scales. The abundance of all pollinator groups increased with native vegetation cover. Most groups showed higher abundances in landscapes with similar-size fragments. The results reinforce the recommendation for maintaining natural habitats around crop areas, even if fragmented, for the conservation of the tomato pollinator assemblage. These findings are valuable for planning landscape management in the studied area to improve bee conservation, ecosystem services, and food production.     

The population genetics of two orchid bees suggests high dispersal,low diploid male production and only an effect of island isolation in lowering genetic diversity

Orchid bees (Hymenoptera, Apidae, Euglossini) are important pollinators of many plant families in Neotropical forests, habitats that have become increasingly degraded and fragmented by agricultural practices. To understand the extent to which loss of natural habitat and isolation has affected the genetic diversity and diploid male production (DMP) of two orchid bee species, Euglossa dilemma and Euglossa viridissima, we collected and genotyped 1686 males at five microsatellite loci and tested for differences in allelic richness, heterozygosity and DMP across three different types of land use (natural, agricultural and urban) and between mainland and island populations in the Yucatan Peninsula of Mexico. We also investigated the impact of land use and geographic isolation on gene flow. Euglossa dilemma and E. viridissima seemed to be particularly resilient to loss of natural habitat; in locations with human impact, we did not find reduced genetic diversity, and populations generally showed very little population genetic structure. Only on islands did E. dilemma show significantly reduced genetic diversity. Even after accounting for putative null alleles, DMP was very low (0.2–1.3%) across all sampling sites, including on islands. We therefore suggest that DMP is an insensitive measure of inbreeding and population decline in our two study species.     

Fragmentation in the clouds? The population genetics of the native bee <Emphasis Type="Italic">Partamona bilineata</Emphasis> (Hymenoptera: Apidae: Meliponini) in the cloud forests of Guatemala

Habitat fragmentation and loss are important drivers of genetic differentiation, often leading to a decrease in genetic diversity. Yet, natural populations of tropical bees often show a lack of differentiation, even in fragmented landscapes, suggesting resilience to deal with unfavourable land use. It is not clear what leads to this lack of differentiation, but large population sizes, high rates of dispersal and stable demography likely play important roles. Here, we investigate the population genetic structure and infer the present and historic demography of the eusocial stingless bee Partamona bilineata from tropical montane cloud forests in Guatemala. We used microsatellites and mitochondrial DNA to test for genetic differentiation, to infer migration rates, and to evaluate the effects of landscape. We also used demographic modelling to trace population sizes over time. We found that six populations of P. bilineata exhibited only subtle differentiation, with the exception of one site at the edge of the cloud forest, which was clearly distinct from all others. Effective population sizes (number of colonies) appeared to be rather small (18?±?6 colonies) compared to the original sample size (N?=?51?±?9), but stable over time, and inferred rates of gene flow were low; yet, no genetic bottleneck was detected. A statistical model including elevation was the best in explaining the observed pattern of differentiation. We find that P. bilineata does not exhibit strong genetic structure, making it a resilient species for provision of pollination services. But, at the same time, our data point to the potential vulnerability of this and similar species, as effective population sizes appear to be low and hence populations may be easily affected by future environmental change. As such, P. bilineata may be representative of many other tropical stingless bees, for which lack of differentiation has been invoked.     

Population genetics of wild and managed pollinators: implications for crop pollination and the genetic integrity of wild bees

Loss of habitat and chemical use associated with agriculture can cause population declines of wild pollinators. Less is known about the evolutionary consequences of interactions between species used in commercial agriculture and wild pollinators. Given population declines of many wild bee species, it is crucial to understand if commercial queens become established in natural areas, if wild bees visit agricultural fields and have the potential to interact with commercial bees, and if gene flow occurs between commercial and wild bees. We drew on a long-term data set that documents commercial bumble bee (Bombus impatiens) use in New England, and we conducted genetic analyses of foraging B. impatiens from areas with varying intensities of commercial bee use. In agricultural areas with a history of commercial bee use we also sampled bees directly from commercial hives. We found significant genetic differences among foraging B. impatiens and B. impatiens sampled directly from hives (average pairwise F′_ST = 0.14), but not among samples of foraging bees from natural areas (average F′_ST among foraging bees?=?0.002). Furthermore, Bayesian analysis of population structure revealed that foraging bees caught in areas with a history of commercial bee use grouped with samples from natural areas. These results document an agricultural setting where there was no widespread introgression of alleles from commercial bumble bees to wild bumble bees, commercial bumble bees did not become established in natural areas, and wild bees were providing pollination services to crops.     

Foraging habitats and floral resource use by colonies of long- and short-tongued bumble bee species in an agricultural landscape with kabocha squash fields

Bumble bees pollinate and forage on flowers of crop and wild plants in agricultural landscapes. These interactions may depend on landscape patterns and bumble bee traits. We studied the abundance, colony density, and foraging range in long-tongued Bombus diversus Smith and short-tongued B. hypocrita Pérez, and evaluated their visits to flowers of wild plants and cultivated kabocha squash (Cucurbita maxima Duchesne). In forests in a farmland, B. hypocrita workers were trapped more frequently in the canopy. Full-sibs determined by nuclear microsatellite genotypes among workers collected in the farmland showed higher colony density and a larger foraging radius in B. hypocrita (30.8 km^?2 and 848 m) than in B. diversus (8.3 km^?2 and 723 m), respectively. Regarding wild plants, workers more frequently visited shallow flowers in B. hypocrita and deep flowers in B. diversus. These results suggest that bumble bees with different traits forage on different wild flowers in different habitats. Squash flowers were visited by both bumble bee species at similar frequency in the latter period of colony growth when males and new queens appeared. Composition of full-sib workers visiting squash and wild flowers did not depend on the number of collected workers of individual colonies, indicating that foraging on squash flowers was not associated with colony growth. Thus, growth and reproduction of bumble bee colonies may be supported by various wild plants and cultivated squash, respectively.     

Beekeeping practices and geographic distance,not land use,drive gene flow across tropical bees

Across the globe, wild bees are threatened by ongoing natural habitat loss, risking the maintenance of plant biodiversity and agricultural production. Despite the ecological and economic importance of wild bees and the fact that several species are now managed for pollination services worldwide, little is known about how land use and beekeeping practices jointly influence gene flow. Using stingless bees as a model system, containing wild and managed species that are presumed to be particularly susceptible to habitat degradation, here we examine the main drivers of tropical bee gene flow. We employ a novel landscape genetic approach to analyse data from 135 populations of 17 stingless bee species distributed across diverse tropical biomes within the Americas. Our work has important methodological implications, as we illustrate how a maximum‐likelihood approach can be applied in a meta‐analysis framework to account for multiple factors, and weight estimates by sample size. In contrast to previously held beliefs, gene flow was not related to body size or deforestation, and isolation by geographic distance (IBD) was significantly affected by management, with managed species exhibiting a weaker IBD than wild ones. Our study thus reveals the critical importance of beekeeping practices in shaping the patterns of genetic differentiation across bee species. Additionally, our results show that many stingless bee species maintain high gene flow across heterogeneous landscapes. We suggest that future efforts to preserve wild tropical bees should focus on regulating beekeeping practices to maintain natural gene flow and enhancing pollinator‐friendly habitats, prioritizing species showing a limited dispersal ability.     

Non-native plants affect generalist pollinator diet overlap and foraging behavior indirectly,via impacts on native plant abundance

Flowering invasive plants can have dramatic effects on the resource landscape available to pollinators. Because many pollinators exhibit behavioral plasticity in response to competitor or resource density, this in turn can result in impacts on ecological processes such as pollination and plant reproduction. We examine how interactions between five common generalist eusocial bees change across an invasion gradient by examining how bee abundance and diet overlap changed with variation in both invasive plant abundance and competitor abundance in a temperate oak-savannah ecosystem. Specifically we focus on the bumblebees Bombus bifarius, B. mixtus, B. melanopygus and B. vosnesenskii, as well as the non-native honeybee Apis mellifera, and their interactions with the native flowering plants Camassia quamash, Camassia liechtlinii, and the invasive shrub Cytisus scoparius. We further examine whether changes in pollinator visits to the invasive and two common native plants can explain changes in diet overlap. Abundance of the invasive plant and other common floral resources had strong impacts on focal bee abundance, with certain species more likely to be present at highly invaded sites. This may be because highly invaded sites tended to be embedded in forested landscapes where those bees are common. Diet overlap was most affected by abundance of a common native plant, rather than the invasive plant, with diet overlap increasing non-linearly with abundance of the native plant. Furthermore, Apis mellifera, did not appear to have direct competitive effects on native bumblebees in this habitat. However, visit patterns suggest that bees most abundant at highly invaded sites may compete for access to native resources. Thus the impacts of this invasive plant on our focal bee species may be primarily indirect, via its’ competitive effects on native plants.     

Effect of coffee agriculture management on the population structure of a forest dwelling rodent (<Emphasis Type="Italic">Heteromys desmarestianus goldmani</Emphasis>)

Most of the natural habitat in tropical regions exists as scattered fragments embedded in a matrix of different agricultural uses. As a result of this agricultural expansion, habitat loss and fragmentation have become the main drivers of biodiversity loss. Understanding the long-term effects of agricultural management on populations is of great importance for the development of successful conservation strategies. Our study uses genetic data to determine the effect of agricultural management practices on the population structure of a common tropical forest rodent (Heteromys desmarestianus goldmani). We sampled 136 individuals from one forest fragment and three coffee farms representing varying degrees of management intensity in southern Mexico. Using microsatellite markers, we evaluated the genetic structure of H. d. goldmani in the study area. Our results show higher genetic differentiation and lower connectivity for individuals within high and medium intensity coffee farms than for those near and within the forest fragments. Our results suggest that the population structure observed is driven by landscape characteristics other than distance.     

The role of very small fragments in conserving genetic diversity of a common tree in a hyper fragmented Brazilian Atlantic forest landscape

In hyper fragmented biomes, conservation of extant biota relies on preservation and proper management of remnants. The maintenance of genetic diversity and functional connectivity in a landscape context is probably key to long-term conservation of remnant populations. We measured the genetic diversity in seedlings and adults of tree Copaifera langsdorffii and evaluated whether edge and density-dependent effects drive natural regeneration in a set of very small and degraded Brazilian Atlantic forest fragments. We evaluated the role of small remnants in the conservation of genetic diversity in a hyper fragmented landscape and discuss the challenge of long-term population sustainability of such altered habitats. High genetic diversity in adults indicated these fragments are valuable targets for C. langsdorffii in situ conservation, but both genetic diversity and divergence among patches decreased in seedlings. In our landscape, regeneration increased as it neared edges and adults; suggesting this population is resilient to fragmentation. However, at a broader scale, current levels of gene flow have not been sufficient to prevent the loss of genetic diversity across generations. Restoration plans, even at a small scale, are necessary to promote fragment connectivity and spatially expand opportunities for the fairly restricted gene flow observed in this severely fragmented Brazilian Atlantic forest region.     

Landscape composition modifies pollinator densities,foraging behavior and yield formation in faba beans

Wildlife-friendly management practices promote pollinators and pollination services in agricultural landscapes. Wild bee densities are driven by landscape composition, as they benefit from an increased availability of nesting and foraging resources at landscape scale. However, effects of landscape composition on bee foraging decisions and consequences for crop pollination have rarely been studied. We investigated, how landscape composition affects bee densities and foraging behavior in faba bean (Vicia faba L.) fields and how this impacts faba bean yield. We recorded densities and nectar robbing behavior of honeybees, long- tongued and short-tongued bumblebees in faba bean fields in eleven landscapes with varying landscape composition (e.g. land cover of oilseed rape, faba bean and semi-natural habitats). Moreover, we assessed yield components of faba beans via pollinator exclusion experiments. Increasing covers of faba bean and semi-natural habitats positively influenced bumblebee densities, while high oilseed rape covers negatively affected short-tongued bumblebee densities in bean fields. Increased faba bean covers enhanced the proportion of nectar-robbing short-tongued bumblebees. The number of beans per pod was increased by insect pollination, while the number of pods was decreased; these effects however depended on variety. Landscape composition interacted with bee densities in shaping yield components in V. faba. Our study emphasizes the importance of considering landscape management to maximize crop yields, as shown for the case of faba beans. The composition of agricultural landscape can modulate bee densities in crop fields, bees foraging behavior and pollination services.     

Thinking beyond Western commercial honeybee hives: towards improved conservation of honey bee diversity

A decline of wild pollinators, along with a decline of bee diversity, has been a cause of concern among academics and governmental organizations. According to IPBES, a lack of wild pollinator data contributes to difficulties in comprehensively analyzing the regional status of wild pollinators in Africa, Latin America, Asia and Oceania. It may have also contributed to the prevailing lack of awareness of the diversity of honey bees, of which the managed Apis mellifera is often considered as “the (only) honey bee,” despite the fact that there are eight other honey bee species extant in Asia. A survey of 100 journal articles published in 2016 shows that 57% of the studies still identified A. mellifera as “the honey bee.” In total, 80% of studies were conducted solely on A. mellifera. This focus on A. mellifera has also caused the honey standard of Codex Alimentarius and the European Union to be based solely on A. mellifera, causing improper evaluation of honeys from other species. We recommend adapting current standards to reflect the diversity of honey bees and in the process correct failures in the honey market and pave the way towards improved protection of honey bee species and their habitats.     

Genetic evidence of fragmented populations and inbreeding in the Colombian endemic Dahl’s toad-headed turtle (<Emphasis Type="Italic">Mesoclemmys dahli</Emphasis>)

Population fragmentation is one of the most concerning consequences of habitat fragmentation, as small and isolated populations suffer increased genetic drift and inbreeding. However, the extent to which habitat fragmentation leads to population fragmentation depends not only on the landscape structure, but also on the response of organisms to it. This behavioral component makes it difficult to detect population fragmentation even if the habitat is fragmented, unless appropriate tools are used. In this study, we used a molecular approach to evaluate if Dahl’s toad-headed turtle (Mesoclemmys dahli) population was fragmented, given that it occurs in a very restricted area within the most degraded biome of Colombia, the tropical dry forest. We developed a panel of 15 microsatellite loci in order to perform the first genetic assessment of M. dahli across its complete geographic range. We found that M. dahli has significant genetic structure with at least four subpopulations, with surprisingly moderate to high levels of genetic diversity. Despite high levels of genetic diversity, subpopulations are very small (effective population sizes?<?50) and isolated, with little to no contemporary gene flow among them. As a consequence, mating among related individuals has been occurring, and all four populations are showing high degrees of inbreeding. To counteract this threat, we recommend an urgent genetic rescue strategy accompanied by habitat restoration, and advocate for a new conservation status assessment, not based on geographic range, but on adult population size and level of fragmentation.     

Isolation and characterization of ten microsatellite loci in stingless bee Trigona spinipes (Apidae: Meliponini)

Stingless bees are the most abundant pollinators of Brazilian tropical flora. Trigona spinipes has some of the largest colonies of any stingless bee species found in several types of environment. This work describes the isolation and characterization of microsatellite loci for this species. A microsatellite‐enriched genomic library was constructed and ten primer pairs were designed for T. spinipes. The primers were tested in 20 unrelated individuals. The mean number of alleles was 8.10 and mean observed and expected heterozygosity were 0.655 and 0.680, respectively. Primers were also tested in cross‐species amplification and five loci were successfully amplified in Trigona chanchamayoensis, Trigona hyalinata, Tetragonisca angustula, Partamona mulata and Frieseomelitta varia. The microsatellite primers described herein will be useful for evaluating genetic variability and gaining a better understanding of the population structure of T. spinipes as well as other species of stingless bees.     

Isolation from forest habitats reduces chances of the presence of <Emphasis Type="Italic">Osmoderma eremita</Emphasis> sensu lato (Coleoptera,Scarabaeidae) in rural avenues

Decline and fragmentation of natural habitats, such as old-growth forests, reduces their availability in the landscape. The solution to this problem for many forest-dwelling species, may be colonization of alternative habitats, such as parks, orchards or rural avenues, located in the highly fragmented agricultural landscape. Our main objective was to determine the effect of both habitat quality parameters and isolation from potential forest habitats, as primary habitats, on the occurrence of the hermit beetle (Osmoderma) in rural avenues in south-western Poland. The study was based on the results of an inventory of the species in 201 rural avenues within an area of approx. 30,000 km². Occurrence of the hermit beetle in such alternative habitats was affected by both habitat quality parameters and connectivity with suitable forest habitats. The species occurrence in an avenue was significantly positively affected by mean tree diameter and diversity of tree species, but probability of occurrence decreased as isolation of avenue from the deciduous forest increased. Moreover, in the study area the hermit beetle seemed to avoid alleys with a large proportion of Acer platanoides, Fraxinus excelsior and Populus spp. Spatially isolated roadside avenues have limited value in the preservation of the hermit beetle in the long term conservation management of the species. Conservation plans in such habitats should therefore take into account surrounding suitable habitats.     

Habitat selection by Canada lynx: making do in heavily fragmented landscapes

Habitat loss and fragmentation result in landscapes where high quality habitat patches are surrounded by matrix habitats of low and variable quality. For mobile species to persist in such landscapes, individual animals often rely on the high quality habitats but also use matrix habitats for supplemental resources or while moving between higher quality patches. Determining what habitat features animals select when in these matrix areas is important, as retaining desirable features in lower quality habitats may enable species persistence. We examine a population of US federally threatened Canada lynx (Lynx canadensis) in northcentral Washington, near the southwestern range limit, where lynx habitat is fragmented by topography, wildfires, and human impacts. We used Global Positioning System radio-collar data from 17 lynx in the North Cascade Mountains during 2007–2013 to explore lynx habitat use. We used Random Forest models to analyze core hunting, resting, and denning habitat, and the habitats lynx select while between patches of core habitat. While selecting core habitat, lynx used spruce (Picea engelmannii)-fir (Abies lasiocarpa), lodgepole pine (Pinus contorta), and mixed sub-boreal-Douglas fir (Pseudotsuga menziesii) forests, and avoided dry forests and forest openings including new burns. When not in core habitat, lynx used a wider range of habitats, including new burns where fire skips and residual trees offered cover. Our results show clearly that Canada lynx tolerate a wider range of habitats where they occupy fragmented landscapes. Consequently, maintaining animals in fragmented landscapes requires that we identify and conserve not only the core habitats a particular species selects, but also the habitat features animals use while in less suitable environments.     

Farming for bees: annual variation in pollinator populations across agricultural landscapes

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The use of a mixed rubber landscape by tufted-ear marmosets

With the loss and fragmentation of tropical forests, the survival of primates depends on their ability to adapt to human-introduced modifications in their habitat. Marmosets are known for their ecological and behavioral plasticity and have been registered in various agricultural landscapes. Our goal was to describe the ecology of tufted-ear marmosets (Callithrix sp.) in a rubber/forest landscape, monitoring their use of habitat and diet. We followed two groups using radio telemetry and visual observations for nine months at the Michelin plantation Ltd. in Bahia, Brazil. Both groups used mainly pioneer forest and rubber with pioneer vegetation more than expected according to availability, even though they explored all types of vegetation. Rubber monocultures act as corridors for marmoset locomotion among more suitable habitats. Feeding, gummivory and socialization were mainly performed in the pioneer forest (with or without rubber), in which most sleeping sites and food sources were found. Groups of marmosets can incorporate agroforest matrixes to their area of use and activity patterns. Maintenance of marmosets in fragmented landscapes might be favored by their diet flexibility, with the use of resources such as gum and fruit, including exotic plants. Although known for their ecological flexibility, marmosets do require certain resources to be present in native habitat to adapt to agricultural landscapes. Patches of forest within a rubber landscape and pioneer vegetation in the rubber inter-rows should be considered to maintain populations of Callithrix in rubber landscapes.     

Conservation value of degraded habitats for forest birds in southern Peninsular Malaysia

Clearance of tropical forest for agricultural purposes is generally assumed to seriously threaten the survival of forest species. In this study, we quantified the conservation value, for forest bird species, of three degraded habitat types in Peninsular Malaysia, namely rubber tree plantations, oil palm plantations, and open areas. We surveyed these degraded habitats using point counts to estimate their forest bird species richness and abundance. We assessed whether richness, abundance, and activities of different avian dietary groups (i.e. insectivores and frugivores) varied among the habitats. We identified the critical habitat elements that accounted for the distribution of forest avifauna in these degraded habitats. Our results showed that these habitats harboured a moderate fraction of forest avifauna (approximately 46–76 species) and their functions were complementary (i.e. rubber tree plantations for moving; open habitats for perching; shrubs in oil palm plantations for foraging). In terms of species richness and abundance, rubber tree plantations were more important than oil palm plantations and open habitats. The relatively high species richness of this agricultural landscape was partly due to the contiguity of our study areas with extensive forest areas. Forecasts of forest-species presence under various canopy cover scenarios suggest that leaving isolated trees among non-arboreal crops could greatly attract relatively tolerant species that require tree canopy. The conservation value of degraded habitats in agricultural landscapes seems to depend on factors such as the type of crops planted and distance to primary forest remnants.     

Accompanying vegetation in young <Emphasis Type="Italic">Pinus radiata</Emphasis> plantations enhances recolonization by <Emphasis Type="Italic">Ceroglossus chilensis</Emphasis> (Coleoptera: Carabidae) after clearcutting

The replacement of native forests by Pinus radiata plantations modifies habitat availability and quality for wildlife, constituting a threat to species survival. However, the presence of understory in mature pine plantations minimizes the negative impacts of native forest replacement, rendering a secondary habitat for wildlife. Whether forest-dwelling species recolonize clear-felled areas pending on the spontaneous development of accompanying vegetation growing after harvesting is yet to be assessed. In this context, we analyze the abundance, movement and habitat selection of the endemic ground beetle Ceroglossus chilensis (Coleoptera: Carabidae) in an anthropic forest landscape consisting of native forest remnants, adult pine plantations (>?20 years) with a well-developed understory, and young (1–2 years) pine plantations with varying degrees of accompanying vegetation development. Particularly, we analyze the likelihood that C. chilensis would recolonize young pine plantations depending on the presence (>?70% cover) or the absence (<?20% cover) of this accompanying vegetation. C. chilensis shows a greater probability of selecting habitats with understory (pine plantations and native forest) and young plantations with accompanying vegetation (future understory) than habitats without such vegetation. Movement of C. chilensis also favors their permanence in habitats with understory vegetation, coinciding with higher abundances than in young pine plantations devoid of accompanying vegetation. Hence, the effect of clearcutting could be mitigated by allowing the development of accompanying vegetation into a future understory, which facilitates the recolonization of pine plantations and its use as secondary habitat for wildlife.     

Ambush Predation of Stingless Bees (<Emphasis Type="Italic">Tetragonisca angustula</Emphasis>) by the Solitary-Foraging Ant <Emphasis Type="Italic">Ectatomma tuberculatum</Emphasis>

Social insect colonies are high-value foraging targets for insectivores, prompting the evolution of complex colony defensive adaptations as well as specialized foraging tactics in social insect predators. Predatory ants that forage on other social insects employ a diverse range of behaviors targeted at specific prey species. Here, we describe a solitary foraging strategy of the ant Ectatomma tuberculatum, on nest guards of the stingless bee Tetragonisca angustula. We observed multiple instances of E. tuberculatum ambushing and successfully capturing the hovering and standing guards of T. angustula near nest entrances. The unique hovering behavior of the guard caste of this bee species, an adaptation to frequent cleptoparasitism by other stingless bees, may make these guards particularly vulnerable to ground-based, ambush attacks by E. tuberculatum. Likewise, the behavior of the foraging ants appears to adaptively exploit the defensive formations and activity patterns of these bees. These observations suggest an adaptive and targeted predatory strategy aimed at gathering external guard bees as prey from these heavily fortified nests.