Low resilience to deforestation in nocturnal bees is counteracted by a broad resource range and reliance on pioneers

Nocturnal floral scent profiles of Myrtaceae fruit crops

With plants whose flowers open at night and stay open during the day, nocturnal pollinators may exploit floral resources before diurnal competitors. Moths, bats, and beetles are the most familiar nocturnal pollinators, whereas nocturnal bees as pollinators remain poorly understood. The common Cerrado tree Machaerium opacum (Fabaceae) has white and strongly scented melittophilous flowers, which first open at the night and remain open during the day and, thus, have the potential to be visited by both nocturnal and diurnal bees. We asked: (1) what is the plant’s breeding system? (2) when during the night do the flowers open? (3) what are the visual and olfactory floral cues? and (4) which nocturnal/diurnal bees visit and pollinate the flowers? We show that M. opacum is self-incompatible. Its flowers open synchronously at 03:30 h, produce nectar exclusively at night, and have an explosive mechanism of pollen presentation. The flowers have pure white petals, release strong scents during anthesis, and are pollinated by nocturnal and diurnal bees. We recorded four nocturnal and 17 diurnal species as flower visitors, with females of nocturnal species of Ptiloglossa (Colletidae) being the most abundant. After an initial pollen-releasing visit, only a minor amount of pollen remains in a flower. Several floral traits favor visits by nocturnal bees: (1) night-time flower opening, (2) nectar production at night, (3) almost complete pollen release during the first flower visit, and (4) pure white petals and strong odor production prior to sunrise, facilitating visual and olfactory detection of flowers when light is dim.

Artificial light at night (ALAN) disrupts natural light–dark cycles and affects the behaviour, navigation, and activity of nocturnal pollinators. These disruptions reduce flower visitation and pollination efficiency, weakening reproductive success in night-blooming plants and threatening ecosystem stability. A structured literature review was conducted using Web of Science, Scopus, Google Scholar, and ScienceDirect. Studies focusing on ALAN’s behavioural, ecological, and pollination-related impacts on nocturnal pollinators were selected and synthesised. ALAN causes behavioural disorientation, altered foraging, and reduced pollen transfer in moths, beetles, bats, and nocturnal bees. White and green lights are most disruptive, leading to up to 62% declines in nocturnal visits and reduced fruit set. Long-term exposure contributes to declines in nocturnal pollinator diversity and reduced yields in crops dependent on night pollination. ALAN is an emerging global threat to pollination services. Mitigation through warm-spectrum lighting, reduced illumination, and ecological light management is essential to conserve nocturnal pollinators, maintain biodiversity, and support ecosystem and agricultural resilience.

Summary 1. We related above-ground biomass allocation to light interception by trees and lianas growing in three tropical rain forest stands that were 0.5, 2 and 3-year-old regeneration stages after slash and burn agriculture. 2. Stem height and diameter, leaf angle, the vertical distribution of total above-ground biomass and leaf longevity were measured in individuals of three short-lived pioneers (SLP), four later successional species (LS) and three lianas (L). Daily light capture per individual ( Φ d ) was calculated with a canopy model. Mean daily light interception per unit leaf area ( Φ area ), leaf mass ( Φ leaf mass ) and above-ground mass ( Φ mass ) were used as measures of instantaneous efficiency of biomass use for light capture. 3. With increasing stand age, vegetation height and leaf area index increased while light at the forest floor declined from 34 to 5%. The SLP, Trema micanthra and Ochroma pyramidale , dominated the canopy early in succession and became three times taller than the other species. SLP had lower leaf mass fractions and leaf area ratios than the other groups and this difference increased with stand age. 4. Over time, the SLP intercepted increasingly more light per unit leaf mass than the other species. Lianas, which in the earliest stage were self-supporting and started climbing later on, gradually became taller at a given mass and diameter than the trees. Yet, they were not more efficient than trees in light interception. 5. SLP had at least three-fold shorter leaf life spans than LS and lianas. Consequently, total light interception calculated over the mean life span of leaves ( Φ leaf mass total = Φ area × SLA death leaves × leaf longevity) was considerably lower for the SLP than for the other groups. 6. Synthesis . We suggest that early dominance in secondary forest is associated with a high rate of leaf turnover which in turn causes inefficient long-term use of biomass for light capture, whereas persistence in the shade is associated with long leaf life spans. This analysis shows how inherent tradeoffs in crown and leaf traits drive long-term competition for light, and it presents a conceptual tool to explain why early dominants are not also the long-term dominants.

Plant-pollinator interactions are key for the reproduction of wild plants and for food security. However, the role nocturnal pollinators play in wild plant communities is not yet clear. Specifically, it has rarely been studied whether nocturnal pollinators are comparable to diurnal ones in the pollination services they deliver in plant communities. We tested whether nocturnal pollinators have the potential to provide high pollination services to the plants they visit by carrying high conspecific pollen loads. We studied pollen loads carried by nocturnal and diurnal pollinators captured over 24-hour cycles in co-flowering plant communities in Swiss ruderal meadows. Pollen load was less diverse at night, and the proportion of conspecific pollen carried by nocturnal pollinators was higher than that of diurnal ones. Because the majority of plant species visited at night were also visited during the day, floral resource availability could drive the observed patterns in pollen load and amount of conspecific pollen. Nevertheless, nocturnal pollinators do not only carry pollen but can remove and potentially deposit conspecific pollen to the plants they visit. Therefore, pollinators active at night might be an important pollination vector for more plant species than previously thought and should not be neglected in pollination studies.

Bees exemplify flights under bright sunlight. A few species across bee families have evolved nocturnality, displaying remarkable adaptations to overcome limitations of their daylight-suited apposition eyes. Phase inversion to nocturnality in a minority of bees that co-exist with diurnal bees provides a unique opportunity to study ecological benefits that mediate total temporal niche shifts. While floral traits and sensory modalities associated with the evolution of classical nocturnal pollination syndromes, e.g. by bats and moths, are well-studied, nocturnality in bees represents a poorly understood, recently invaded, extreme niche. To test the competitive release hypothesis, we examine how nocturnality shapes foraging by comparing pollen loads, nest pollen, and flower visitation of sympatric nocturnal and diurnal carpenter bees. We predicted that nocturnal bees primarily use night-blooming flowers, show little/no resource overlap with diurnal species and competitive release favors night-time pollen collection for provisioning. Contrarily, we found substantial resource overlap between nocturnal and diurnal bees. Flower opening times, floral longevity and plant abundance did not define nocturnal flower use. Smaller pollen loads on nocturnal foragers suggest subsistence on resource leftovers largely from diurnal flowers. Greater pollen types/diversity on nocturnal foragers indicate lower floral constancy compared to diurnal congenerics. Reduced activity during new moon compared to full moon suggests constraints to nocturnal foraging. Invasion and sustenance within the nocturnal niche is characterized by: (i) opportunistic foraging on residual resources as indicated by smaller pollen loads, extensive utilization of day-blooming flowers and substantial overlap with diurnal bees, (ii) generalization at two levels�between and within foraging trips as indicated by lower floral constancy, (iii) reduced foraging on darker nights, indicating visual constraints despite sensitive optics. This together with smaller populations and univoltine breeding in nocturnal compared to multivoltine diurnal counterparts suggest that nocturnality imposes substantial fitness costs. In conclusion, the evolution of nocturnality in bees is accompanied by resource generalization instead of specialization. Reduced floral constancy suggests differences in foraging strategies of nocturnal and diurnal bees which merits further investigation. The relative roles of competition, floral rewards and predators should be examined to fully understand the evolution and maintenance of nocturnality in bees. © Copyright © 2020 Somanathan, Krishna, Jos, Gowda, Kelber and Borges.

Bees are the most important diurnal pollinators of angiosperms. In several groups of bees a nocturnal/crepuscular habit developed, yet little is known about their role in pollination and whether some plants are adapted specifically to these bees. We used a multidisciplinary approach to investigate the reproductive biology and to understand the role of nocturnal/crepuscular bees in pollination of Campomanesia phaea (Myrtaceae), popularly named cambuci. We studied the floral biology and breeding system of C.phaea. We collected the floral visitors and tested the pollinators' effectiveness. We also determined the floral scents released at night and during daytime, and studied behavioural responses of crepuscular/nocturnal bees towards these scents. The flowers of cambuci were self-incompatible and had pollen as the only resource for flower visitors. Anthesis lasted around 14h, beginning at 04:30h at night. The flowers released 14 volatile compounds, mainly aliphatic and aromatic compounds. We collected 52 species of floral visitors, mainly bees. Nocturnal and crepuscular bees (four species) were among the most frequent species and the only effective pollinators. In field bioassays performed at night, nocturnal/crepuscular bees were attracted by a synthetic scent blend consisting of the six most abundant compounds. This study describes the first scent-mediated pollination system between a plant and its nocturnal bee pollinators. Further, C.phaea has several floral traits that do not allow classification into other nocturnal pollination syndromes (e.g. pollinator attraction already before sunrise, with pollen as the only reward), instead it is a plant specifically adapted to nocturnal bees.

Early pioneer species share life histories enabling them to colonize disturbed sites, but how much they differ demographically and how such differentiation determines pioneer species turnover during succession are still open questions. Here, we approached these issues by comparing the demography of dominant pioneer tree species during the secondary succession of tropical rainforest in Southeast Mexico. We assessed changes in population density, population structure, vital rates and intrinsic population growth rate (r) of the pioneer species Trema micrantha, Cecropia peltata and Trichospermum mexicanum during the first 35 years of succession. For this, we combined chronosequence and long‐term (from 2000 to 2018) data from 14 abandoned cornfields with 0.5–35 years fallow age. Trema colonized and disappeared first during succession (<15 years), followed by Cecropia (<28) and Trichospermum (>31). All species exhibited hump‐shaped successional trajectories of population density and biomass with Trema reaching a peak first, followed by Cecropia and later Trichospermum. Species exhibited a fast reduction in r with fallow age, with Trema reaching negative growth rates (r < 0) in the third, Cecropia in the fourth, and Trichospermum in the seventh year of succession. Recruitment, growth and mortality rates of seedlings and juveniles defined the period of population increase and the age of succession at which each species reached maximum density and biomass. The mortality rate in mature stages determined how long each species persisted during succession. An important variation in species replacement occurred among study sites. In some sites, one species was abundant and the others were almost absent, while it was the opposite in other sites. We inferred that priority inhibitory effects operated among species during the field colonization. Synthesis. Although Trema, Cecropia and Trichospermum are considered typical pioneer trees, these species differed importantly in their demographic attributes during succession. The speed at which r declined with age of succession indicated the moment at which each species reached its maximum density and species replacement sequence during succession. However, inter‐specific priority inhibitory effects during field colonization may also be involved in the chance of colonization and replacement between species with similar regeneration strategies.

Summary Plant–pollinator interactions are crucial for the reproduction of most angiosperms. When faced with perturbations, plant–pollinator networks might be robust mainly due to the presence of highly generalist species. Perturbations can, in turn, affect how pollinators exploit their food sources and therefore their degree of generalization. In particular, generalization of pollinators might vary with forager density. At high densities floral resources available in plant communities would be more rapidly depleted than at low densities. According to optimal foraging theory (OFT), this decrease in resources should lead to an increase in diet breadth. We investigated the impact of pollinator density on diet breadth of Bombus terrestris. We recorded the individual foraging behaviour of bumblebees from eight colonies. They foraged in presence of either one or several conspecifics on experimental plant communities composed of five plant species. Diet breadth was calculated as the number of plant species visited, as well as by the Levins index. We analyzed the effect of forager density on diet breadth at both the individual and the colony levels. We found that forager density affected degree of generalization at individual and colony levels. A more competitive environment increased individual generalization, as predicted by OFT, and decreased the variability in generalization across colonies. Moreover, we found that bumblebee size was positively related to the amplitude of diet breadth change. Synthesis. Our study sheds light on an additional level of complexity of plant–pollinator systems, showing that pollinator diet breadth is a flexible trait which results from behavioural adaptation to resource availability. More generally, changes in foraging insects’ diet via competition for resources are likely to ensue from anthropogenic ecosystem disturbance and to impact upon the functioning of plant–pollinator networks.

Patterns of resource use (i.e. dietary richness, breadth and overlap) for the coexisting but differently sized species Calamoecia lucasi and Boeckella minuta were examined in specimens collected from Wallerawang Reservoir between April 1986 and September 1987. Significant differences in the dietary richness and dietary breadth were found between the species. Dietary overlap, as measured by Schoener's index, fluctuated within a relatively low range throughout the time interval. The effective resource partitioning may account for the perennial coexistence of these species. Since the degree of resource overlap cannot be directly related to the extent of competition, further experimental studies are necessary to determine how important the resource partitioning is in processes structuring associations of calanoid species.

Pollinating insects are critical to ecosystem stability and food security. Concerns about the impact of insect declines have therefore seen increased research on the role of wild pollinators in cropping systems. However, this research has predominantly focused on diurnal pollinators such as bees and flies, leaving the role of nocturnal pollinators poorly understood in comparison.Here, we review the literature on nocturnal pollinators of food crops and medicinal plants by undertaking an abstract, title, and keyword literature search in Web of Science Core Collection [v.5.32].We found interactions recorded between plants and nocturnal pollinators for 52 plant families, with Cactaceae, Fabaceae and Asparagaceae being mentioned most frequently in the context of nocturnal pollination. We identified 81 animal families that behave as nocturnal crop pollinators, with Sphingidae and Noctuidae moths and Phyllostomidae bats being mentioned most frequently.The evidence to support claims of pollination by nocturnally active animals varied in strength and mostly involved observations of flower visitation or pollination being inferred based on floral traits. There was a lack of strong experimental evidence. Detailed experimental work, such as pollinator exclusion experiments, is therefore required to corroborate the patterns we have discovered.Our review is biased towards publications in the English language, but despite this our study shows tropical regions such as Brazil appear to be hotspots for nocturnal crop pollination.Policy implications. Our findings suggest that nocturnal pollinators visit a large range of crop plants, and may be more important to ecosystem function and food production than currently thought. Current policies in cropping systems implemented to protect bees, such as regulations on pesticide use, are unlikely to also protect nocturnal pollinators. As we develop a better understanding of the importance of nocturnal pollinators for crop plants, many of these regulations may need to be updated to ensure pollination service is not being compromised.

Vertical and temporal patterns of tree architecture and their relationship with woody plant crown exposure index varied with succession in evergreen broad-leaved forests in eastern China. Linking temporal pattern of tree architecture with changing light conditions through forest succession is important for understanding plant adaptive strategies. We determined vertical (canopy, sub-canopy, and understory species) and temporal (pioneer, mid-successional, and climax species) patterns of tree height, stem basal area, crown area and depth, leaf coverage, leaf convergence (clumped vs. dispersed leaves) and stretch direction of branches (vertical, leaned and horizontal branches) and their relationship with crown exposure index (CEI) for woody plants among three successional series in subtropical evergreen broad-leaved forests in eastern China. The series included three stages: secondary shrub (early-), young (mid-) and climax forests (late-successional stage). Tree height, crown area and depth, stem basal diameter and leaf coverage were the greatest in canopy trees, intermediate in sub-canopy trees, and the smallest in understory plants among the three successional stages; the above parameters and the proportions of dispersed leaves and leaned branches were climax > mid-successional > pioneer species. In contrast, the proportions of clumped leaves and vertical branches were pioneer > mid-successional > climax species. Between canopy and understory species, the patterns of branch stretch direction and leaf convergence were not consistent among the three successional stages. Tree height, crown area and depth, leaf coverage, and stem basal diameter were positively correlated with CEI for both vertically different species and successional species. Tree architectural traits were interactively affected by forest age and CEI (p < 0.01). In conclusion, tree architecture varies with changes in both forest vertical structure and successional status. The large variability of tree architectural traits in relation to CEI and forest age reflects a strong control of light availability that affects biomass allocation strategies of trees. Our study demonstrated that light induced shift in tree architecture may result in species coexistence through divergence of vertical space, as well as species replacement through forest succession.

Patterns of inter- and intra-specific resource use were examined between bill morphs of the African finch Pyrenestes ostrinus and Quelea erythrops. On my study area in south-central Cameroon diet overlap and breadth were examined after the major dry season when food was most limiting. Overlap values between P. ostrinus and O. erythrops declined with food supply, suggesting that interspecific competition occurred. Changes in the diets of small morphs which had bills more similar in size to Q. erythrops were primarily responsible for this decline. In contrast, diet overlap between morphs increased as food supply declined. Diet breath of small morphs also increased while crop size declined. Diet breadth and crop size in large morphs remained low throughout the study. These results, examined within the context of bill morphology, finch abundance, food supply and crop fullness are consistent with intraspecific competition occurring between morphs. Additionally, small morph and Q. erythrops exploitation of scarce supplies of soft seeds may be responsible for large morphs specializing on hard seeds during the non-breeding season

Diurnal versus nocturnal pollination in a subalpine wetland: From network structure to plant reproduction

Oil palm plantations have become a major agricultural landscape in the Neotropics, especially in Colombia, the largest oil palm producer in the region. The Orinoco, or Llanos, region of eastern Colombia is predicted to increase expansion for palm oil acreage over the coming decades, with implications for biodiversity loss. Describing dietary diversity of frugivorous bats is a functional approach to understanding the effect of oil palm dominated landscapes on bat-fruit interactions. Our objective was to characterize the diet of the dominant (most abundant) bat species present in an oil palm landscape from the Colombian Llanos. We compared diet breadth of bat species on the basis of Levin’s index and we assessed differences in the frequency of seed consumption through Chi-square tests (χ2). We calculated diet overlap with a Morisita-Horn index. We characterized diet breadth and overlap for four taxa (three species and one species complex) of bats from 149 fecal samples and 344 individual bats, from which we identified 13 seed species. Dietary composition differed significantly among bat species, as did diet breadth. Diet breadth was highest in Carollia spp. and lowest in Sturnira lilium. The greatest degree of diet overlap ocurred between Artibeus lituratus and A. planirostris and the lowest overlap between S. lilium and all the other species. Considering the functional identity of the plants dispersed by bats in our sample, where most of them are pioneer species that colonize disturbed areas, it is fundamental to preserve habitats such as forest fragments that maintain bat assemblages with diverse diets in agriculturally disturbed landscapes. This may have important implications in future restoration process at these sites.