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.     

Complementary roles of two resilient neotropical mammalian seed dispersers

Capuchin monkeys (Cebus spp. and Sapajus spp.) and coatis (Nasua spp.) coexist in most neotropical forests, including small forest remnants. Both capuchins and coatis eat fruit and disperse seeds, but little is known about whether their roles in seed dispersal are redundant or complementary. We compiled 49 studies from the literature on feeding by capuchins and/or coatis, of which 19 were comprehensive enough for our analyses. We determined the relative importance of fruit eating to each species and compared their diets. Additionally, we analysed the structure of three fruit–frugivore networks built with both animal groups and the fruits they eat and evaluated whether fruit traits influenced the network topology. Fruits represented the largest part of capuchin and coati diets, even though coatis have been known for their opportunistic and generalist diets. Capuchins and coatis also exhibited similar general diet parameters (niche breadth and trophic diversity). The three networks exhibited high connectance values and variable niche overlap. A Multiple Correspondence Analysis, failed to detect any trait or trait combination related to food use. In conclusion, capuchins and coatis both have generalist diets; they feed on many different species of fruits and exhibit important complementarity as seed dispersers. Both are likely to be particularly important seed dispersers in disturbed and fragmented forests.     

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.     

Measuring fruit patch size for three sympatric indonesian primate species

Food availability is one of the basic factors affecting primate density and socioecology, but food availability is difficult to assess. Two different ways to obtain accurate estimates of food availability have been proposed: using phenology data or using the behaviour of animals. Phenology data can be refined by only including trees that are large enough to be used; including (potential) tree species in which by the concerned primate species forage; or including (fruiting) trees of these species that actually produce fruit. Alternatively, the sizes of the actually visited trees (foraging trees) give an estimate of fruit availability. These measures are compared for three sympatric primate species at the Ketambe Research Station, Sumatra, Indonesia: the Thomas langur, the long-tailed macaque and the orangutan. The sizes of fruiting trees and the foraging trees are larger than the potential trees. The sizes of the potential trees and of the fruiting trees are similar for the three primate species. This, however, is not reflected in the use of trees: the langurs forage on average in trees of similar size to those producing fruit, whereas the macaques and orangutans forage in trees larger than those producing fruit. The use of trees does not necessitate a different cut off point of included dbhs for the three compared primate species. The use of trees of different sizes, however, may be regulated by food competition. This indicates that sympatric primates make different foraging decisions and that behavioural measures of food availability will be less reliable.     

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.     

Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa

The threat that forest fragmentation and habitat loss presents for several Alouatta taxa requires us to determine the key elements that may promote the persistence of howler monkeys in forest fragments and to evaluate how changes in the availability of these elements may affect their future conservation prospects. In this study we analyzed the relationship between the availability of both big trees of top food taxa (BTTFT) (diameter at breast height>60) and fruit of top food taxa (FrTFT) in the home ranges of two groups of Alouatta palliata mexicana occupying different forest fragments in Los Tuxtlas, Mexico, and their diet and activity pattern. Both study groups preferred big trees for feeding and the group with lower availability of BTTFT in their home range fed from more, smaller food sources. Furthermore, both study groups also increased the number of food sources when their consumption of fruit decreased, and the group with lower availability of FrTFT in their home range fed from more food sources. The increase in the number of food sources used under such conditions, in turn, set up a process of higher foraging effort and lower rest. In summary, our results support other studies that suggest that the availability of big trees and fruit may be two important elements influencing the persistence of howler monkeys in forest fragments. Am. J. Primatol. 71:654–662, 2009. © 2009 Wiley‐Liss, Inc.     

Possible use of heterospecific food-associated calls of macaques by sika deer for foraging efficiency

Heterospecific communication signals sometimes convey relevant information for animal survival. For example, animals use or eavesdrop on heterospecific alarm calls concerning common predators. Indeed, most observations have been reported regarding anti-predator strategies. Use of heterospecific signals has rarely been observed as part of a foraging strategy. Here, I report empirical evidence, collected using playback experiments, showing that Japanese sika deer, Cevus nippon, use heterospecific food calls of Japanese macaques, Macaca fuscata yakui, for foraging efficiency. The deer and macaques both inhabit the wild forest of Yakushima Island with high population densities and share many food items. Anecdotal observations suggest that deer often wait to browse fruit falls under the tree where a macaque group is foraging. Furthermore, macaques frequently produce food calls during their foraging. If deer effectively obtain fruit from the leftovers of macaques, browsing fruit fall would provide a potential benefit to the deer, and, further, deer are likely to associate macaque food calls with feeding activity. The results showed that playback of macaque food calls under trees gathered significantly more deer than silence control periods. These results suggest that deer can associate macaque food calls with foraging activities and use heterospecific calls for foraging efficiency.     

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.     

Associations between primates and other mammals in a central Amazonian forest landscape

Little information exists on mixed-species groups between primates and other mammals in Neotropical forests. In this paper, we describe three such associations observed during an extensive large-vertebrate survey in central Amazonia, Brazil. Mixed-species groups between a primate species and another mammal were observed on seven occasions between squirrel monkeys (Saimiri cf. ustus) and either South American coatis (Nasua nasua) or tayras (Eira barbara) and between brown capuchins (Cebus apella) and coatis. All associations were restricted to floodplain forest during its dry stage. We suggest that the associations involving the coatis are connected to foraging and vigilance but may be induced by a common alternative food resource at a time of food shortage.     

Optimal locomotion modes of foraging birds in trees

This paper compares the energy costs of various modes of locomotion of birds foraging in trees. For birds moving vertically in trees by climbing and hopping (but not by flying) the best choice of locomotion mode depends on the distance between visited trees in relation to the height h of the zone searched for food in trees.
When the distance between successively visisted trees is longer than about half the distance coverable in gliding flight with height loss h , then it is cheapest in energy to hop or climb upwards in a tree and fly downwards to the next tree. When the distance between successively visited trees is shorter than about half the distance coverable in gliding flight with height loss h , then it is cheapest in energy to move alternately downwards and upwards in trees (downwards in the first, upwards in the second, downwards in the third tree, etc.) and to fly level between trees.
Treecreepers and woodpeckers are adapted morphologically to the former mode, but more generalized tree foragers might use either mode depending on the spacing of trees.     

Response of the foraging behaviour of red wood ants (Formica rufa group) to exclusion from trees

Abstract 1 Because of the large numbers within a colony and their aggressive nature, red wood ants (Formica rufa group) have a potential to greatly influence the cold‐temperate forest ecosystem. Wood ants are omnivorous and hunt in trees as well as on the forest floor. 2 A field experiment in a mixed forest in central Sweden was carried out to examine (i) the foraging behaviour of wood ants on the forest floor and (ii) the impact of increased numbers of wood ants on the soil fauna. The foraging behaviour of wood ants was manipulated by excluding the ants from their food resources in the tree canopy, with the intention to increase ant activity on the forest floor. To estimate this activity, the number of trees with foraging ants, the numbers of ants going to and from their nests and the prey carried by home‐running wood ants were determined during the summer period. Pitfall traps were placed in the soil to determine effects on mobile soil invertebrates. 3 When excluded from local trees, wood ants searched other trees further away from the nests rather than searching more intensively for prey on the forest floor. By contrast to the initial hypothesis, more soil‐living prey were caught by ants in the control plots than in the plots where the local trees were not accessible to the wood ants. The proportion of soil‐living to tree‐living prey tended to be greater in the control plots. 4 In the treated plots (no access to the trees), wood ants had a negative effect on the activity of Linyphiidae spiders. There was little effect of wood ants on other soil invertebrates. 5 This study suggests that the role of wood ants as top predators in the forest soil food‐web in central Sweden is limited.     

Sources of variation in the incidence of ant–aphid mutualism in boreal forests

• 1 The mutualism between wood ants of the Formica rufa group and aphids living in the canopy of trees is a widespread phenomenon in boreal forests, and it can affect tree growth. However, not all trees in the forest are involved in this interaction.
• 2 To assess the incidence of host trees involved in this ant–aphid mutualism and its spatial distribution in boreal forests, we inventoried sample plots with a radius of 10–15 m around wood ant mounds in 12 forest stands of two age classes (5–12‐year‐old sapling stands and 30–45‐year‐old pole stands) and two dominant tree species (Scots pine and silver birch) in Eastern Finland from 2007 to 2009.
• 3 The proportion of trees visited by ants out of all trees on the individual study plots were in the range 4–62%, and 1.5–39% of the trees on the plots were consistently visited by ants during all 3 years. The percentage of host trees increased with the ant mound base area on the plots. Trees visited by ants were larger and closer to the mound than trees not visited by ants. Within the group of visited trees, more ants were found on bigger trees and on trees close to the ant mounds.
• 4 Extrapolated from plot to stand level, we estimated that 0.5–6.6% of the trees were host trees in at least one of the three study years, and that only 0.01–2.3% of all the trees were consistently visited by ants during all 3 years. It is concluded that ant–aphid mutualism is a minor occurrence at the stand level.

     

Mallards Feed Longer to Maintain Intake Rate under Competition on a Natural Food Distribution

Animals foraging in groups may benefit from a faster detection of food and predators, but competition by conspecifics may reduce intake rate. Competition may also alter the foraging behaviour of individuals, which can be influenced by dominance status and the way food is distributed over the environment. Many studies measuring the effects of competition and dominance status have been conducted on a uniform or highly clumped food distribution, while in reality prey distributions are often in‐between these two extremes. The few studies that used a more natural food distribution only detected subtle effects of interference and dominance. We therefore conducted an experiment on a natural food distribution with focal mallards Anas platyrhynchos foraging alone and in a group of three, having a dominant, intermediate or subordinate dominance status. In this way, the foraging behaviour of the same individual in different treatments could be compared, and the effect of dominance was tested independently of individual identity. The experiment was balanced using a 4 × 4 Latin square design, with four focal and six non‐focal birds. Individuals in a group achieved a similar intake rate (i.e. number of consumed seeds divided by trial length) as when foraging alone, because of an increase in the proportion of time feeding (albeit not significant for subordinate birds). Patch residence time and the number of different patches visited did not differ when birds were foraging alone or in a group. Besides some agonistic interactions, no differences in foraging behaviour between dominant, intermediate and subordinate birds were measured in group trials. Possibly group‐foraging birds increased their feeding time because there was less need for vigilance or because they increased foraging intensity to compensate for competition. This study underlines that a higher competitor density does not necessarily lead to a lower intake rate, irrespective of dominance status.     

Improvement of almond production using Bombus terrestris (Hymenoptera: Apidae) in Mediterranean conditions

Almond trees are one of the most important crops in the Balearic Islands. The pollination of almonds is limited to the activity of insects, and cross‐pollination is necessary for fruit development. Currently, honey bees and wild bee populations are declining considerably due to multiple causes, such as the use of pesticides, diseases and habitat loss. An alternative to increase the almond production is the use of commercial pollinators. In this long‐term (3 years) study, the effect of the introduction of Bombus terrestris colonies on almond production was evaluated in two orchards. Two experimental designs were carried out to study the best management of this pollinator. For 2 years, all bumble bee colonies were placed in the middle of the plot and during the last year, the bumble bee colonies were distributed homogenously in the plot. Fruit set and the foraging behaviour of bumble bees during the blossoming period was determined, and the effect of different environmental variables on the visitation rate of bumble bees was assessed by means of a generalized linear mixed model (GLMM). Moreover, for the first time, the spatial distribution of fruit set was evaluated. Our results show that fruit set was significantly higher in the fields where B. terrestris had been introduced than in the control plots. This increased production resulted in a positive economic balance for the farmer. Moreover, bumble bees showed to prefer trees in a southwest orientation that were close to their colony. The activity of bumble bees showed to be significantly influenced by wind speed (the higher the speed the more flowers are visited by B. terrestris) and time after flowering (visitation rate decreased with days after flowering). In order to improve its management and obtain the highest possible almond production, it is important to understand the activity and behaviour of this pollinator.     

The survival advantage of olfaction in a competitive environment

Olfaction is generally assumed to be critical for survival because this sense allows animals to detect food and pheromonal cues. Although the ability to sense sex pheromones [1, 2, 3] is likely to be important for insects, the contribution of general odor detection to survival is unknown. We investigated the extent to which the olfactory system confers a survival advantage on Drosophila larvae foraging for food under conditions of limited resources and competition from other larvae.     

Influence of intertree distance on foraging behaviour of Rhagoletis pomonella in the field

Abstract. 1. We tested a prediction from contemporary foraging theory that animals should decrease their allocation of energy to the searching of individual patches when interpatch travel costs decrease.
2. We used individual Rhagoletis pomonella Walsh (Diptera: Tephritidae) females foraging for oviposition sites (= Crataegus fruit) in a host tree which was surrounded by four other trees at varying distances.
3. We found that flies generally invested less search, measured as time spent searching a tree or number of leaves visited on a tree, when neighbouring trees were nearby than when farther away.
4. Under our test conditions, flies appeared to have difficulty locating neighbouring trees at a distance of more than 1.6 m.
5. Our study calls into question the interpretation of search effort by insects within resource patches in the absence of information on interpatch distances.     

The Huh Vocalization of White-faced Capuchins: a Spacing Call Disguised as a Food Call?

White-faced capuchins, (thus capuchins, predictably emit huh vocalizations at high rates within dense fruit patches. We sought to determine why white-faced capuchins at the La Selva Biological Station, Costa Rica produce these food-associated calls. Here we analyze the contexts in which this intra-group vocalization was emitted, including the spatial responses elicited from other troop members. A cumulative 26.6 h of continuous focal samples and 3314 spectrograms (including 1643 huhs) were analyzed from a study troop with 16 focal subjects. The mean individual rate of huhs was greater (1) during foraging versus nonforaging activities; (2) during fruit foraging compared to both visual searching for foraging sites and foraging for arthropod prey; and (3) when the nearest neighbor was within a 10 m radius of the focal animal compared to when the nearest neighbor was at greater distances. A huh also predicted a significant increase in nearest-neighbour distance; on average, mean nearest-neighbor distance increased 3 m within 2 min following a huh vocalization. Null models of change in mean nearest-neighbor distance over time were generated from the original data set by treating predetermined time points (140 s intervals) in the focal recordings as if those points marked instances at which huhs were produced by the focal subject. No significant alterations in nearest-neighbor distance were detected within time lags up to 100 s in these null models, supporting the conclusion that huhs are causally linked with subsequent increases in nearest-neighbor distances. Huhs were most evident when capuchins were within dense fruit patches, but these calls were produced across all foraging contexts. Our results suggest that huhs may not be food calls in the usual sense (i.e. informing others of the location of food sources to be shared), but may be more appropriately described as spacing calls. Huhs probably act to increase foraging efficiency by reducing overlap in foraging areas with other troop members.     

Resource patch size and flexible foraging in white-faced capuchins (Cebus capucinus)

White-faced capuchins (Cebus capucinus)on Barro Colorado Island, Panama, have a flexible foraging strategy. Typically, foraging party size is small and individuals feed dispersed from one another. When seasonal fruiting of large volume trees occurs, the majority of the group forages simultaneously. As C. capucinusdo not display a rigorous dominance structure and there are few indications that individuals or coalitions monopolize food patches,individuals are expected to display scramble strategies instead of high frequencies of contest competition. I recorded foraging party size (simultaneous foragers), the total number of animals to feed successively, and the diameter at breast height (DBH) of fruit trees used in two habituated troops. Individuals in each group spent a substantial amount of time — 65 and 48% of foraging time for each group — foraging in party sizes of one. Monkeys predominantly foraged alone in small trees (0- to 20- cm DBH), successively in medium trees (21- to 60- cm DBH), and simultaneously in large trees (>61- cm DBH). They used small trees more frequently than all other tree classes. In medium-sized trees, although fruit was plentiful, space was limited. In these trees Cebusforaged successively. In large-volume trees, space and fruit were abundant and several individuals fed together. As the DBH of fruiting trees increased, the average foraging party size increased exponentially. Cebus capucinusat Barro Colorado Island modify their foraging party size to adapt to the seasonal patterns of fruit production.     

Seasonal variation in foraging conditions for Ring Ouzels Turdus torquatus in upland habitats and their effects on juvenile habitat selection

Recent studies indicate that variation in juvenile survival may be particularly important in driving avian population dynamics. The quality of habitats available to inexperienced juveniles of migrant species is critical to their survival because they must obtain enough food to build up fat reserves for migration, while avoiding predation. We radiotracked 110 juvenile Ring Ouzels Turdus torquatus, a species of high conservation concern in the UK, to quantify for the first time seasonal patterns in foraging habitat and food abundance during this potentially key life‐history period. Key attributes of foraging plots were compared with those on control plots (representing the broad habitat types selected by foraging juveniles) during 2007–08. Birds foraged on invertebrates in grass‐rich plots during June to mid‐July and then shifted to foraging mainly on moorland berries in higher‐altitude, heather‐rich plots during mid‐July to early‐September. Juveniles selected invertebrate foraging plots with low soil acidity, and increasingly selected plots with high earthworm (an important food) biomass and grass cover, but low grass and all vegetation height as the season progressed. In contrast, earthworm biomass and grass cover remained constant, and grass and all vegetation height increased, on control plots. Juveniles selected berry foraging plots with higher abundance of ripe Bilberries Vaccinium myrtillus and Crowberries Empetrum nigrum than found on control plots. Juvenile Ring Ouzels thus appear to require access to short, grass‐ and invertebrate‐rich habitat during early summer, and taller, heather‐dominated and berry‐rich areas in late summer. The use of two distinct habitat types during the pre‐migratory period illustrates the need for a detailed understanding of the requirements of juvenile birds.     

Effects of a Typhoon on Foraging Behavior and Foraging Success of <Emphasis Type="Italic">Macaca fuscata</Emphasis> on Kinkazan Island,Northern Japan

We studied the effects of typhoon damage on the food habits, time budgets, and moving distances of Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan. Before the typhoon (pre-typhoon phase), the macaques fed on various food items, including fruit in trees (Swida macrophylla) and nuts (Torreya nucifera) on the ground. After the typhoon passed (post-typhoon phase), the macaques fed intensively on the seeds of Perilla frutescens (a forb) and the nuts of Quercus serrata on the ground. One may attribute the changes to decreased food availability or foraging efficiency of fruits and nuts on the ground, due to their concealment by leaf litter and mud and their consumption by other animals, such as sika deer (Cervus nippon) and field mice (Apodemus argenteus). In the post-typhoon phase, the macaques fed more quickly on seeds of Perilla frutescens, spent less time traveling, and moved over shorter distances. The differences may be due to changes in the distribution of staple foods between the 2 phases. We also evaluated the energy intake and energy balance of the macaques in both phases, based on observations of foraging and nutritional analyses of the food items. There is no significant difference in either parameter between the 2 phases. The changes in food habits and movement behavior may have compensated for the reduced food availability or foraging efficiency caused by the typhoon. Both behavioral changes and nutritional issues are important when investigating the effects of storms on animal ecology.