Solitary Foragers Research Articles

Time allocation to balance group living trade-offs in Ethiopian wolves

Living in groups requires individuals to make trade-offs to maintain group cohesion and enhance individual and inclusive fitness. One way animals can do this is by adjusting the way they allocate time to different behaviours. Ethiopian wolves (Canis simensis) are highly social, cooperative breeders (only the dominant pair breeds and all members help to raise the litter), but solitary foragers. To investigate how Ethiopian wolves allocate their time to balance the costs and benefits of group living, we analysed the time budgets of 47 wolves across six behaviours. We hypothesized that group size and territory density would affect wolves’ time allocation between solitary (foraging) and communal activities (patrolling and socialising) differently in relation to their age, dominance status or sex, and whether the pack was breeding or not. Our results showed that the time spent foraging alone increased at higher territorial densities, as expected from interference competition, particularly among subadults, subordinates and individuals in breeding packs. On the other hand, as pack size increased, adult wolves spent a lower proportion of time patrolling, while the time spent socialising did not change. Living in groups reduces the costs of communal activities, but crowded territories come at the cost of interference competition for solitary foragers, particularly the animals further down the hierarchy ranks, subadults, and individuals investing in breeding. Such trade-offs could impose an upper limit to group size and population growth within a limited space. Furthermore, anthropogenic disturbance could alter the balance of social and solitary activities of Ethiopian wolves.

Variation in abundance and habitat use of the critically endangered Microcebus gerpi across its fragmented range.

A link between the abundance of species and their degree of ecological specialization has previously been suggested within the primate order. Many species of lemurs were only recently described and even basic ecological data are not yet available for them. We investigated the habitat use, abundance, and habitat characteristics of the critically endangered Microcebus gerpi and evaluated potential impacts of vegetation structure and human disturbances on variations in its abundance. We determined abundance by systematic nocturnal surveys along 13 transects that were also used for characterizing the vegetation structure in seven study sites that were widely distributed within its range. Although M. gerpi occurred in all studied lowland rainforest and littoral forest fragments in central eastern Madagascar and therefore has a higher ecological plasticity and wider distribution than previously thought, its actual Area of Occupancy is very small (339.78 km2 ) due to an extreme degree of habitat fragmentation throughout its range. M. gerpi occurred with a mean encounter rate of 3.04 individuals/km but abundance varied substantially between sites (0.75-4.5 individuals/km). Statistical modeling revealed that the cover of small- to medium-sized trees had a positive impact on the abundance of M. gerpi, whereas a composite disturbance score (CDS), formed on the basis of information on the prominence of fires, cattle, charcoal production and wood extraction inside and around the forest, had a negative impact on abundance. These results suggest that M. gerpi is slightly less threatened than expected because of its larger geographic range, but also that it responds negatively to human disturbances. These findings raise strong conservation concerns and question the long-term viability of the remaining small and isolated populations of this arboreal solitary forager.

Directed retreat and navigational mechanisms in trail following Formica obscuripes

Ant species exhibit behavioural commonalities when solving navigational challenges for successful orientation and to reach goal locations. These behaviours rely on a shared toolbox of navigational strategies that guide individuals under an array of motivational contexts. The mechanisms that support these behaviours, however, are tuned to each species’ habitat and ecology with some exhibiting unique navigational behaviours. This leads to clear differences in how ant navigators rely on this shared toolbox to reach goals. Species with hybrid foraging structures, which navigate partially upon a pheromone-marked column, express distinct differences in their toolbox, compared to solitary foragers. Here, we explore the navigational abilities of the Western Thatching ant (Formicaobscuripes), a hybrid foraging species whose navigational mechanisms have not been studied. We characterise their reliance on both the visual panorama and a path integrator for orientation, with the pheromone’s presence acting as a non-directional reassurance cue, promoting continued orientation based on other strategies. This species also displays backtracking behaviour, which occurs with a combination of unfamiliar terrestrial cues and the absence of the pheromone, thus operating based upon a combination of the individual mechanisms observed in solitarily and socially foraging species. We also characterise a new form of goalless orientation in these ants, an initial retreating behaviour that is modulated by the forager’s path integration system. The behaviour directs disturbed inbound foragers back along their outbound path for a short distance before recovering and reorienting back to the nest.

Two is better than one: innovative ants overcome the nature-inspired cognitive challenge of pupal insertion

IntroductionThe cognitive abilities of animals play a crucial role in their capacity to adapt to changing environments. Experiments to understand cognition are usually performed on animals such as non-human primates, canids, or corvids. These studies often use food as the motivating factor. However, in the current study, we used a new paradigm to investigate the ability of ponerine ants, who are solitary foragers, to solve a nature-inspired problem. As pupae are the most invested brood item and are directly associated with the colony’s fitness, we designed an experiment that presented a challenge to colony relocation by imposing restrictions on the transportation of pupae to the new nest.MethodsWe used a narrow nest entrance through which an adult could enter, but it rendered the passage of an adult holding a pupa virtually impossible. Through this, we examined the capacity of these ants to overcome the “pupal insertion” challenge by investigating eight colonies involving 425 pupal insertions performed by 104 uniquely labeled ants. ResultsWe found that 80% of all pupae were inserted into the nest by employing a novel cooperative behavior: one ant pushed the pupa while the other ant(s) inside the nest pulled it. Even though individual ants showed high variability in their performance regarding pupal insertion, the initial three successive insertions showed a significant improvement in their performance. Such improvement was also documented at the colony level, with shorter durations and fewer attempts for subsequent pupal insertions. DiscussionOur study demonstrated that ants can overcome difficult environmental challenges through innovation and subsequently improve their performance without training or reward.

No food left behind: foraging route choices among free-ranging Japanese macaques (Macaca fuscata) in a multi-destination array at the Awajishima Monkey Center, Japan.

Animals must make route choices every day when moving through their habitat while foraging. Choosing an optimal route can be cognitively costly, and primates and other animals have been shown to use simple heuristics, "rules of thumb", to make foraging route choices. We investigated the potential use of heuristics among foraging free-ranging Japanese monkeys (Macaca fuscata) during solitary foraging trials. We also investigated the potential influence of individual variables (age and sex) and social variables (presence in the central group, presence of potential inter- and intraspecific competitors), on the use of heuristics, route length and trial time. We used a multi-destination foraging experiment with 6 platforms in a (4m×8m) Z-array, completed by 29 Japanese macaques in 155 runs at the Awajishima Monkey Center in Japan. Our results showed that the macaques chose routes consistent with heuristics (e.g. nearest neighbour heuristic 19.4%, convex hull heuristic 4.5%) and selected optimal routes (shortest path in 23.9% of the trials). We also identified a potential new heuristic that was used most frequently, that we termed the "sweep heuristic" (27.1% of trials), which we interpreted as a strategy to deal with competitive foraging trade-offs - choosing routes to prioritize not leaving isolated food pieces behind. Age was significantly related to trial time; juvenile macaques were faster than adults and young adults, using speed to gain access to resources. Solitary trials with conspecifics present took significantly longerroutes. Our results suggest that contextual factors led to variation in Japanese macaque decision-making, and we suggest that the preferential use of a sweep heuristic may have been a response to high intragroup competition.

Optimal foraging strategies for mutually avoiding competitors

Many animals are known to exhibit foraging patterns where the distances they travel in a given direction are drawn from a heavy-tailed Lévy distribution. Previous studies have shown that, under sparse and random resource conditions, solitary non-destructive (with regenerating resources) foragers perform a maximally efficient search with Lévy exponent μ equal to 2, while for destructive foragers, efficiency decreases with μ monotonically and there is no optimal μ. However, in nature, there also exist situations where multiple foragers, displaying avoidance behavior, interact with each other competitively. To understand the effects of such competition, we develop a stochastic agent-based simulation that models competitive foraging among mutually avoiding individuals by incorporating an avoidance zone, or territory, of a certain size around each forager which is not accessible for foraging by other competitors. For non-destructive foraging, our results show that with increasing size of the territory and number of agents the optimal Lévy exponent is still approximately 2 while the overall efficiency of the search decreases. At low values of the Lévy exponent, however, increasing territory size actually increases efficiency. For destructive foraging, we show that certain kinds of avoidance can lead to qualitatively different behavior from solitary foraging, such as the existence of an optimal search with 1<μ<2. Finally, we show that the variance among the efficiencies of the agents increases with increasing Lévy exponent for both solitary and competing foragers, suggesting that reducing variance might be a selective pressure for foragers adopting lower values of μ. Taken together, our results suggest that, for multiple foragers, mutual avoidance and efficiency variance among individuals can lead to optimal Lévy searches with exponents different from those for solitary foragers.

Correlated expression of phenotypic and extended phenotypic traits across stingless bee species: worker eye morphology, foraging behaviour, and nest entrance architecture

Stingless bees are the most species-rich group of eusocial bees and show great diversity in behaviour, ecology, nest architecture, colony size, and worker morphology. How this variation relates to varying selection pressures and constraints is not well understood. Variation can be caused by selection acting on behavioural or morphological traits, both alone and in correlation across traits. Here we tested whether behavioural and morphological traits important for foraging and defence are linked to nest-entrance architecture, an extended phenotype relevant to both foraging and nest defence. Using 23 species we investigated whether eye size, nest entrance size, landing behaviour and foraging method show cross-species correlations. A phylogenetically-controlled comparative analysis revealed that species with relatively smaller eyes build relatively larger entrances, which in turn are associated with faster landing approaches and fewer landing errors by foragers, both of which could reduce predation risk. Concerning foraging, mass-recruiting species have c. 10-times larger entrance holes than species with a solitary foraging strategy. Larger entrances could help species with mass recruitment to rapidly increase forager traffic or mount a strong defensive response when under attack. Our results show that studying correlations among different traits helps understand phenotypic diversity in species rich groups.

Evolution of Social Organization: Phylogenetic Analyses of Ecology and Sexual Selection in Weavers.

AbstractCrook published a landmark study on the social organization of weavers (or weaverbirds, family Ploceidae) that contributed to the emergence of sociobiology, behavioral ecology, and phylogenetic comparative methods. By comparing ecology, spatial distribution, and mating systems, Crook suggested that the spatial distribution of food resources and breeding habitats influence weaver aggregation during both the nonbreeding season (flocking vs. solitary foraging) and the breeding season (colonial vs. solitary breeding), and the latter in turn impacts mating systems and sexual selection. Although Crook's study stimulated much follow-up research, his conclusions have not been scrutinized using phylogenetically controlled analyses. We revisited Crook's hypotheses using modern phylogenetic comparative methods on an extended data set of 107 weaver species. We showed that both diet and habitat type are associated with spatial distribution and that the latter predicts mating system, consistent with Crook's propositions. The best-supported phylogenetic path model also supported Crook's arguments and uncovered a direct relationship between nonbreeding distribution and mating system. Taken together, our phylogenetically corrected analyses confirm Crook's conjectures on the roles of ecology in social organizations of weavers; however, our analyses also uncovered an association between nonbreeding distributions and mating systems, which was not envisaged by Crook.

Shedding Lights on Crude Venom from Solitary Foraging Predatory Ant Ectatomma opaciventre: Initial Toxinological Investigation

Some species of primitive predatory ants, despite living in a colony, exercise their hunting collection strategy individually; their venom is painful, paralyzing, digestive, and lethal for their prey, yet the toxins responsible for these effects are poorly known. Ectatomma opaciventre is a previously unrecorded solitary hunting ant from the Brazilian Cerrado. To overcome this hindrance, the present study performed the in vitro enzymatic, biochemical, and biological activities of E. opaciventre to better understand the properties of this venom. Its venom showed several proteins with masses ranging from 1–116 kDa, highlighting the complexity of this venom. Compounds with high enzymatic activity were described, elucidating different enzyme classes present in the venom, with the presence of the first L-amino acid oxidase in Hymenoptera venoms being reported. Its crude venom contributes to a state of blood incoagulability, acting on primary hemostasis, inhibiting collagen-induced platelet aggregation, and operating on the fibrinolysis of loose red clots. Furthermore, the E. opaciventre venom preferentially induced cytotoxic effects on lung cancer cell lines and three different species of Leishmania. These data shed a comprehensive portrait of enzymatic components, biochemical and biological effects in vitro, opening perspectives for bio-pharmacological application of E. opaciventre venom molecules.

A Day in the Life of the Giant Ant Dinoponera lucida Emery, 1901 (Hymenoptera, Formicidae): Records of Activities and Intraspecific Interactions

Ants present a wide variety of nesting sites, feeding habits, and trophic interactions, but the biology of most species remains unknown. Dinoponera lucida is a poneromorph ant forest-specialist and solitary forager, endemic to the Brazil’s Atlantic Forest. Herein we describe foraging activities, guard and maintenance of the nests, orientation mode, and intraspecific interactions performed by D. lucida. We found three nests distant from each other at least 8.5 m, and the mean reached distance by a worker was 3.8 m. The workers showed colony fidelity and random forage in their territory. We observed two non-agonistic interactions between workers from the same nest, and two agonistic interactions between foraging workers from different nests. The low frequency of agonistic interactions suggests that workers from different nests are unlikely to forage in the same area. Our results expand the knowledge on ants’ natural history through data on foraging activities, guard and maintenance of the nests, orientation mode and intraspecific interactions.

Consensus driven by a minority in heterogenous groups of the cockroach Periplaneta americana

SummaryMany social species are able to perform collective decisions and reach consensus. However, how the interplay between social interactions, the diversity of preferences among the group members and the group size affects these dynamics is usually overlooked. The collective choice between odourous and odorless shelters is tested for the following three groups of social cockroaches (Periplaneta americana) which are solitary foragers: naive (individuals preferring the odorous shelter), conditioned (individuals without preference), and mixed (combining, unevenly, conditioned, and naive individuals). The robustness of the consensus is not affected by the naive individuals' proportion, but the rate and the frequency of selection of the odorous shelter are correlated to this proportion. In mixed groups, the naive individuals act as influencers. Simulations based on the mechanisms highlighted in our experiments predict that the consensus emerges only for intermediate group sizes. The universality of these mechanisms suggests that such phenomena are widely present in social systems.

Exploring the behavioral reactions to a mirror in the nocturnal grey mouse lemur: sex differences in avoidance.

Most mirror-image stimulation studies (MIS) have been conducted on social and diurnal animals in order to explore self-recognition, social responses, and personality traits. Small, nocturnal mammals are difficult to study in the wild and are under-represented in experimental behavioral studies. In this pilot study, we explored the behavioral reaction of a small nocturnal solitary forager—the grey mouse lemur (Microcebus murinus)—an emergent animal model in captivity. We assessed whether MIS can be used to detect a repeatable behavioral reaction, whether individuals will present a similar reaction toward a conspecific and the mirror, and whether males and females respond similarly. We tested 12 individuals (six males and six females) twice in three different contexts: with a mirror, with a live conspecific, and with a white board as a neutral control. We detected significant repeatability for the activity component of the behavioral reaction. There was a significant effect of the context and the interaction between presentation context and sex for avoidance during the first session for males but not for females. Males avoided the mirror more than they avoided a live conspecific. This pilot study opens a discussion on the behavioral differences between males and females regarding social interactions and reproduction in the nocturnal solitary species, and suggests that males are more sensitive to context of stimulation than females.

The effect of habitat quality on the blood parasite assemblage in understorey avian insectivores in the Eastern Himalaya, India

The anthropogenic alteration of natural habitats can modify interactions between various biotic and abiotic factors. The prevalence of avian blood parasites in free‐living host species in the tropics has shown contrasting patterns in altered landscapes. Here, we investigate these potential associations between understorey insectivorous bird species of the Eastern Himalayas and avian haemosporidians in primary and selectively logged forests. We describe patterns related to host–parasite associations, host life‐history traits and host specificity in primary and logged forests. Using parasite‐specific cytochrome‐b gene markers, we screened 545 individual birds from nine families, 33 genera and 57 species. Of these, 34.67% were infected with Leucocytozoon spp., 13.94% with Haemoproteus spp., 3.30% with Plasmodium spp. and 8.44% with co‐infections. We found that parasite prevalence did not change with logging; however, host specificity and life‐history traits did have associations with infection prevalence. We report a vertical stratification in genera‐specific infections driven by vector groups – upper canopy and midstorey foragers had high Leucocytozoon and Haemoproteus prevalence, respectively. In addition, species foraging in mixed‐species flocks showed increased infection risk with Leucocytozoon, whereas solitary foragers had a high prevalence of Plasmodium. This study also highlights that avian parasite lineages are genetically more distinct in primary forest than in logged forest plots. Although our study demonstrates no influence of selective logging on parasite prevalence, it does reflect a positive influence of host abundance and logged habitats on parasite diversity. Our work reveals valuable patterns in terms of phylospecificity and genetic variation in parasite assemblages. Further research with a focus on parasite intensity and vector abundance will help us to understand anthropogenic impacts on parasite transmission dynamics in Eastern Himalayan birds.

Fine-scale foraging effort and efficiency of Macaroni penguins is influenced by prey type, patch density and temporal dynamics

Difficulties quantifying in situ prey patch quality have limited our understanding of how marine predators respond to variation within and between patches, and throughout their foraging range. In the present study, animal-borne video, GPS, accelerometer and dive behaviour data loggers were used to investigate the fine-scale foraging behaviour of Macaroni penguins (Eudyptes chrysolophus) in response to prey type, patch density and temporal variation in diving behaviour. Individuals mainly dived during the day and utilised two strategies, targeting different prey types. Subantarctic krill (Euphausia vallentini) were consumed during deep dives, while small soft-bodied fish were captured on shallow dives or during the ascent phase of deep dives. Despite breeding in large colonies individuals seemed to be solitary foragers and did not engage with conspecifics in coordinated behaviour as seen in other group foraging penguin species. This potentially reflects the high abundance and low manoeuvrability of krill. Video data were used to validate prey capture signals in accelerometer data and a Support Vector Machine learning algorithm was developed to identify prey captures that occurred throughout the entire foraging trip. Prey capture rates indicated that Macaroni penguins continued to forage beyond the optimal give up time. However, bout-scale analysis revealed individuals terminated diving behaviour for reasons other than patch quality. These findings indicate that individuals make complex foraging decisions in relation to their proximate environment over multiple spatio-temporal scales.

Description of a Unique Solitary Feeding Strategy Observed in Bottlenose Dolphins (Tursiops truncatus) in the Biloxi Marsh, Louisiana

Bottlenose dolphins’ (Tursiops truncatus) foraging strategies in the Biloxi Marsh have received little attention when compared with other comparable habitats in the southeastern United States. Previous reports of dolphin foraging in this region have included sophisticated strategies such as strand feeding but have not included a detailed analysis of the observed behavior. Dolphins were observed performing a unique solitary foraging strategy, termed marsh bank feeding. Although this behavior was observed to occasionally result in stranding upon the marsh bank, it is argued here that the observed behavior is fundamentally different than the definitions for strand feeding, as well as other prominent shallow water foraging strategies. Video footage resulting from observations made between 2013 and 2019 were analyzed in order to establish the components of the behavior, enabling a detailed comparison to other dolphin foraging strategies.

Foragers of the stingless bee Plebeia droryana inform nestmates about the direction, but not the distance to food sources

The tropical stingless bees have evolved intricate communication systems to recruit nestmates to food locations. Some species are able to accurately communicate the location of food, whereas others simply announce the presence of food in the environment. Plebeia droryana is a tiny Neotropical stingless bee that, until recently, was thought to use a solitary foraging strategy, that is without the use of a recruitment communication system. However, recent research has indicated that P. droryana might be able to recruit nestmates to specific food source locations. We tested this by studying whether foragers can guide nestmates in the direction and the distance of artificial feeders placed in the vicinity of the colony. We trained bees to a scented sucrose solution feeder at 10 m and placed different feeders either in different directions (experiment 1) or in different distances (experiment 2). We found that P. droryana directs newcomers in the right direction, but distance information does not seem to be communicated. Moreover, we then tested whether newcomers use chemical and visual cues originating from nestmates foraging at the food source, but found no evidence for the use of these social cues provided by conspecifics. The potential mechanism that P. droryana may use to orient recruits toward the food source, however, remains unknown and requires further study.

Spatial cognition in the context of foraging styles and information transfer in ants.

Ants are central-place foragers: they always return to the nest, and this requires the ability to remember relationships between features of the environment, or an individual's path through the landscape. The distribution of these cognitive responsibilities within a colony depends on a species' foraging style. Solitary foraging as well as leader-scouting, which is based on information transmission about a distant targets from scouts to foragers, can be considered the most challenging tasks in the context of ants' spatial cognition. Solitary foraging is found in species of almost all subfamilies of ants, whereas leader-scouting has been discovered as yet only in the Formica rufa group of species (red wood ants). Solitary foraging and leader-scouting ant species, although enormously different in their levels of sociality and ecological specificities, have many common traits of individual cognitive navigation, such as the primary use of visual navigation, excellent visual landmark memories, and the subordinate role of odour orientation. In leader-scouting species, spatial cognition and the ability to transfer information about a distant target dramatically differ among scouts and foragers, suggesting individual cognitive specialization. I suggest that the leader-scouting style of recruitment is closely connected with the ecological niche of a defined group of species, in particular, their searching patterns within the tree crown. There is much work to be done to understand what cognitive mechanisms underpin route planning and communication about locations in ants.

Comparison of solitary and collective foraging strategies of Caenorhabditis elegans in patchy food distributions.

Collective foraging has been shown to benefit organisms in environments where food is patchily distributed, but whether this is true in the case where organisms do not rely on long-range communications to coordinate their collective behaviour has been understudied. To address this question, we use the tractable laboratory model organism Caenorhabditis elegans, where a social strain (npr-1 mutant) and a solitary strain (N2) are available for direct comparison of foraging strategies. We first developed an on-lattice minimal model for comparing collective and solitary foraging strategies, finding that social agents benefit from feeding faster and more efficiently simply owing to group formation. Our laboratory foraging experiments with npr-1 and N2 worm populations, however, show an advantage for solitary N2 in all food distribution environments that we tested. We incorporated additional strain-specific behavioural parameters of npr-1 and N2 worms into our model and computationally identified N2's higher feeding rate to be the key factor underlying its advantage, without which it is possible to recapitulate the advantage of collective foraging in patchy environments. Our work highlights the theoretical advantage of collective foraging owing to group formation alone without long-range interactions and the valuable role of modelling to guide experiments. This article is part of the theme issue 'Multi-scale analysis and modelling of collective migration in biological systems'.

Volatile Urinary Signals of Two Nocturnal Primates, Microcebus murinus and M. lehilahytsara

Mouse lemurs are small, nocturnal, arboreal solitary foragers and are endemic primates of Madagascar. This lifestyle and their high predation risk can explain why mouse lemurs rely heavily on olfaction for intraspecific communication. As they often use urine for this purpose, we investigated dichloromethane extracts of the urine of two mouse lemur species, the gray mouse lemur (Microcebus murinus) and the Godman’s mouse lemur (M. lehilahytsara), using gas-chromatography-mass spectrometry. We detected 977 different volatile compounds of different compound classes in 22 urine extracts obtained from nine M. murinus (four males, five females) and nine M. lehilahytsara (three males, six females) individuals. We compared the volatile profiles of the sexes and species using principal component analyses and discriminant function analyses and detected a significant difference in the urinary profiles of males and females and in the profiles of M. murinus and M. lehilahytsara. These very complex sex- and species-specific signatures could be used for distance communication in the context of species recognition, for mate search and in male-male competition. Our study provides important mechanistic insights into complex chemical signaling pathways in primates that are mirrored, in the case of mouse lemurs, by their extraordinarily rich repertoire of olfactory receptors. The production of highly informative olfactory signals may be complementing the complex acoustic signaling system of these solitary foragers suggesting the existence of a multimodal communication network that should be highly beneficial for any species living in dispersed social networks.

Factors influencing prey capture success and profitability in Australasian gannets (Morus serrator).

ABSTRACTKnowledge of the factors influencing foraging efficiency in top predators can provide insights into the effects of environmental variability on their populations. Seabirds are important marine predators foraging in a highly temporally and spatially variable environment. While numerous studies have focussed on search time and its effects on foraging energetics in seabirds, relatively little is known about the factors influencing capture success and prey profitability in these predators. In the present study, animal-borne cameras were used to investigate the chase durations, capture success, handling durations and profitability of prey consumed by Australasian gannets (Morus serrator) (n=95) from two breeding colonies in south-eastern Australia exposed to different oceanographic conditions. Capture success was generally lower when individuals foraged alone. However, foraging in multi-species groups and in high prey densities increased chase time, while larger prey elicited longer handling times. While prey type influenced profitability, high prey density and foraging in multi-species groups was found to lower prey profitability due to increased time expenditure. While previous studies have found group foraging reduces search time, the increased profitability explains why some animals may favour solitary foraging. Therefore, future studies should combine search time and the currently found factors.