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.

Picking pithy plants: Pith selectivity by wild white-faced capuchin monkeys, Cebus imitator.

Understanding diet selectivity is a longstanding goal in primate ecology. Deciphering when and why primates consume different resources can provide insights into their nutritional ecology as well as adaptations to food scarcity. Plant pith, the spongy interior of plant stems, is occasionally eaten by primates, but the context is poorly understood. We examine the ecological, mechanical, chemical, and nutritional basis of plant pith selection by a wild, frugivorous-omnivorous primate (Cebus imitator). We test the hypothesis that pith is a fallback food, that is, consumed when fruit is less abundant, and test for differences between plant species from which pith is eaten versus avoided. We collected 3.5 years of capuchin pith consumption data to document dietary species and analyzed "pith patch visits" in relation to fruit availability, visits to fruit patches, and climatic seasonality. We analyzed dietary and non-dietary species for relative pith quantity, mechanical hardness, odor composition, and macronutrient concentrations. Capuchins ate pith from 11 of  ~300 plant species common in the dry forest, most commonly Bursera simaruba. We find that pith consumption is not directly related to fruit availability or fruit foraging but occurs most frequently (84% of patch visits) during the months of seasonal transition. Relative to common non-dietary species, dietary pith species have relatively higher pith quantity, have softer outer branches and pith, and contain more terpenoids, a class of bioactive compounds notable for their widespread medicinal properties. Our results suggest that greater pith quantity, lower hardness, and a more complex, terpenoid-rich odor profile contribute to species selectivity; further, as pith is likely to be consistently available throughout the year, the seasonality of pith foraging may point to zoopharmacognosy, as seasonal transitions typically introduce new parasites or pathogens. Our study furthers our understanding of how climatic seasonality impacts primate behavior and sheds new light on food choice by an omnivorous primate.

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.

Linking bacteria, volatiles and insects on carrion: the role of temporal and spatial factors regulating inter-kingdom communication via volatiles.

Multi-kingdom community complexity and the chemically mediated dynamics between bacteria and insects have recently received increased attention in carrion research. However, the strength of these inter-kingdom interactions and the factors that regulate them are poorly studied. We used 75 piglet cadavers across three forest regions to survey the relationship between three actors (epinecrotic bacteria, volatile organic compounds (VOCs) and flies) during the first 4 days of decomposition and the factors that regulate this interdependence. The results showed a dynamic bacterial change during decomposition (temperature-time index) and across the forest management gradient, but not between regions. Similarly, VOC emission was dynamic across a temperature-time index and the forest management gradient but did not differ between regions. However, fly occurrence was dynamic across both space and time. The strong interdependence between the three actors was mainly regulated by the temperature-time index and the study regions, thereby revealing regulation at temporal and spatial scales. Additionally, the actor interdependence was stable across a gradient of forest management intensity. By combining different actors of decomposition, we have expanded our knowledge of the holistic mechanisms regulating carrion community dynamics and inter-kingdom interactions, an important precondition for better describing food web dynamics and entire ecosystem functions.

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.

Assessing urinary odours across the oestrous cycle in a mouse model using portable and benchtop gas chromatography-mass spectrometry.

For female mammals, communicating the timing of ovulation is essential for reproduction. Olfactory communication via volatile organic compounds (VOCs) can play a key role. We investigated urinary VOCs across the oestrous cycle using laboratory mice. We assessed the oestrous stage through daily vaginal cytology and analysed urinary VOCs using headspace gas chromatography-mass spectrometry (GC-MS), testing a portable GC-MS against a benchtop system. We detected 65 VOCs from 40 samples stored in VOC traps and analysed on a benchtop GC-MS, and 15 VOCs from 90 samples extracted by solid-phase microextraction (SPME) and analysed on a portable GC-MS. Only three compounds were found in common between the two techniques. Urine collected from the fertile stages of the oestrous cycle had increased quantities of a few notable VOCs compared with urine from non-fertile stages. These VOCs may be indicators of fertility. However, we did not find significant differences in chemical composition among oestrous stages. It is possible that changes in VOC abundance were too small to be detected by our analytical methods. Overall, the use of VOC traps combined with benchtop GC-MS was the more successful of the two methods, yet portable GC-MS systems may still have utility for some in situ applications.

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.

Fruit scent and observer colour vision shape food-selection strategies in wild capuchin monkeys.

The senses play critical roles in helping animals evaluate foods, including fruits that can change both in colour and scent during ripening to attract frugivores. Although numerous studies have assessed the impact of colour on fruit selection, comparatively little is known about fruit scent and how olfactory and visual data are integrated during foraging. We combine 25 months of behavioural data on 75 wild, white-faced capuchins (Cebus imitator) with measurements of fruit colours and scents from 18 dietary plant species. We show that frequency of fruit-directed olfactory behaviour is positively correlated with increases in the volume of fruit odours produced during ripening. Monkeys with red-green colour blindness sniffed fruits more often, indicating that increased reliance on olfaction is a behavioural strategy that mitigates decreased capacity to detect red-green colour contrast. These results demonstrate a complex interaction among fruit traits, sensory capacities and foraging strategies, which help explain variation in primate behaviour.

Fruit scent as an evolved signal to primate seed dispersal.

The tremendous diversity of floral and fruit traits is, to a large extent, a set of adaptations that promote plant reproduction through animal pollinators and seed dispersers. Yet, it is still unknown whether fruit scent is a by-product of fruit maturation or an evolved communication channel with animal mutualists. We show that in species that specialize on seed dispersal by lemurs-an olfactorily oriented primate-fruits increase scent production and change their chemical composition significantly more than sympatric species whose seeds are largely dispersed by birds. We further show that lemurs use these shifts in fruit scent to identify ripe fruits. These results show that fruit scent is an evolved communication system that facilitates animal-plant mutualism.

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.

Function of bacterial community dynamics in the formation of cadaveric semiochemicals during in situ carcass decomposition.

The decomposition of dead mammalian tissue involves a complex temporal succession of epinecrotic bacteria. Microbial activity may release different cadaveric volatile organic compounds which in turn attract other key players of carcass decomposition such as scavenger insects. To elucidate the dynamics and potential functions of epinecrotic bacteria on carcasses, we monitored bacterial communities developing on still-born piglets incubated in different forest ecosystems by combining high-throughput Illumina 16S rRNA sequencing with gas chromatography-mass spectrometry of volatiles. Our results show that the community structure of epinecrotic bacteria and the types of cadaveric volatile compounds released over the time course of decomposition are driven by deterministic rather than stochastic processes. Individual cadaveric volatile organic compounds were correlated with specific taxa during the first stages of decomposition which are dominated by bacteria. Through best-fitting multiple linear regression models, the synthesis of acetic acid, indole and phenol could be linked to the activity of Enterobacteriaceae, Tissierellaceae and Xanthomonadaceae, respectively. These conclusions are also commensurate with the metabolism described for the dominant taxa identified for these families. The predictable nature of in situ synthesis of cadaveric volatile organic compounds by epinecrotic bacteria provides a new basis for future chemical ecology and forensic studies.

Fruit Odor as A Ripeness Signal for Seed-Dispersing Primates? A Case Study on Four Neotropical Plant Species.

Fleshy fruits contain a myriad of secondary metabolites that may fulfill various non-mutually exclusive ecological functions. Among them are defense against pathogens and herbivores, manipulation of frugivores' gut retention time, or controlling the germination process. In addition, it has been suggested that aroma compounds may be used as fruit-selection cues by frugivores, and that plants may be under selection to provide a reliable signal for ripeness to seed-dispersal vectors through ripe fruit aroma. A previous project demonstrated that fruit odor of two Neotropical primate-dispersed plant species can be used by primates to identify ripe fruits. Here, we provide data supporting the hypothesis that olfactory conspicuousness of ripeness in these two species may be an evolved signal rather than a cue exploited by primates. We analyzed the odors of ripe and unripe fruits of the two species along with odors of two sympatric species whose main dispersal vector is passerine birds. We show that only primate-dispersed species significantly change their odor profiles upon ripening. Thus, odor of bird-dispersed species is not informative regarding their ripeness level and is likely to fulfill other functions. We discuss these data in light of the multiple hypotheses for the presence of fruit secondary metabolites, and we offer a roadmap for future studies to establish the hypothesis that fruit odor is an evolved signal for ripeness.

Chemical recognition of fruit ripeness in spider monkeys (Ateles geoffroyi).

Primates are now known to possess well-developed olfactory sensitivity and discrimination capacities that can play a substantial role in many aspects of their interaction with conspecifics and the environment. Several studies have demonstrated that olfactory cues may be useful in fruit selection. Here, using a conditioning paradigm, we show that captive spider monkeys (Ateles geoffroyi) display high olfactory discrimination performance between synthetic odor mixtures mimicking ripe and unripe fruits of two wild, primate-consumed, Neotropical plant species. Further, we show that spider monkeys are able to discriminate the odor of ripe fruits from odors that simulate unripe fruits that become increasingly similar to that of ripe ones. These results suggest that the ability of spider monkeys to identify ripe fruits may not depend on the presence of any individual compound that mark fruit ripeness. Further, the results demonstrate that spider monkeys are able to identify ripe fruits even when the odor signal is accompanied by a substantial degree of noise.

Led by the nose: Olfaction in primate feeding ecology.

Olfaction, the sense of smell, was a latecomer to the systematic investigation of primate sensory ecology after long years in which it was considered to be of minor importance. This view shifted with the growing understanding of its role in social behavior and the accumulation of physiological studies demonstrating that the olfactory abilities of some primates are on a par with those of olfactory-dependent mammals such as dogs and rodents. Recent years have seen a proliferation of physiological, behavioral, anatomical, and genetic investigations of primate olfaction. These investigations have begun to shed light on the importance of olfaction in the process of food acquisition. However, integration of these works has been limited. It is therefore still difficult to pinpoint large-scale evolutionary scenarios, namely the functions that the sense of smell fulfills in primates' feeding ecology and the ecological niches that favor heavier reliance on olfaction. Here, we review available behavioral and physiological studies of primates in the field or captivity and try to elucidate how and when the sense of smell can help them acquire food.