Tropical bee species abundance differs within a narrow elevational gradient.

Insect pollination is among the most essential ecosystem services for humanity. Globally, bees are the most effective pollinators, and tropical bees are also important for maintaining tropical biodiversity. Despite their invaluable pollination service, basic distributional patterns of tropical bees along elevation gradients are globally scarce. Here, we surveyed bees at 100 m elevation intervals from 800 to 1100 m elevation in Costa Rica to test if bee abundance, community composition and crop visitor assemblages differed by elevation. We found that 18 of 24 bee species spanning three tribes that represented the most abundantly collected bee species showed abundance differences by elevation, even within this narrow elevational gradient. Bee assemblages at the two crop species tested, avocado and squash, showed community dissimilarity between high and low elevations, and elevation was a significant factor in explaining bee community composition along the gradient. Stingless bees (Tribe Meliponini) were important visitors to both crop species, but there was a more diverse assemblage of bees visiting avocado compared to squash. Our findings suggest that successful conservation of tropical montane bee communities and pollination services will require knowledge of which elevations support the highest numbers of each species, rather than species full altitudinal ranges.

Free-Living Aquatic Turtles as Sentinels of Salmonella spp. for Water Bodies.

Reptile-associated human salmonellosis cases have increased recently in the United States. It is not uncommon to find healthy chelonians shedding Salmonella enterica. The rate and frequency of bacterial shedding are not fully understood, and most studies have focused on captive vs. free-living chelonians and often in relation to an outbreak. Their ecology and significance as sentinels are important to understanding Salmonella transmission. In 2012-2013, Salmonella prevalence was determined for free-living aquatic turtles in man-made ponds in Clarke and Oconee Counties, in northern Georgia (USA) and the correlation between species, basking ecology, demographics (age/sex), season, or landcover with prevalence was assessed. The genetic relatedness between turtle and archived, human isolates, as well as, other archived animal and water isolates reported from this study area was examined. Salmonella was isolated from 45 of 194 turtles (23.2%, range 14-100%) across six species. Prevalence was higher in juveniles (36%) than adults (20%), higher in females (33%) than males (18%), and higher in bottom-dwelling species (31%; common and loggerhead musk turtles, common snapping turtles) than basking species (15%; sliders, painted turtles). Salmonella prevalence decreased as forest cover, canopy cover, and distance from roads increased. Prevalence was also higher in low-density, residential areas that have 20-49% impervious surface. A total of 9 different serovars of two subspecies were isolated including 3 S. enterica subsp. arizonae and 44 S. enterica subsp. enterica (two turtles had two serotypes isolated from each). Among the S. enterica serovars, Montevideo (n = 13) and Rubislaw (n = 11) were predominant. Salmonella serovars Muenchen, Newport, Mississippi, Inverness, Brazil, and Paratyphi B. var L(+) tartrate positive (Java) were also isolated. Importantly, 85% of the turtle isolates matched pulsed-field gel electrophoresis patterns of human isolates, including those reported from Georgia. Collectively, these results suggest that turtles accumulate Salmonella present in water bodies, and they may be effective sentinels of environmental contamination. Ultimately, the Salmonella prevalence rates in wild aquatic turtles, especially those strains shared with humans, highlight a significant public health concern.

Plant species with the trait of continuous flowering do not hold core roles in a Neotropical lowland plant-pollinating insect network.

Plant-animal interaction science repeatedly finds that plant species differ by orders of magnitude in the number of interactions they support. The identification of plant species that play key structural roles in plant-animal networks is a global conservation priority; however, in hyperdiverse systems such as tropical forests, empirical datasets are scarce. Plant species with longer reproductive seasons are posited to support more interactions compared to plant species with shorter reproductive seasons but this hypothesis has not been evaluated for plant species with the longest reproductive season possible at the individual plant level, the continuous reproductive phenology. Resource predictability is also associated with promoting specialization, and therefore, continuous reproduction may instead favor specialist interactions. Here, we use quantitative pollinating insect-plant networks constructed from countryside habitat of the Tropical Wet forest Life Zone and modularity analysis to test whether plant species that share the trait of continuous flowering hold core roles in mutualistic networks. With a few exceptions, most plant species sampled within our network were assigned to the role of peripheral. All but one network had significantly high modularity scores and each continuous flowering plant species was in a different module. Our work reveals that the continuous flowering plant species differed in some networks in their topological role, and that more evidence was found for the phenology to support specialized subsets of interactions. Our findings suggest that the conservation of Neotropical pollinating insect communities may require planting species from each module rather than identifying and conserving network hubs.

Bee communities and pollination services in adjacent crop fields following flower removal in an invasive forest shrub.

The habitat boundaries between crops and seminatural areas influence bee movements and pollination services to crops. Edges also provide favorable conditions for invasive plants, which may usurp pollinators and reduce visitation to native or crop plants. Alternatively, floral displays of alien plants may facilitate, or increase, the pollination success of adjacent plants by attracting more pollinators to the area. Therefore, pollination services of bees from seminatural habitats to crop areas should vary with the presence of invasive floral resources and distance from habitat edges. To test the hypothesis that floral resources of invasive forest shrubs affect the bee community and pollination services in adjacent crop fields, we conducted a 2-yr field experiment along forest-crop edges at five isolated forest remnants. We removed flower buds from a dominant invasive shrub, Lonicera maackii (Amur honeysuckle), along forest-crop edges and paired removals with controls of intact flowers. The bee community, their pollination services, and flower visitation rates were quantified along a 200-m gradient into an adjacent crop field using pan traps and sentinel cucumber plants. Impacts to the bee community were dependent of bee functional traits. Larger bees visited fewer sentinel cucumber flowers in flower removal plots, which corresponded with decreased cucumber pollination compared to plots with honeysuckle flowers at distances >100 m from forest edges. Small-bodied and weaker flying bees visited sentinel plants more frequently closer to the forest edge and increased pollination services to cucumber at distances <100 m from L. maackii shrubs in flower removal plots. After 2 yr, bee abundance and species richness increased within flower removal plots across all distances. High functional diversity of the bee community increased pollination services to sentinel plants and increased cucumber production within 200 m from forest remnants. Our findings suggest that dense floral resources of invasive shrubs suppressed forest-edge bee communities and their pollination services, but also attracted large-bodied generalist bees, which were effective pollinators. This study helps explain how life histories and functional attributes of bees can predict either facilitation or suppression of pollination services to crop or native plants in response to invasive floral resources.

Urbanized White Ibises (Eudocimus albus) as Carriers of Salmonella enterica of Significance to Public Health and Wildlife.

Worldwide, Salmonella spp. is a significant cause of disease for both humans and wildlife, with wild birds adapted to urban environments having different opportunities for pathogen exposure, infection, and transmission compared to their natural conspecifics. Food provisioning by people may influence these factors, especially when high-density mixed species flocks aggregate. White Ibises (Eudocimus albus), an iconic Everglades species in decline in Florida, are becoming increasingly common in urbanized areas of south Florida where most are hand-fed. We examined the prevalence of Salmonella shedding by ibises to determine the role of landscape characteristics where ibis forage and their behavior, on shedding rates. We also compared Salmonella isolated from ibises to human isolates to better understand non-foodborne human salmonellosis. From 2010-2013, 13% (n = 261) adult/subadult ibises and 35% (n = 72) nestlings sampled were shedding Salmonella. The prevalence of Salmonella shedding by ibises significantly decreased as the percent of Palustrine emergent wetlands and herbaceous grasslands increased, and increased as the proportion of open-developed land types (e.g. parks, lawns, golf courses) increased, suggesting that natural ecosystem land cover types supported birds with a lower prevalence of infection. A high diversity of Salmonella serotypes (n = 24) and strain types (43 PFGE types) were shed by ibises, of which 33% of the serotypes ranked in the top 20 of high significance for people in the years of the study. Importantly, 44% of the Salmonella Pulsed-Field Gel Electrophoresis patterns for ibis isolates (n = 43) matched profiles in the CDC PulseNet USA database. Of these, 20% came from Florida in the same three years we sampled ibis. Importantly, there was a negative relationship between the amount of Palustrine emergent wetland and the number of Salmonella isolates from ibises that matched human cases in the PulseNet database (p = 0.056). Together, our results indicate that ibises are good indicators of salmonellae strains circulating in their environment and they have both the potential and opportunity to transmit salmonellae to people. Finally, they may act as salmonellae carriers to natural environments where other more highly-susceptible groups (nestlings) may be detrimentally affected.

MORTALITY OF SELECTED AVIAN ORDERS SUBMITTED TO A WILDLIFE DIAGNOSTIC LABORATORY (SOUTHEASTERN COOPERATIVE WILDLIFE DISEASE STUDY, USA): A 36-YEAR RETROSPECTIVE ANALYSIS.

To determine the relative importance of mortality factors for birds and to assess for patterns in avian mortality over time, we retrospectively examined data of birds submitted to the Southeastern Cooperative Wildlife Disease Study (SCWDS; http://vet.uga.edu/scwds ), US, from 1976 to 2012. During this period, SCWDS, a wildlife diagnostic laboratory, received 2,583 wild bird specimens, from the taxonomic orders Apodiformes, Caprimulgiformes, Cuculiformes, Passeriformes, and Piciformes, originating from 22 states. Data from 2,001 of these birds were analyzed using log-linear models to explore correlations between causes of mortality, taxonomic family, demography, geographic location, and seasonality. Toxicosis was the major cause of mortality, followed by trauma, bacterial infection, physiologic stress, viral infection, and other (mortality causes with low sample numbers and etiologies inconsistent with established categories). Birds submitted during fall and winter had a higher frequency of parasitic infections, trauma, and toxicoses, whereas birds submitted during the spring and summer were more likely to die of an infectious disease, physiologic stress, or trauma. We noted a decrease in toxicoses concurrent with an increase in bacterial infections and trauma diagnoses after the mid-1990s. Toxicosis was the most commonly diagnosed cause of death among adult birds; the majority of juveniles died from physiologic stress, trauma, or viral infections. Infectious agents were diagnosed more often within the families Cardinalidae and Fringilidae, whereas noninfectious etiologies were the primary diagnoses in the Bombycillidae, Parulidae, Sturnidae, Turdidae, and Icteridae. There are important inherent limitations in the examination of data from diagnostic labs, as submission of cases varies in timing, frequency, location, and species and is often influenced by several factors, including media coverage of high-profile mortality events. Notwithstanding, our data provide a rare opportunity to examine long-term, regional, and temporal patterns in causes of avian mortality, and they allow for the analysis of novel and rare mortality factors.

Intercropping with shrub species that display a 'steady-state' flowering phenology as a strategy for biodiversity conservation in tropical agroecosystems.

Animal species in the Neotropics have evolved under a lower spatiotemporal patchiness of food resources compared to the other tropical regions. Although plant species with a steady-state flowering/fruiting phenology are rare, they provide predictable food resources and therefore may play a pivotal role in animal community structure and diversity. I experimentally planted a supplemental patch of a shrub species with a steady-state flowering/fruiting phenology, Hamelia patens Jacq., into coffee agroforests to evaluate the contribution of this unique phenology to the structure and diversity of the flower-visiting community. After accounting for the higher abundance of captured animals in the coffee agroforests with the supplemental floral resources, species richness was 21% higher overall in the flower-visiting community in these agroforests compared to control agroforests. Coffee agroforests with the steady-state supplemental floral patch also had 31% more butterfly species, 29% more hummingbird species, 65% more wasps and 85% more bees than control coffee agroforests. The experimental treatment, together with elevation, explained 57% of the variation in community structure of the flower-visiting community. The identification of plant species that can support a high number of animal species, including important ecosystem service providers, is becoming increasingly important for restoration and conservation applications. Throughout the Neotropics plant species with a steady-state flowering/fruiting phenology can be found in all aseasonal forests and thus could be widely tested and suitable species used throughout the tropics to manage for biodiversity and potentially ecosystem services involving beneficial arthropods.

Coffee agroforests remain beneficial for neotropical bird community conservation across seasons.

Coffee agroforestry systems and secondary forests have been shown to support similar bird communities but comparing these habitat types are challenged by potential biases due to differences in detectability between habitats. Furthermore, seasonal dynamics may influence bird communities differently in different habitat types and therefore seasonal effects should be considered in comparisons. To address these issues, we incorporated seasonal effects and factors potentially affecting bird detectability into models to compare avian community composition and dynamics between coffee agroforests and secondary forest fragments. In particular, we modeled community composition and community dynamics of bird functional groups based on habitat type (coffee agroforest vs. secondary forest) and season while accounting for variation in capture probability (i.e. detectability). The models we used estimated capture probability to be similar between habitat types for each dietary guild, but omnivores had a lower capture probability than frugivores and insectivores. Although apparent species richness was higher in coffee agroforest than secondary forest, model results indicated that omnivores and insectivores were more common in secondary forest when accounting for heterogeneity in capture probability. Our results largely support the notion that shade-coffee can serve as a surrogate habitat for secondary forest with respect to avian communities. Small coffee agroforests embedded within the typical tropical countryside matrix of secondary forest patches and small-scale agriculture, therefore, may host avian communities that resemble those of surrounding secondary forest, and may serve as viable corridors linking patches of forest within these landscapes. This information is an important step toward effective landscape-scale conservation in Neotropical agricultural landscapes.

Do shade-grown coffee plantations pose a disease risk for wild birds?

Shade-grown coffee plantations are often promoted as a conservation strategy for wild birds. However, these agro-ecosystems are actively managed for food production, which may alter bird behaviors or interactions that could change bird health, compared to natural forest. To examine whether there is a difference between the health parameters of wild birds inhabiting shade-grown coffee plantations and natural forest, we evaluated birds in Costa Rica for (1) their general body condition, (2) antibodies to pathogens, (paramyxovirus and Mycoplasma spp.), and (3) the prevalence and diversity of endo-, ecto-, and hemoparasites. We measured exposure to Mycoplasma spp. and paramyxovirus because these are pathogens that could have been introduced with domestic poultry, one mechanism by which these landscapes could be detrimental to wild birds. We captured 1,561 birds representing 75 species. Although seasonal factors influenced body condition, we did not find bird general body condition to be different. A total of 556 birds of 31 species were tested for antibodies against paramyxovirus-1. Of these, five birds tested positive, four of which were from shade coffee. Out of 461 other tests for pathogens (for antibodies and nucleotide detection), none were positive. Pterolichus obtusus, the feather mite of chickens, was found on 15 birds representing two species and all were from shade-coffee plantations. Larvated eggs of Syngamus trachea, a nematode typically associated with chickens, were found in four birds captured in shade coffee and one captured in forest. For hemoparasites, a total of 1,121 blood smears from 68 bird species were examined, and only one species showed a higher prevalence of infection in shade coffee. Our results indicate that shade-coffee plantations do not pose a significant health risk to forest birds, but at least two groups of pathogens may deserve further attention: Haemoproteus spp. and the diversity and identity of endoparasites.

Bird community response to fruit energy.

1. The abundance and predictability of food resources have been posited as explanations for the increase of animal species richness in tropical habitats. However, the heterogeneity of natural ecosystems makes it difficult to quantify a response of animal species richness to these qualities of food resources. 2. Fruit-frugivore studies are especially conducive for testing such ecological theories because fruit is conspicuous and easily counted. Fruit-frugivore research in some locations has demonstrated a relationship between animal abundance and fruit resource abundance, both spatially and temporally. These studies, which typically use fruit counts as the variable of fruit abundance, have never documented a response of species richness at the community level. Furthermore, these studies have not taken into account factors influencing the detection of an individual within surveys. 3. Using a combination of nonstandard approaches to fruit-frugivore research, we show a response of bird species richness to fruit resources. First, we use uniform and structurally similar, one-ha shade-grown coffee plots as replicated experimental units to reduce the influence of confounding variables. Secondly, we use multi-season occupancy modelling of a resident omnivorous bird assemblage in order to account for detection probability in our analysis of site occupancy, local immigration and local emigration. Thirdly, we expand our variable of fruit abundance, Fruit Energy Availability (FEA), to include not only fruit counts but also fruit size and fruit quality. 4. We found that a site's average monthly FEA was highly correlated (0.90) with a site's average bird species richness. In our multi-season occupancy model 92% of the weight of evidence supported a single model that included effects of FEA on initial occupancy, immigration, emigration and detection. 5. These results demonstrate that fruit calories can broadly influence the richness of a neotropical bird community, and that fluctuations of FEA explains much of the site occupancy patterns of component species. This study shows that in depauperate, managed landscapes fruit resource abundance supports more species and fruit constancy allows for higher levels of avian persistence, an important practical concept for conservation planning.