What drives seed dispersal effectiveness?

Seed dispersal is a critical phase in plant reproduction and forest regeneration. In many systems, the vast majority of woody species rely on seed dispersal by fruit-eating animals. Animals differ in their size, movement patterns, seed handling, gut physiology, and many other factors that affect the number of seeds they disperse, the quality of treatment each individual seed receives, and consequently their relative contribution to plant fitness. The seed dispersal effectiveness framework (SDE) was developed to allow systematic and standardized quantification of these processes, offering a potential for understanding the large-scale dynamics of animal-plant interactions and the ecological and evolutionary consequences of animal behavior for plant reproductive success. Yet, despite its wide acceptance, the SDE framework has primarily been employed descriptively, almost always in the context of local systems. As such, the drivers of variation in SDE across systems and the relationship between its components remain unknown. We systematically searched studies that quantified endozoochorous SDE for multiple animal species dispersing one or more plant species in a given system and offered an integrative examination of the factors driving variation in SDE. Specifically, we addressed three main questions: (a) Is there a tradeoff between high dispersal quality and quantity? (b) Does animal body mass affect SDE or its main components? and (c) What drives more variation in SDE, seed dispersal quality, or quantity? We found that: (a) the relationship between quality and quantity is mediated by body size; (b) this is the result of differential relationships between body mass and the two components, while total SDE is unaffected by body mass; (c)neither quality nor quantity explain more variance in SDE globally. Our results also highlight the need for more standardized data to assess large-scale patterns in SDE.

Fruit scent as an honest signal for fruit quality.

BACKGROUND: Fleshy fruits evolved to be attractive to seed dispersers through various signals such as color and scent. Signals can evolve through different trajectories and have various degrees of reliability. The strongest substrate on which reliable signals can evolve is when there is an inherent link between signal and reward, rendering cheating costly or impossible. It was recently proposed that aliphatic esters in fruit scent may be predictive of sugar content due to their synthesis from products of sugar fermentation. We test this hypothesis on a case study of wild fig species (Ficus tiliifolia) from Madagascar, which relies on seed dispersal by lemurs. RESULTS: We found a strong positive correlation between signal (esters) and reward (sugar). We also found that non-esters, including direct fermentation products, in fruit scent do not indicate sugar levels, which implies that this relationship is not simply a product of fruit maturation wherein more mature fruits emit more scent and contain more sugar. CONCLUSIONS: While based on a single taxon, these results strongly support the hypothesis that a biochemical link between ester synthesis and sugar may render the ester fraction of fruit scent an honest signal for fruit quality, with consequences for animal sensory and feeding ecology, and the evolution of plants in the context of seed dispersal.

Madagascar Terrestrial Camera Survey Database 2021: A collation of protected forest camera surveys from 2007-2021.

Madagascar is a threatened global biodiversity hotspot and conservation priority, yet we lack broad-scale surveys to assess biodiversity across space and time. To fill this gap, we collated camera trap surveys, capturing species occurrences within Madagascar into a single standardized database. This data set includes nine distinct protected areas of Madagascar and encompasses 13 subprojects, 38 camera arrays, and 1156 sampling units (independent camera site per survey) within two important biodiversity eco-regions: western dry deciduous forest and eastern humid rainforest. Camera surveys were conducted from June 2007 to January 2021. The final data set includes 17 unique families of mammals (Bovidae, Canidae, Cheirogaleidae, Daubentoniidae, Equidae, Eupleridae, Felidae, Hominidae, Indriidae, Lemuridae, Lepilemuridae, Muridae, Nesomyidae, Pteropodidae, Soricidae, Suidae, Tenrecidae) comprising 45 species and 27 unique families of birds (Accipitridae, Acrocephalidae, Alcedinidae, Bernieridae, Brachypteraciidae, Caprimulgidae, Cisticolidae, Columbidae, Coraciidae, Corvidae, Cuculidae, Dicruridae, Mesitornithidae, Monarchidae, Motacillidae, Muscicapidae, Numididae, Phasianidae, Rallidae, Sarothruridae, Strigidae, Sturnidae, Sulidae, Threskiornithidae, Upupidae, Vangidae, Zosteropidae) comprising 58 species. Images were processed and verified by individual project data set creators and camera operation and species tables were then collated. The final product represents the first broad-scale freely available standardized formal faunal database for Madagascar. Data are available through this publication and at DOI: 10.5281/zenodo.5801806. These data will be useful for examining species-level and community-level trends in occurrence across space or time within Madagascar and globally, evaluating native and invasive species dynamics, and will aid in determining species conservation status and planning for at-risk species. There are no copyright restrictions; please cite this paper when using the data for publication.

In the eye of the beholder: Is color classification consistent among human observers?

Colorful displays have evolved in multiple plant and animal species as signals to mutualists, antagonists, competitors, mates, and other potential receivers. Studies of color have long relied on subjective classifications of color by human observers. However, humans have a limited ability to perceive color compared to other animals, and human biological, cultural, and environmental variables can influence color perception. Here, we test the consistency of human color classification using fruit color as a model system. We used reflectance data of 67 tropical fruits and surveyed 786 participants to assess the degree to which (a) participants of different cultural and linguistic backgrounds agree on color classification of fruits; and (b) human classification to a discrete set of commonly used colors (e.g., red, blue, green) corresponds to natural clusters based on light reflectance measures processed through visual systems of other animals. We find that individual humans tend to agree on the colors they attribute to fruits across language groups. However, these colors do not correspond to clearly discernible clusters in di- or tetrachromatic visual systems. These results indicate that subjective color categorizations tend to be consistent among observers and can be used for large synthetic studies, but also that they do not fully reflect natural categories that are relevant to animal observers.

Lessons Learned and Paths Forward for Rabies Dog Vaccination in Madagascar: A Case Study of Pilot Vaccination Campaigns in Moramanga District.

Canine rabies causes an estimated 60,000 human deaths per year, but these deaths are preventable through post-exposure prophylaxis of people and vaccination of domestic dogs. Dog vaccination campaigns targeting 70% of the population are effective at interrupting transmission. Here, we report on lessons learned during pilot dog vaccination campaigns in the Moramanga District of Madagascar. We compare two different vaccination strategies: a volunteer-driven effort to vaccinate dogs in two communes using static point vaccination and continuous vaccination as part of routine veterinary services. We used dog age data from the campaigns to estimate key demographic parameters and to simulate different vaccination strategies. Overall, we found that dog vaccination was feasible and that most dogs were accessible to vaccination. The static-point campaign achieved higher coverage but required more resources and had a limited geographic scope compared to the continuous delivery campaign. Our modeling results suggest that targeting puppies through community-based vaccination efforts could improve coverage. We found that mass dog vaccination is feasible and can achieve high coverage in Madagascar; however, context-specific strategies and an investment in dog vaccination as a public good will be required to move the country towards elimination.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Discovery of Lanama Virus, a Distinct Member of Species Kunsagivirus C (Picornavirales: Picornaviridae), in Wild Vervet Monkeys (Chlorocebus pygerythrus).

We report the discovery and sequence-based molecular characterization of a novel virus, lanama virus (LNMV), in blood samples obtained from two wild vervet monkeys (Chlorocebus pygerythrus), sampled near Lake Nabugabo, Masaka District, Uganda. Sequencing of the complete viral genomes and subsequent phylogenetic analysis identified LNMV as a distinct member of species Kunsagivirus C, in the undercharacterized picornavirid genus Kunsagivirus.

Sweet tooth: Elephants detect fruit sugar levels based on scent alone.

The ability to assess food quality is crucial to all organisms. Fleshy fruits are a major source of nutrients to various animals, and unlike most food sources, have evolved to be attractive and to be consumed by animals to promote seed dispersal. It has recently been established that fruit scent-the bouquet of volatile chemicals emitted by ripe fruit-is an evolved communication system between plants and animals. Further, it has been argued that chemicals that are synthesized from sugar and its products may be an honest signal for sugar content and fruit quality. Elephants are important seed dispersers for numerous species and possess an olfactory system that is likely to outperform most other animals. We tested the hypothesis that fruit scent signifies sugar content and that elephants are capable of assessing fruit sugar levels based on scent alone. Using a paired-choice test of marula fruits (Sclerocarya birrea) by semitame African elephants, we show that elephants are capable of identifying more sugar-rich fruits based on scent alone and that this is likely based on two chemical compounds: ethanol and ethyl acetate, both downstream products of sugar fermentation. These results shed light on the mechanisms driving elephant feeding ecology, plant signaling, and the coevolutionary process between angiosperms and animal seed dispersers.

The evolution of fruit scent: phylogenetic and developmental constraints.

BACKGROUND: Fruit scent is increasingly recognized as an evolved signal whose function is to attract animal seed dispersers and facilitate plant reproduction. However, like all traits, fruit scent is likely to evolve in response to conflicting selective pressures and various constraints. Two major constraints are (i) phylogenetic constraints, in which traits are inherited from ancestors rather than adapted to current conditions and (ii) developmental constraints, if phenotypes are limited by the expression of other traits within the individual. We tested whether phylogenetic constraints play a role in fruit scent evolution by calculating the phylogenetic signal in ripe fruits of 98 species from three study sites. We then estimated the importance of developmental constraints by examining whether ripe fruits tend to emit compounds that are chemically similar to, and share biosynthetic pathways with, compounds emitted by conspecific unripe fruits from which they develop. RESULTS: We show that closely related taxa are not more similar to each other than to very distinct taxa, thus indicating that fruit scent shows little phylogenetic signal. At the same time, although ripe and unripe fruits of the same species tend to emit different chemicals, they tend to employ chemicals originating from similar biosynthetic pathways, thus indicating that some developmental constraints determine ripe fruit scent. CONCLUSIONS: Our results highlight the complex landscape in which fruit scent has evolved. On one hand, fruit scent evolution is not limited by common ancestry. On the other hand, the range of chemicals that can be employed in ripe fruits is probably constrained by the needs of unripe fruits.

Ultraviolet radiation changes plant color.

BACKGROUND: Plant absorption of ultraviolet (UV) radiation can result in multiple deleterious effects to plant tissues. As a result, plants have evolved an array of strategies to protect themselves from UV radiation, particularly in the UV-B range (280-320 nm). A common plant response to UV exposure is investment in phenolic compounds that absorb damaging wavelengths of light. However, the inverse phenomenon - plant reflectance of UV to protect plant tissues - has not previously been explored. In a paired experiment, we expose half of our sample (N = 108) of insect-pollinated plants of the cultivar Zinnia Profusion Series to UV radiation, and protect the other half from all light < 400 nm for 42 days, and measure leaf and flower reflectance using spectroscopy. We compare UV-B reflectance in leaves and flowers at the beginning of the experiment or flowering, and after treatment. RESULTS: We find that plants protected from UV exposure downregulate UV-B reflectance, and that plants exposed to increased levels of UV show trends of increased UV-B reflectance. CONCLUSIONS: Our results indicate that upregulation of UV-B reflecting pigments or structures may be a strategy to protect leaves against highly energetic UV-B radiation.

Signal and reward in wild fleshy fruits: Does fruit scent predict nutrient content?

Plant species with fleshy fruits offer animals rewards such as sugar, protein, and fat, to feed on their fruits and disperse their seeds. They have also evolved visual and olfactory signals indicating their presence and ripeness.In some systems, fruit color serves as a reliable visual signal of nutrient content. Yet even though many volatile chemicals used as olfactory signals derive from nutrients animals seek, it is still unknown whether fruit scent encodes information regarding nutrient content in wild fruits.We examine the relationship between olfactory signals and nutrient rewards in 28 fruiting plant species in Madagascar. We measured the relative amounts of four chemical classes in fruit scent using gas chromatography and mass spectrometry, as well as the relative amounts of sugar and protein in fruit pulp.We found that protein levels are not associated with elevated amounts of chemically related volatile compounds in fruit scent. In contrast, sugar content is strongly associated with the chemical composition of fruit scent.To our knowledge, this is the first research to explore the connection between fruit chemical signals and nutrient rewards. Our results imply that in the case of sugar, fruit scent is predictive of nutrient content and hence an honest signal.

Causative agent of canine heartworm (Dirofilaria immitis) detected in wild lemurs.

The lemurs of Madagascar are threatened by human activities. We present the first molecular detection of canine heartworm (Dirofilaria immitis) in a wild non-human primate, the mouse lemur (Microcebus rufus). Zoonotic D. immitis infection has been associated with clinical pathology that includes serious and often fatal cardiac and pulmonary reactions. With human encroachment and associated increases in free-roaming dog populations in Madagascar, we examined lemurs for zoonotic canid pathogens. D. immitis presents a new potential conservation threat to lemurs. We highlight the need for wide-ranging and effective interventions, particularly near protected areas, to address this growing conservation issue.

The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists.

The adaptive significance of fruit colour has been investigated for over a century. While colour can fulfil various functions, the most commonly tested hypothesis is that it has evolved to increase fruit visual conspicuousness and thus promote detection and consumption by seed dispersing animals. However, fruit colour is a complex trait which is subjected to various constraints and selection pressures. As a result, the effect of animal selection on fruit colour are often difficult to identify, and several studies have failed to detect it. Here, we employ an integrative approach to examine what drives variation in fruit colour. We quantified the colour of ripe fruit and mature leaves of 97 tropical plant species from three study sites in Madagascar and Uganda. We used phylogenetically controlled models to estimate the roles of phylogeny, abiotic factors, and dispersal mode on fruit colour variation. Our results show that, independent of phylogeny and leaf coloration, mammal dispersed fruits are greener than bird dispersed fruits, while the latter are redder than the former. In addition, fruit colour does not correlate with leaf colour in the visible spectrum, but fruit reflection in the ultraviolet area of the spectrum is strongly correlated with leaf reflectance, emphasizing the role of abiotic factors in determining fruit colour. These results demonstrate that fruit colour is affected by both animal sensory ecology and abiotic factors and highlight the importance of an integrative approach which controls for the relevant confounding factors.

Frugivores and the evolution of fruit colour.

The ecological function of fruit colour has been the focus of many studies. The most commonly tested hypothesis is that fruit colour has evolved to facilitate detection by seed-dispersing animals. We tested whether distributions of fruit colours are consistent with the hypothesis that colour is an evolved signal to seed dispersers using a comparative community approach. We compared the contrast between ripe fruits and leaf backgrounds at two sites, one in Madagascar where seed dispersers are primarily night-active, red-green colour-blind lemurs, and the other in Uganda, where most vertebrate seed dispersers are day-active primates and birds with greater capacity for colour vision. We show that fruits in Uganda have higher contrast against leaf background in the red-green and luminance channels whereas fruits in Madagascar contrast more in the yellow-blue channel. These results indicate that fruit colour has evolved to contrast against background leaves in response to the visual capabilities of local seed disperser communities.

Increased environmental sample area and recovery of Clostridium difficile spores from hospital surfaces by quantitative PCR and enrichment culture.

OBJECTIVE: Clostridium difficile spores play an important role in transmission and can survive in the environment for several months. Optimal methods for measuring environmental C. difficile are unknown. We sought to determine whether increased sample surface area improved detection of C. difficile from environmental samples. SETTING: Samples were collected from 12 patient rooms in a tertiary-care hospital in Toronto, Canada. METHODS: Samples represented small surface-area and large surface-area floor and bedrail pairs from single-bed rooms of patients with low (without prior antibiotics), medium (with prior antibiotics), and high (C. difficile infected) shedding risk. Presence of C. difficile in samples was measured using quantitative polymerase chain reaction (qPCR) with targets on the 16S rRNA and toxin B genes and using enrichment culture. RESULTS: Of the 48 samples, 64·6% were positive by 16S qPCR (geometric mean, 13·8 spores); 39·6% were positive by toxin B qPCR (geometric mean, 1·9 spores); and 43·8% were positive by enrichment culture. By 16S qPCR, each 10-fold increase in sample surface area yielded 6·6 times (95% CI, 3·2-13) more spores. Floor surfaces yielded 27 times (95% CI, 4·9-181) more spores than bedrails, and rooms of C. difficile-positive patients yielded 11 times (95% CI, 0·55-164) more spores than those of patients without prior antibiotics. Toxin B qPCR and enrichment culture returned analogous findings. CONCLUSIONS: Clostridium difficile spores were identified in most floor and bedrail samples, and increased surface area improved detection. Future research aiming to understand the role of environmental C. difficile in transmission should prefer samples with large surface areas.

Tree community structure reflects niche segregation of three parapatric squirrel monkey species (Saimiri spp.).

Integration between ecology and biogeography provides insights into how niche specialization affects the geographical distribution of species. Given that rivers are not effective barriers to dispersal in three parapatric species of squirrel monkeys (Saimiri vanzolinii, S. cassiquiarensis and S. macrodon) inhabiting floodplain forests of Central Amazonia, we tested whether forest structure and tree diversity may explain species differences in niche specialization and spatial segregation. We sampled 6617 trees of 326 species in three habitats (high várzea, low várzea and chavascal) used by three Saimiri species, and estimated tree species richness in each of them. For each tree, we measured variables known to influence habitat use in primates, such as crown area and presence of lianas, epiphytes and hemi-epiphytes. We used ANOVA to compare these variables and performed multivariate analyses (NMDS, ANOSIM and SIMPER) to evaluate dissimilarities in forest structure among each habitat inhabited by the three Saimiri species. We identified differences in the tree species richness, crown area and presence of lianas, epiphytes and hemi-epiphytes between the three habitats for all Saimiri species. NMDS demonstrated that areas of high and low várzeas occupied by S. vanzolinii were clearly separated from the other species. We also found that different plant species contributed to dissimilarity among Saimiri ranges. Our findings support the hypothesis that tree community structure may promote niche specialization and spatial segregation among primates. We discuss how these patterns could have been favored by historical changes in forest flood patterns, the evolutionary history of Saimiri spp., and past competition.

Comparison of gastrointestinal parasite communities in vervet monkeys.

Globally, habitat degradation is accelerating, especially in the tropics. Changes to interface habitats can increase environmental overlap among nonhuman primates, people, and domestic animals and change stress levels in wildlife, leading to changes in their risk of parasite infections. However, the direction and consequences of these changes are unclear, since animals may benefit by exploiting human resources (e.g., improving nutritional health by eating nutritious crops) and decreasing susceptibility to infection, or interactions with humans may lead to chronic stress and increased susceptibility to infection. Vervet monkeys are an excellent model to understand parasitic disease transmission because of their tolerance to anthropogenic disturbance. Here we quantify the gastrointestinal parasites of a group of vervet monkeys (Chlorocebus aethiops) near Lake Nabugabo, Uganda, that frequently overlaps with people in their use of a highly modified environment. We compare the parasites found in this population to seven other sites where vervet monkey gastrointestinal parasites have been identified. The vervets of Lake Nabugabo have the greatest richness of parasites documented to date. We discuss how this may reflect differences in sampling intensity or differences in the types of habitat where vervet parasites have been sampled.

The Paucity of Frugivores in Madagascar May Not Be Due to Unpredictable Temperatures or Fruit Resources.

The evolution of ecological idiosyncrasies in Madagascar has often been attributed to selective pressures stemming from extreme unpredictability in climate and resource availability compared to other tropical areas. With the exception of rainfall, few studies have investigated these assumptions. To assess the hypothesis that Madagascar's paucity of frugivores is due to unreliability in fruiting resources, we use statistical modeling to analyze phenology datasets and their environmental correlates from two tropical wet forests, the Réserve Naturelle Intégrale Betampona in Madagascar, and Kibale National Park in Uganda. At each site we found that temperature is a good environmental predictor of fruit availability. We found no evidence of a significant difference in the predictability of fruit availability between the two sites, although the shorter duration of phenological monitoring at Betampona (two years, versus 15 years at Kibale) limits our ability to infer long-term patterns. Comparisons of long-term temperature data from each site (15 years from Kibale and 14 from Betampona) indicate that temperature is more predictable at Betampona than at Kibale. However, there does appear to be a difference between the two sites in the total fruit availability at any given time, with fruit being generally less abundant at Betampona. Our results appear contrary to the prevailing hypothesis of a selective force imposed by unpredictable resource availability or temperature, and we suggest other possible explanations for Madagascar's unique biota.

Social Behaviours and Networks of Vervet Monkeys Are Influenced by Gastrointestinal Parasites.

Substantial research has shown that while some parasite infections can be fatal to hosts, most infections are sub-clinical and non-lethal. Such sub-clinical infections can nonetheless have negative consequences for the long-term fitness of the host such as reducing juvenile growth and the host's ability to compete for food and mates. With such effects, infected individuals are expected to exhibit behavioural changes. Here we use a parasite removal experiment to quantify how gastrointestinal parasite infections affect the behaviour of vervet monkeys (Chlorocebus aethiops) at Lake Nabugabo, Uganda. Behavioural profiles and the structure of nearest neighbour relationships varied significantly. As predicted, after deworming the duration of the resting events decreased, which is consistent with the idea that parasite infections are energetically costly. In contrast to what was predicted, we could not reject the null hypothesis and we observed no change in either the frequency or duration of grooming, but we found that the duration of travel events increased. A network analysis revealed that after deworming, individuals tended to have more nearest neighbours and hence probably more frequent interactions, with this effect being particularly marked for juveniles. The heightened response by juveniles may indicate that they are avoiding infected individuals more than other age classes because it is too costly to move energy away from growth. We consider that populations with high parasite burden may have difficulties developing social networks and behaviours that could have cascading effects that impact the population in general.