Sensory Basis of Food Detection in Wild <Emphasis Type="BoldItalic">Microcebus murinus</Emphasis>

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.     

Cattle use visual cues to track food locations

We tested the hypothesis that cattle aided by visual cues would be more efficient than uncued animals in locating and consuming foods placed in either fixed or variable locations within a 0.64-ha experimental pasture. Eight yearling steers were randomly selected and trained to associate traffic barricades and traffic cones with high- (oat-barley mixture) and low- (straw) quality foods, respectively. Initially steers were randomly assigned to 1 of 4 food location/visual cue treatments: fixed locations/with cues (F/C), variable locations/with cues (V/C), fixed locations/no cues (F/NC), or variable locations/no cues (V/NC). High- and low-quality foods and their respective cue (or no cue) were placed in the experimental pasture. Individual animals were allowed to explore the pasture for 10 min twice per day every other day for 1 week. Minutes until feeding, first feed type consumed (i.e., high-quality, low-quality, or no food consumed), animal location and activity (i.e., feeding, standing, or moving), and total intake of high- and low-quality feed were recorded during each 10-min trial. At the end of each week, location/visual cue treatments were randomly assigned to another 2 steers, which permitted an independent test of each animal in each treatment over a 4-week period. Animals in the F/C and V/C treatments took about 2 min to initially locate and consume a food, compared to F/NC and V/NC animals who took nearly 4 and 6 min, respectively. The high-quality food was the first food located and consumed by F/C, V/C, F/NC, and V/NC animals during 79, 77, 67, and 54% of sampling occasions, respectively. Cued animals typically spent more time feeding (P=0.0004) and less time standing (P=0.005) than uncued animals. Cued animals had a higher mean intake than uncued animals of high- (P=0.001) and low- (P=0.04) quality food. Mean high-quality intake for F/C, V/C, F/NC, and V/NC treatments was 266, 245, 214, and 126 (+/-22) g, respectively; mean low-quality intake for the same treatments was 36, 32, 12, and 10 (+/-10) g. Cued animals also consumed more food per distance traveled than uncued animals (P=0.005). Animals located food quicker (P=0.03) and consumed more high-quality food (P=0.02) when food locations were constant than when they were variable. Our data strongly indicate that cattle can learn to associate visual cues with disparate food qualities and use this information to forage more efficiently in both fixed and variable foraging environments.     

Comparing apples and oranges—the influence of food mechanical properties on ingestive bite sizes in lemurs

Previously we found that Maximum Ingested Bite Size (V_b)—the largest piece of food that an animal will ingest whole without biting first—scales isometrically with body size in 17 species of strepsirrhines at the Duke Lemur Center (DLC). However, because this earlier study focused on only three food types (two with similar mechanical properties), it did not yield results that were easily applied to describing the broad diets of these taxa. Expressing V_b in terms of food mechanical properties allows us to compare data across food types, including foods of wild lemurs, to better understand dietary adaptations in lemurs. To this end, we quantified V_b in five species of lemurs at the DLC representing large and small frugivores and folivores using ten types of food that vary widely in stiffness and toughness to determine how these properties relate to bite sizes. We found that although most species take smaller bites of stiffer foods, this negative relationship was not statistically significant across the whole sample. However, there is a significant relationship between bite size and toughness. All three of the more frugivorous taxa in our sample take significantly smaller bites of tougher foods. However, the two more folivorous lemurs do not. They take small bites for all foods. This suggests that the species most adapted to the consumption of tough foods do not modulate their ingestive sizes to accommodate larger pieces of weak foods. Am J Phys Anthropol 157:513–518, 2015. © 2015 Wiley Periodicals, Inc.     

Additive and synergistic integration of multimodal cues of both hosts and non-hosts during host selection by woodboring insects

Host selection by herbivorous insects is primarily thought to depend on attraction to olfactory cues emitted from the host species. However, the discrimination of these hosts from non-host species may also arise from the adaptive detection and avoidance of non-host cues, including visual characteristics. Many generalist, conifer-colonising beetles, for example, use characteristic volatiles to identify and discriminate against non-host angiosperm trees such as aspens and birches while flying. These trees also differ in bark reflectance characteristics, which could also mediate host/non-host discrimination by interacting with semiochemicals. We tested this hypothesis by evaluating the responses of eight species of polyphagous woodboring beetles to traps which simulated the visual appearance of coniferous hosts (black) and angiosperm non-hosts (white), and which were baited with host or non-host volatiles. As predicted, three species of large woodboring beetle and a woodboring wasp all avoided white, non-host-simulating traps that were baited with attractive kairomones, and preferred black, host-simulating traps. Conversely, three ambrosia beetle species demonstrated weaker visual preferences, possibly because they preferentially colonise fallen hosts that would transmit less accurate visual information. However, the ambrosia beetle Trypodendron lineatum did show a greater preference for host-coloured traps when these released host-associated kairomones in addition to their pheromone, and also avoided white non-host traps, but only when these released non-host volatiles. To our knowledge, this is the first evidence that multiple non-host cues could synergistically mediate the adaptive discrimination of hosts and non-hosts. Our results suggest that successful host location by generalists arises from the complex integration of cues in multiple sensory modes, and that foraging herbivores evaluate both hosts and non-hosts during their search.     

Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs

The size of the infraorbital foramen (IOF) has been used in drawing both phylogenetic and ecological inferences regarding fossil taxa. Within the order Primates, frugivores have relatively larger IOFs than folivores or insectivores. This study uses relative IOF size in lemurs to test prior trophic inferences for subfossil lemurs and to explore the pattern of variation within and across lemur families. The IOFs of individuals belonging to 12 extinct lemur species were measured and compared to those of extant Malagasy strepsirhines. Observations matched expectations drawn from more traditional approaches (e.g. dental morphology and microwear, stable isotope analysis) remarkably well. We confirm that extinct lemurs belonging to the families Megaladapidae and Palaeopropithecidae were predominantly folivorous and that species belonging to the genus Pachylemur (Lemuridae) were frugivores. Very high values for relative IOF area in Archaeolemur support frugivory but are also consistent with omnivory, as certain omnivores use facial touch cues while feeding. These results provide additional evidence that the IOF can be used as an informative osteological feature in both phylogenetic and paleoecological interpretations of the fossil record.     

Flying bats use serial sampling to locate odour sources

Olfactory tracking generally sacrifices speed for sensitivity, but some fast-moving animals appear surprisingly efficient at foraging by smell. Here, we analysed the olfactory tracking strategies of flying bats foraging for fruit. Fruit- and nectar-feeding bats use odour cues to find food despite the sensory challenges derived from fast flight speeds and echolocation. We trained Jamaican fruit-eating bats (Artibeus jamaicensis) to locate an odour reward and reconstructed their flight paths in three-dimensional space. Results confirmed that bats relied upon olfactory cues to locate a reward. Flight paths revealed a combination of odour- and memory-guided search strategies. During ‘inspection flights’, bats significantly reduced flight speeds and flew within approximately 6 cm of possible targets to evaluate the presence or absence of the odour cue. This behaviour combined with echolocation explains how bats maximize foraging efficiency while compensating for trade-offs associated with olfactory detection and locomotion.     

Multimodal Floral Signals and Moth Foraging Decisions

Background

Combinations of floral traits – which operate as attractive signals to pollinators – act on multiple sensory modalities. For Manduca sexta hawkmoths, how learning modifies foraging decisions in response to those traits remains untested, and the contribution of visual and olfactory floral displays on behavior remains unclear.

Methodology/Principal Findings

Using M. sexta and the floral traits of two important nectar resources in southwestern USA, Datura wrightii and Agave palmeri, we examined the relative importance of olfactory and visual signals. Natural visual and olfactory cues from D. wrightii and A. palmeri flowers permits testing the cues at their native intensities and composition – a contrast to many studies that have used artificial stimuli (essential oils, single odorants) that are less ecologically relevant. Results from a series of two-choice assays where the olfactory and visual floral displays were manipulated showed that naïve hawkmoths preferred flowers displaying both olfactory and visual cues. Furthermore, experiments using A. palmeri flowers – a species that is not very attractive to hawkmoths – showed that the visual and olfactory displays did not have synergistic effects. The combination of olfactory and visual display of D. wrightii, however – a flower that is highly attractive to naïve hawkmoths – did influence the time moths spent feeding from the flowers. The importance of the olfactory and visual signals were further demonstrated in learning experiments in which experienced moths, when exposed to uncoupled floral displays, ultimately chose flowers based on the previously experienced olfactory, and not visual, signals. These moths, however, had significantly longer decision times than moths exposed to coupled floral displays.

Conclusions/Significance

These results highlight the importance of specific sensory modalities for foraging hawkmoths while also suggesting that they learn the floral displays as combinatorial signals and use the integrated floral traits from their memory traces to mediate future foraging decisions.     

Olfactory and visual plant cues as drivers of selective herbivory

Food quality is an important consideration in the foraging strategy of all animals, including herbivores. Those that can detect and assess the nutritional value of plants from afar, using senses such as smell and sight, can forage more efficiently than those that must assess food quality by taste alone. Selective foraging not only affects herbivore fitness but can influence the structure and composition of plant communities, yet little is known about how olfactory and visual cues help herbivores to find preferred plants. We tested the ability of a free‐ranging, generalist mammalian browser, the swamp wallaby Wallabia bicolor, to use olfactory and visual plant cues to find and/or browse differentially on Eucalyptus pilularis seedlings grown under different nutrient conditions. Low‐nutrient seedlings differed from high‐nutrient seedlings, having lighter coloured leaves, red stems and lower biomass and nitrogen content. In the absence of visual cues, wallabies used odour to differentiate vials containing cut seedlings. They visited and investigated patches with high‐nutrient seedling odour most, followed by patches with low‐nutrient seedling odour, and patches with no added odour least. However, when visual and olfactory cues of seedlings were present, wallabies reversed their foraging response and were more likely to browse low‐ than high‐nutrient seedlings. This browsing difference, in turn, disappeared when long‐range visual cues were reduced by pinning seedlings horizontal to the ground. We suggest that visual cues overrode the effects of olfactory cues on browsing patterns of intact seedlings. Our study shows that herbivores can respond to odours of higher nutrient plants but in ecologically realistic scenarios they use a variety of visual and olfactory cues, with a context‐dependent outcome that is not always selection of high nutrient food. Our results demonstrate the importance of testing the sensory abilities of herbivores in realistic multi‐sensory settings to understand their function in selective foraging.     

The influence of developmental environment on the evolution of olfactory foraging behaviour in procellariiform seabirds

The evolutionary origins of foraging behaviour by procellariiform seabirds (petrels, albatrosses and shearwaters) are poorly understood. Moreover, proximate factors affecting foraging ecology, such as the influence of environment on the development of sensory systems, have yet to be addressed. Here, we apply comparative methods based on current procellariiform phylogenies to identify associations between sensory modalities and the developmental environment that may underlie the evolution of complex foraging behaviour. We postulate that, for burrow-nesting species, smell is likely to dominate the sensory world of the developing chick. Alternatively, for ground-nesting species, chicks receive exposure to a range of visual, auditory and olfactory cues. We employ maximum likelihood to test models of correlated trait evolution between nesting habit and olfactory foraging style and to reconstruct the ancestral states of these characters when coded as binary states. Our results suggest that nesting behaviour has evolved in conjunction with foraging style. Based on this analysis, we propose that nesting on the surface was a life-history innovation that opened up a new developmental environment with profound effects on the foraging ecology of procellariiform seabirds.     

Allocation of Colony‐Level Foraging Effort in Vespula germanica in Response to Food Resource Quantity,Quality, and Associated Olfactory Cues

In social insects, selection takes place primarily at the level of the colony. Therefore, unlike solitary insects, social species are expected to forage at rates that maximize colony fitness rather than individual fitness. Workers can increase the net benefit of foraging by responding to increased resource availability, by responding more strongly to higher‐quality resources, and by decreasing the uncertainty with which nestmates find resources. Unlike many ants and social bees, no social wasp is known to utilize a nest‐based recruitment signal to inform nestmates of food location. On the other hand, wasps do learn the odor of food brought to the nest and use this cue to locate the food source outside the nest. Here, we quantify the effects of three food‐associated variables on the allocation of foraging effort in the yellowjacket Vespula germanica. We used an experimental approach to assess whether resource quantity, quality, or associated olfactory information affect the probability that a forager will leave the nest on a foraging trip. We addressed these questions by inserting a known amount of sucrose solution directly into nests and recording foraging effort (departure rate) over the subsequent hour‐long observation period. No differences were found in foraging effort because of the presence/absence of olfactory cues, but there was strong evidence that foraging effort increased in response to resource influx and resource quality. Thus, while olfactory cues are learned in the nest, only resource quality and the cue of increased amount of food in the nest factor into a forager's decision of whether or not to depart on a foraging trip. However, as prior work has shown, once a wasp forager leaves the nest, it uses the learned olfactory cues to aid in finding resources.     

Assessment of Rival Males through the Use of Multiple Sensory Cues in the Fruitfly Drosophila pseudoobscura

Environments vary stochastically, and animals need to behave in ways that best fit the conditions in which they find themselves. The social environment is particularly variable, and responding appropriately to it can be vital for an animal’s success. However, cues of social environment are not always reliable, and animals may need to balance accuracy against the risk of failing to respond if local conditions or interfering signals prevent them detecting a cue. Recent work has shown that many male Drosophila fruit flies respond to the presence of rival males, and that these responses increase their success in acquiring mates and fathering offspring. In Drosophila melanogaster males detect rivals using auditory, tactile and olfactory cues. However, males fail to respond to rivals if any two of these senses are not functioning: a single cue is not enough to produce a response. Here we examined cue use in the detection of rival males in a distantly related Drosophila species, D. pseudoobscura, where auditory, olfactory, tactile and visual cues were manipulated to assess the importance of each sensory cue singly and in combination. In contrast to D. melanogaster, male D. pseudoobscura require intact olfactory and tactile cues to respond to rivals. Visual cues were not important for detecting rival D. pseudoobscura, while results on auditory cues appeared puzzling. This difference in cue use in two species in the same genus suggests that cue use is evolutionarily labile, and may evolve in response to ecological or life history differences between species.     

Disentangling olfactory and visual information used by field foraging birds

Foraging strategies of birds can influence trophic plant–insect networks with impacts on primary plant production. Recent experiments show that some forest insectivorous birds can use herbivore‐induced plant volatiles (HIPVs) to locate herbivore‐infested trees, but it is unclear how birds combine or prioritize visual and olfactory information when making foraging decisions. Here, we investigated attraction of ground‐foraging birds to HIPVs and visible prey in short vegetation on farmland in a series of foraging choice experiments. Birds showed an initial preference for HIPVs when visual information was the same for all choice options (i.e., one experimental setup had all options with visible prey, another setup with hidden prey). However, if the alternatives within an experimental setup included visible prey (without HIPV) in competition with HIPV‐only, then birds preferred the visual option over HIPVs. Our results show that olfactory cues can play an important role in birds’ foraging choices when visual information contains little variation; however, visual cues are preferred when variation is present. This suggests certain aspects of bird foraging decisions in agricultural habitats are mediated by olfactory interaction mechanisms between birds and plants. We also found that birds from variety of dietary food guilds were attracted to HIPVs; hence, the ability of birds to use plant cues is probably more general than previously thought, and may influence the biological pest control potential of birds on farmland.     

Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues

1. Olfactory predator search processes differ fundamentally to those based on vision, particularly when odour cues are deposited rather than airborne or emanating from a point source. When searching for visually cryptic prey that may have moved some distance from a deposited odour cue, cue context and spatial variability are the most likely sources of information about prey location available to an olfactory predator. 2. We tested whether the house mouse (Mus domesticus), a model olfactory predator, would use cue context and spatial variability when searching for buried food items; specifically, we tested the effect of varying cue patchiness, odour strength, and cue-prey association on mouse foraging success. 3. Within mouse- and predator-proof enclosures, we created grids of 100 sand-filled Petri dishes and buried peanut pieces in a set number of these patches to represent visually cryptic 'prey'. By adding peanut oil to selected dishes, we varied the spatial distribution of prey odour relative to the distribution of prey patches in each grid, to reflect different levels of cue patchiness (Experiment 1), odour strength (Experiment 2) and cue-prey association (Experiment 3). We measured the overnight foraging success of individual mice (percentage of searched patches containing prey), as well as their foraging activity (percentage of patches searched), and prey survival (percentage of unsearched prey patches). 4. Mouse foraging success was highest where odour cues were patchy rather than uniform (Experiment 1), and where cues were tightly associated with prey location, rather than randomly or uniformly distributed (Experiment 3). However, when cues at prey patches were ten times stronger than a uniformly distributed weak background odour, mice did not improve their foraging success over that experienced when cues were of uniform strength and distribution (Experiment 2). 5. These results suggest that spatial variability and cue context are important means by which olfactory predators can use deposited odour cues to locate visually cryptic prey. They also indicate that chemical crypsis can disrupt these search processes as effectively as background matching in visually based predator-prey systems.     

Host location and selection cues in a generalist tachinid parasitoid

Tachinid flies are diverse and ecologically important insect parasitoids. However, the means by which tachinid species locate and select hosts are poorly known. Many tachinids exhibit unusually wide host ranges and they also possess well-developed visual systems. These characteristics suggest that tachinids differ from parasitic wasps in their reliance on various sensory modes and types of cues. A series of behavioral assays using the generalist tachinid Exorista mella Walker (Diptera: Tachinidae) were conducted to examine what types of cues this parasitoid uses to locate and accept hosts, and how the cues used may reflect its ecological relationships with hosts. Female E. mella responded strongly to host motion in assays using both live hosts and host corpses, and this cue is shown to be an important elicitor of attack behavior. Females also responded to volatile chemicals associated with damaged food plants of their host in an olfactometer. Flies responded only weakly to direct visual contact with stationary hosts and odors directly associated with hosts. The behavior of female E. mella changed with experience such that more experienced flies recognized and attacked hosts more readily than did inexperienced flies. The use of general olfactory and visual cues by E. mella may be an effective strategy by this polyphagous parasitoid to locate a broad range of potential hosts.     

Anemonefishes rely on visual and chemical cues to correctly identify conspecifics

Organisms rely on sensory cues to interpret their environment and make important life-history decisions. Accurate recognition is of particular importance in diverse reef environments. Most evidence on the use of sensory cues focuses on those used in predator avoidance or habitat recognition, with little information on their role in conspecific recognition. Yet conspecific recognition is essential for life-history decisions including settlement, mate choice, and dominance interactions. Using a sensory manipulated tank and a two-chamber choice flume, anemonefish conspecific response was measured in the presence and absence of chemical and/or visual cues. Experiments were then repeated in the presence or absence of two heterospecific species to evaluate whether a heterospecific fish altered the conspecific response. Anemonefishes responded to both the visual and chemical cues of conspecifics, but relied on the combination of the two cues to recognize conspecifics inside the sensory manipulated tank. These results contrast previous studies focusing on predator detection where anemonefishes were found to compensate for the loss of one sensory cue (chemical) by utilizing a second cue (visual). This lack of sensory compensation may impact the ability of anemonefishes to acclimate to changing reef environments in the future.

     

Odour maps in the brain of butterflies with divergent host-plant preferences

Butterflies are believed to use mainly visual cues when searching for food and oviposition sites despite that their olfactory system is morphologically similar to their nocturnal relatives, the moths. The olfactory ability in butterflies has, however, not been thoroughly investigated. Therefore, we performed the first study of odour representation in the primary olfactory centre, the antennal lobes, of butterflies. Host plant range is highly variable within the butterfly family Nymphalidae, with extreme specialists and wide generalists found even among closely related species. Here we measured odour evoked Ca(2+) activity in the antennal lobes of two nymphalid species with diverging host plant preferences, the specialist Aglais urticae and the generalist Polygonia c-album. The butterflies responded with stimulus-specific combinations of activated glomeruli to single plant-related compounds and to extracts of host and non-host plants. In general, responses were similar between the species. However, the specialist A. urticae responded more specifically to its preferred host plant, stinging nettle, than P. c-album. In addition, we found a species-specific difference both in correlation between responses to two common green leaf volatiles and the sensitivity to these compounds. Our results indicate that these butterflies have the ability to detect and to discriminate between different plant-related odorants.     

Visual and Olfactory Responses of Seven Butterfly Species During Foraging

Foraging responses of seven butterfly species were determined for flower models that differed in color, size, and depth of artificial corolla. We measured frequency of visits to flowers of various colors (red, orange, yellow, purple, and white) with or without the application of honey water to flower models. We found that the relative strength of butterfly response to visual versus olfactory cues differed among butterfly species. We suggest that the seven butterfly species tested exhibit four different patterns in how visual and olfactory cues were combined as determinants of foraging importance: (1) vision was given priority over olfaction (in Cethosia cyane and Danaus chrysippus); (2) olfaction was given priority over vision (Cethosia biblis, Idea leuconoe, and Tirumala limniace); (3) olfaction and vision were equally important (Catopsilia pomona); and (4) only olfaction was used (e.g., Danaus genutia, which was not sensitive to the five colors tested but very sensitive to the smell of honey in our experiments). In tests with flower models of different sizes, the visitation frequency of C. cyane, I. leuconoe, and D. chrysippus increased with increasing corolla diameter, provided flowers were sprayed with honey water. C. cyane and D. chrysippus showed this trend because of their strong dependence on visual cues. In contrast, I. leuconoe with its large body size preferred larger flowers, it could be that butterflies need more nectar to support its large body size. Catopsilia pomona tended to visit large and middle-sized flowers because it used both vision and odor to detect food, large or middle-sized flowers could have more vision and odor stimulation than small flowers for foraging butterfly. The other three butterfly species did not show that trend because of lack of dependence on visual cues. There was no correlation between visitation frequency and corolla depth within particular butterfly species. In conclusion, the foraging strategies of butterflies are not only mainly determined by the weights given to visual and olfactory cues, but also affected by body size.     

Early oviposition experience affects patch residence time in a foraging parasitoid

Parasitoids learn olfactory and visual cues that are associated with their hosts, and use these cues to forage more efficiently. Classical conditioning theory predicts that encounters with high-quality hosts will lead to better learning of host-associated cues than encounters with low-quality hosts. We tested this prediction in a two-phase laboratory experiment with the parasitoid Trichogramma thalense Pinto & Oatman (Hymenoptera: Trichogrammatidae) and the host Anagasta kuehniella Zeller (Lepidoptera: Pyralidae).Host quality during the first exposure to hosts affected later foraging behavior for some experimental treatments, as predicted. We used a learning model, followed by patch-time optimization, to interpret our findings. We first simulated the parasitoids' host encounters during the experiment, and predicted their estimate of patch quality after each encounter. We then used dynamic optimization to predict the parasitoids' optimal patch residence times. The model reproduces the trends of the experimental results.     

Predator cue and prey density interactively influence indirect effects on Basal resources in intertidal oyster reefs

Predators can influence prey abundance and traits by direct consumption, as well as by non-consumptive effects of visual, olfactory, or tactile cues. The strength of these non-consumptive effects (NCEs) can be influenced by a variety of factors, including predator foraging mode, temporal variation in predator cues, and the density of competing prey. Testing the relative importance of these factors for determining NCEs is critical to our understanding of predator-prey interactions in a variety of settings. We addressed this knowledge gap by conducting two mesocosm experiments in a tri-trophic intertidal oyster reef food web. More specifically, we tested how a predatory fish (hardhead catfish, Ariopsis felis) directly influenced their prey (mud crabs, Panopeus spp.) and indirectly affected basal resources (juvenile oysters, Crassostrea virginica), as well as whether these direct and indirect effects changed across a density gradient of competing prey. Per capita crab foraging rates were inversely influenced by crab density, but they were not affected by water-borne predator cues. As a result, direct consumptive effects on prey foraging rates were stronger than non-consumptive effects. In contrast, predator cue and crab density interactively influenced indirect predator effects on oyster mortality in two experiments, with trait-mediated and density-mediated effects of similar magnitude operating to enhance oyster abundance. Consistent differences between a variable predator cue environment and other predator cue treatments (no cue and constant cue) suggests that an understanding of the natural risk environment experienced by prey is critical to testing and interpreting trait-mediated indirect interactions. Further, the prey response to the risk environment may be highly dependent on prey density, particularly in prey populations with strong intra-specific interactions.     

Daily lettuce supplements promote foraging behavior and modify the gut microbiota in captive frugivores

For captive primates, greater provisioning of leafy greens or foliage can promote natural foraging behavior while boosting fiber intake. Recalcitrant fiber, although minimally available to endogenous metabolism, is readily fermented into nutrients by gut microbes. Whereas most primates in captivity consume fiber-limited diets and harbor imbalanced gut microbiota compared to their wild conspecifics, the importance of fiber provisioning to primate gut microbiota has predominately been studied in folivores. We, therefore, determined if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores. We provisioned ruffed lemurs (Varecia rubra and V. variegata) with romaine lettuce, on top of the standard dietary fare, for 10 consecutive days. Before and across the period of lettuce supplementation, we collected observational data of animal feeding and fecal samples for microbiome analysis, determined via amplicon sequencing. The ruffed lemurs and their gut microbes responded to lettuce provisioning. In particular, younger animals readily ate lettuce and showed no decline in consumption across study days. When controlling for the effects of host species and social-group membership, lettuce consumption shifted the composition of the gut microbiome away from each lemur's own baseline, an effect that became stronger as the study progressed. In the final study days, Ruminococcaceae UCG-008 and Akkermansia, microbes typically and respectively associated with fiber metabolism and host health, were significantly enriched in the consortia of lettuce-provisioned subjects. Ultimately, the routine offering of lettuce, leafy greens, or foliage to captive frugivores may benefit animal wellbeing.