Primate Crop Feeding Behavior,Crop Protection,and Conservation

Many species across a range of primate genera, irrespective of dietary and locomotory specializations, can and will incorporate agricultural crops in their diets. However, although there is little doubt that rapid, extensive conversion of natural habitats to agricultural areas is significantly impacting primate populations, primate crop foraging behaviors cannot be understood solely in terms of animals shifting to cultivated crops to compensate for reduced wild food availability. To understand fully why, how, and when primates might incorporate crops in their dietary repertoire, we need to examine primate crop foraging behavior in the context of their feeding strategies and nutritional ecology. Here I briefly outline current debates about the use of terms such as human–wildlife conflict and crop raiding and why they are misleading, summarize current knowledge about primate crop foraging behavior, and highlight some key areas for future research to support human–primate coexistence in an increasingly anthropogenic world.     

Crop Feeding by Brown Howlers (<Emphasis Type="Italic">Alouatta guariba clamitans</Emphasis>) in Forest Fragments: The Conservation Value of Cultivated Species

Primates inhabiting human-modified habitats often complement their diets with cultivated species. Although this flexible foraging behavior reduces feeding stress in animals inhabiting small or low-quality habitats, its potential economic costs may promote negative human–nonhuman primate interactions. It is critical to assess the importance of cultivated species to primate diets, the factors influencing their exploitation, and their associated economic costs to evaluate the conservation value of cultivated species and the impact of crop feeding on human–nonhuman primate coexistence. Based on a 30-months study of three groups of brown howlers (Alouatta guariba clamitans) inhabiting <10-ha forest fragments in Rio Grande do Sul State, southern Brazil, and semistructured interviews with landowners, we assessed 1) the cultivated species used as food sources, 2) the relationship between food availability and crop feeding, and 3) the potential economic costs of crop feeding and their impact on landowner–howler coexistence. Brown howlers exploited six cultivated species as fruit or seed sources. This exploitation was concentrated on ripe fruit of Psidium guajava, Citrus reticulata, Diospyros kaki, and Eriobotrya japonica, which together accounted for up to 32% of total feeding records during some months. Availability predicted fruit consumption for three of these species. The overall availability of cultivated fruit also predicted its consumption, whereas overall wild fruit availability did not. Despite potential economic costs of crop feeding (US$320–US$1141 per year), landowners reported no conflict with howlers arising from their behavior, an amicable response that supports the conservation value of cultivated plants in different landscape elements of the anthropogenic matrix.     

Buton macaques (Macaca ochreata brunnescens): crops, conflict, and behavior on farms

One consequence of anthropogenic habitat alteration is that many nonhuman primates are forced into conflict interactions with humans and their livelihood activities, especially through crop raiding. These problems are particularly acute for the endemic and threatened Buton Island macaque (Macaca ochreata brunnescens), in southeast Sulawesi, Indonesia. Our study investigated the crop raiding behavior of this species over time. Foods eaten and the behavioral repertoire exhibited by macaques during crop raiding at and inside farm perimeters were observed over a period of 8 years (2002–2009). Storage organ crops (e.g. sweet potato) were abundant and most frequently raided by macaques. Individual macaques were most commonly observed to raid close (0–10 m) to farm perimeters. Activities such as feeding, resting, moving, and social interaction varied significantly as a function of penetration distance into the farm, but only marginally between age‐sex classes. The annual average raid frequency per farm decreased over the latter years of the study period, raising questions about changes in macaque foraging and ranging behavior over time and their response to farm management and mitigation strategies. Am. J. Primatol. 74:29–36, 2012. © 2011 Wiley Periodicals, Inc.     

Seasonal variation of feeding patterns and food selection by crop-raiding elephants in Zimbabwe

Elephants and humans are increasingly coming into conflict because of the conversion of elephant habitat into agricultural areas. In order to identify trends that influence raiding behaviour, the nutritional makeup of food items consumed by crop‐raiding elephants over a 2‐year period were analysed and a trigger for crop raiding was identified. The point at which the quality of wild grasses declines below the quality of crop species corresponded to the movement of bull elephants out of a protected area and into fields. This finding may have wider implications for developing predictive models of elephant/human interactions.     

Nutritional Characteristics of Wild and Cultivated Foods for Chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) in Agricultural Landscapes

Primate habitats are being transformed by human activities such as agriculture. Many wild primates include cultivated foods (crops) in their diets, calling for an improved understanding of the costs and benefits of crop feeding. We measured the macronutrient and antifeedant content of 44 wild and 21 crop foods eaten by chimpanzees (Pan troglodytes schweinfurthii) in a mosaic habitat at Bulindi, Uganda, to evaluate the common assertion that crops offer high nutritional returns compared to wild forage for primates. In addition, we analyzed 13 crops not eaten at Bulindi but that are consumed by chimpanzees elsewhere to assess whether nutritional aspects explain why chimpanzees in Bulindi ignored them. Our analysis of their wild plant diet (fruit, leaves, and pith) corresponds with previous chemical analyses of primate plant foods. Compared to wild food equivalents, crops eaten by the chimpanzees contained higher levels of digestible carbohydrates (mainly sugars) coupled with lower amounts of insoluble fiber and antifeedants. Cultivated fruits were relatively nutritious throughout the ripening process. Our data support the assumption that eating cultivated foods confers energetic advantages for primates, although crops in our sample were low in protein and lipids compared to some wild foods. We found little evidence that crops ignored by the chimpanzees were less nutritious than those that they did eat. Nonnutritional factors, e.g., similarity to wild foods, probably also influence crop selection. Whether cultivated habitats can support threatened but flexible primates such as chimpanzees in the long term hinges on local people’s willingness to share their landscape and resources with them.     

Gut microbiota composition of Japanese macaques associates with extent of human encroachment

In recent decades, human–wildlife interaction and associated anthropogenic food provisioning has been increasing and becoming more severe due to fast population growth and urban development. Noting the role of the gut microbiome in host physiology like nutrition and health, it is thus essential to understand how human–wildlife interactions and availability of anthropogenic food in habitats can affect an animal's gut microbiome. This study, therefore, set out to examine the gut microbiota of Japanese macaques (Macaca fuscata) with varying accessibility to anthropogenic food and the possibility of using gut microbiota as indicator for macaques’ reliance on anthropogenic food. Using 16S ribosomal RNA gene sequencing, we described the microbial composition of Japanese macaques experiencing different types of human disturbance and anthropogenic food availability—captive, provisioned, crop‐raiding, and wild. In terms of alpha diversity, our results showed that observed richness of gut microbiota did not differ significantly between disturbance types but among collection sites, whereas Shannon diversity index differed by both disturbance types and sites. In terms of beta diversity, captive populations harbored the most distinctive gut microbial composition, and had the greatest difference compared with wild populations. Whereas for provisioned and crop‐raiding groups, the macaques exhibited intermediate microbiota between wild and captive. We identified several potential bacterial taxa at different taxonomic ranks whose abundance potentially could help in assessing macaques’ accessibility to anthropogenic food. This study revealed the flexibility of the gut microbiome of Japanese macaques and provided possible indices based on the gut microbiome profile in assessing macaques’ accessibility to/reliance on anthropogenic foods.     

Flowers Are an important food for small apes in southern Sumatra

Flowers are included in the diets of many primates, but are not generally regarded as making an important contribution to primate energy budgets. However, observations of a number of lemur, platyrrhine, and cercopithecine populations suggest that some flower species may function as key primate fallback foods in periods of low abundance of preferred foods (generally ripe fruits), and that flowers may be preferred foods in some cases. I report heavy reliance on flowers during some study months for a siamang (Symphalangus syndactylus) population in southern Sumatra. Siamangs at Way Canguk spent 12% of feeding time eating flowers from October 2000 to August 2002, and in 1 month flower‐feeding time exceeded 40% of total feeding time. The overall availabilities of fig and nonfig fruits, flowers, and new leaves in the study area were not significant predictors of the proportion of time that siamangs spent consuming any plant part. However, flower‐feeding time was highest in months when nonfig fruit‐feeding time was lowest, and a switch from heavy reliance on fruit to substantial flower consumption was associated with a shift in activity patterns toward reduced energy expenditure, which is consistent with the interpretation that flowers may function as a fallback food for Way Canguk siamangs. Hydnocarpus gracilis, a plant from which siamangs only consume flowers, was the third‐most‐commonly consumed plant at Way Canguk (after Ficus spp. and Dracontomelon dao), and flowers from this plant were available in most months. It is possible that relatively high local availability of these important siamang plant foods is one factor promoting high siamang density in the study area. Am. J. Primatol. 71:624–635, 2009. © 2009 Wiley‐Liss, Inc.     

The effects of extreme seasonality of climate and day length on the activity budget and diet of semi‐commensal chacma baboons (Papio ursinus) in the Cape Peninsula of South Africa

We examined the effects of extreme seasonality on the activity budget and diet of wild chacma baboons with access to a high‐quality, human‐derived food source. The Cape Peninsula of South Africa is unusual among nonhuman primate habitats due to its seasonal extremes in day length and climate. Winter days are markedly shorter and colder than summer days but have higher rainfall and higher primary production of annually flowering plants. This combination of fewer daylight hours but higher rainfall is substantially different from the ecological constraints faced by both equatorial baboon populations and those living in temperate climates with summer rainfall. We sought to understand how these seasonal differences affect time budgets of food‐enhanced troops in comparison to both other food‐enhanced troops and wild foraging troops at similar latitudes. Our results revealed significant seasonal differences in activity budget and diet, a finding that contrasts with other baboon populations with access to high‐return anthropogenic foods. Similar to nonprovisioned troops at similar latitudes, troop members spent more time feeding, socializing, and traveling during the long summer days compared to the short winter days, and proportionately more time feeding and less time resting in summer compared to winter. Summer diets consisted mainly of fynbos and nonindigenous foods, whereas winter diets were dominated by annually flowering plants (mainly grasses) and ostrich pellets raided from a nearby ostrich farm. In this case, food enhancement may have effectively exaggerated seasonal differences in activity budgets by providing access to a high‐return food (ostrich pellets) that was spatially and temporally coincident with abundant winter fallback foods (grasses). The frequent use of both alien vegetation and high‐return, human‐derived foods highlights the dietary flexibility of baboons as a key element of their overall success in rapidly transforming environments such as the South African Cape Peninsula. Am. J. Primatol. 72:104–112, 2010. © 2009 Wiley‐Liss, Inc.     

Responses of Javan Gibbon (Hylobates moloch) Groups in Submontane Forest to Monthly Variation in Food Availability: Evidence for Variation on a Fine Spatial Scale

Primates tend to prefer specific plant foods, and primate home ranges may contain only a subset of food species present in an area. Thus, primate feeding strategies should be sensitive to the phenology of specific species encountered within the home range in addition to responding to larger scale phenomena such as seasonal changes in rainfall or temperature. We studied three groups of Javan gibbons (Hylobates moloch) in the Gunung Halimun‐Salak National Park, Indonesia from April 2008 to March 2009 and used general linear mixed models (GLMM) and a model selection procedure to investigate the effects of variation in fruit and flower availability on gibbon behavior. Preferred foods were defined as foods that are overselected relative to their abundance, while important food species were those that comprised >5% of feeding time. All important species were also preferred. Season and measurements of flower and fruit availability affected fruit‐feeding time, daily path lengths (DPL), and dietary breadth. Models that included the availability of preferred foods as independent variables generally showed better explanatory power than models that used overall fruit or flower availability. For one group, fruit and preferred fruit abundance had the strongest effects on diets and DPL in the models selected, while another group was more responsive to changes in flower availability. Temporal variation in plant part consumption was not correlated in neighboring groups. Our results suggest that fine‐scale local factors are important determinants of gibbon foraging strategies. Am. J. Primatol. 74:1154‐1167, 2012. © 2012 Wiley Periodicals, Inc.     

Supplemented howler monkeys eat less wild fruits,but do not change their activity budgets

Research on the influence of food supplementation on primate behavior has focused on terrestrial and semiterrestrial species. Its effects on highly arboreal species are poorly known. We assessed the influence of food supplementation on the feeding behavior and activity budget of four adult female and two adult male brown howler monkeys (Alouatta guariba clamitans) belonging to two groups (JA and RO) that inhabited periurban forest fragments in southern Brazil. We used the “focal‐animal” method during 6–8 full days per month from March to August 2017 (916 h of observation) to record the behavior of the study subjects. The feeding events of the focal individual were recorded using the “all occurrences” method. The supplementation was unevenly distributed during the day and accounted for 5–6% of all feeding events of male and female howlers, respectively. JA always received fruit in a platform, whereas RO had access to fruits and processed foods on roofs and directly from humans. The mean biomass of wild foods ingested by each adult per day was >300% higher than the ingested biomass of supplemented foods (females: 395 vs. 109 g/day; males: 377 vs. 120 g/day), but the ingestion rate of supplemented foods was ca. 400% higher than that of wild foods (females: 17 vs. 4 g/min; males: 19 vs. 5 g/min). The activity budgets of females and males were dominated by resting (66–72%) followed by feeding (18–14%), moving (12–11%), and socializing (2%). We found that food supplementation reduced the ingestion of wild fruits, but it did not affect the howlers’ need to ingest a given amount of leaves per day and the time spent resting, feeding, moving, and socializing.     

Exploring the effects of spatial autocorrelation when identifying key drivers of wildlife crop‐raiding

Few universal trends in spatial patterns of wildlife crop‐raiding have been found. Variations in wildlife ecology and movements, and human spatial use have been identified as causes of this apparent unpredictability. However, varying spatial patterns of spatial autocorrelation (SA) in human–wildlife conflict (HWC) data could also contribute. We explicitly explore the effects of SA on wildlife crop‐raiding data in order to facilitate the design of future HWC studies. We conducted a comparative survey of raided and nonraided fields to determine key drivers of crop‐raiding. Data were subsampled at different spatial scales to select independent raiding data points. The model derived from all data was fitted to subsample data sets. Model parameters from these models were compared to determine the effect of SA. Most methods used to account for SA in data attempt to correct for the change in P‐values; yet, by subsampling data at broader spatial scales, we identified changes in regression estimates. We consequently advocate reporting both model parameters across a range of spatial scales to help biological interpretation. Patterns of SA vary spatially in our crop‐raiding data. Spatial distribution of fields should therefore be considered when choosing the spatial scale for analyses of HWC studies. Robust key drivers of elephant crop‐raiding included raiding history of a field and distance of field to a main elephant pathway. Understanding spatial patterns and determining reliable socio‐ecological drivers of wildlife crop‐raiding is paramount for designing mitigation and land‐use planning strategies to reduce HWC. Spatial patterns of HWC are complex, determined by multiple factors acting at more than one scale; therefore, studies need to be designed with an understanding of the effects of SA. Our methods are accessible to a variety of practitioners to assess the effects of SA, thereby improving the reliability of conservation management actions.     

Gastrointestinal Parasites in Crop Raiding and Wild Foraging Papio anubis in Nigeria

We compared parasitic infection in a crop-raiding and a wild-foraging troop of olive baboons, Papio anubis, in Gashaka Gumti National Park, Nigeria, to quantify how crop raiding may have influenced primate-parasite interactions. We recovered gastrointestinal parasites from fecal samples from all adult individuals in both troops and processed them via formal-ether sedimentation. We compared parasitic species richness, prevalence, output, and load across troops. We recovered 9 parasite taxa. The wild-foraging troop had a significantly higher mean output than the crop-raiding troop for Physaloptera sp., Trichuris sp., and also a significantly higher total helminth load. The crop-raiding troop had a significantly higher mean output for the protozoan Balantidium coli and also showed a higher parasitic species richness, with 9 species recovered compared to the 7 recorded for the wild-foraging individuals. The changes in nutritional intake, behavior, and human proximity caused by crop raiding may have important epidemiological impacts on wild primate populations, and the nature of such impacts may vary across different taxa of parasites.     

The macronutrient composition of wild and cultivated plant foods of West African chimpanzees (Pan troglodytes verus) inhabiting an anthropogenic landscape

Agricultural expansion encroaches on tropical forests and primates in such landscapes frequently incorporate crops into their diet. Understanding the nutritional drivers behind crop-foraging can help inform conservation efforts to improve human-primate coexistence. This study builds on existing knowledge of primate diets in anthropogenic landscapes by estimating the macronutrient content of 24 wild and 11 cultivated foods (90.5% of food intake) consumed by chimpanzees (Pan troglodytes verus) at Bossou, Guinea, West Africa. We also compared the macronutrient composition of Bossou crops to published macronutrient measures of crops from Bulindi, Uganda, East Africa. The composition of wild fruits, leaves, and pith were consistent with previous reports for primate diets. Cultivated fruits were higher in carbohydrates and lower in insoluble fiber than wild fruits, while wild fruits were higher in protein. Macronutrient content of cultivated pith fell within the ranges of consumed wild pith. Oil palm food parts were relatively rich in carbohydrates, protein, lipids, and/or fermentable fiber, adding support for the nutritional importance of the oil palm for West African chimpanzees. We found no differences in the composition of cultivated fruits between Bossou and Bulindi, suggesting that macronutrient content alone does not explain differences in crop selection. Our results build on the current understanding of chimpanzee feeding ecology within forest-agricultural mosaics and provide additional support for the assumption that crops offer primates energetic benefits over wild foods.     

Crop Damage by Primates: Quantifying the Key Parameters of Crop-Raiding Events

Human-wildlife conflict often arises from crop-raiding, and insights regarding which aspects of raiding events determine crop loss are essential when developing and evaluating deterrents. However, because accounts of crop-raiding behaviour are frequently indirect, these parameters are rarely quantified or explicitly linked to crop damage. Using systematic observations of the behaviour of non-human primates on farms in western Uganda, this research identifies number of individuals raiding and duration of raid as the primary parameters determining crop loss. Secondary factors include distance travelled onto farm, age composition of the raiding group, and whether raids are in series. Regression models accounted for greater proportions of variation in crop loss when increasingly crop and species specific. Parameter values varied across primate species, probably reflecting differences in raiding tactics or perceptions of risk, and thereby providing indices of how comfortable primates are on-farm. Median raiding-group sizes were markedly smaller than the typical sizes of social groups. The research suggests that key parameters of raiding events can be used to measure the behavioural impacts of deterrents to raiding. Furthermore, farmers will benefit most from methods that discourage raiding by multiple individuals, reduce the size of raiding groups, or decrease the amount of time primates are on-farm. This study demonstrates the importance of directly relating crop loss to the parameters of raiding events, using systematic observations of the behaviour of multiple primate species.     

The influence of lunar cycles on crop‐raiding elephants; evidence for risk avoidance

Long‐term solutions to crop raiding by elephants (Loxodonta africana) should be based on an understanding of their behaviour and ecology. The real and perceived risks from humans have been shown to affect elephant behaviour. This is evidenced by elephants predominantly raiding crops at night, avoiding the height of human activity. If such human avoidance behaviours are apparent, it might also be expected that elephants avoid risks associated with higher visibility and increased human activity as may occur during the full moon. However, elephant nocturnal crop‐raiding behaviour in relation to lunar cycles has largely been a neglected factor in studies of human–elephant interactions. In this study around Mikumi National Park, Tanzania, we apply circular statistics in this context for the first time to show a significant decrease in crop raiding during the full moon and apply this method retrospectively to data from another site in West Africa with similar results. Additionally, a greater proportion of farms raided was guarded during the full moon than any other moon phase. Our results indicate that variations in crop raiding with lunar phase could be a general feature of elephant behaviour and thus could be used to design and time mitigation efforts.     

Distinguished primatologist address—moving from advocacy to activism: Changing views of primate field research and conservation over the past 40 years

Field studies of wild nonhuman primates have grown exponentially over the past 40 years and our knowledge of primate behavior, ecology, and social, and mating systems has expanded greatly. However, we are facing a major extinction crisis with some 60% of all primate species listed as threatened and more than 75% of species with declining populations. The primary factor driving primate population decline is human population increase, which over the past 50 years has resulted in the unsustainable conversion and degradation of natural landscapes for industrial agriculture, the production of nonagricultural commodities for international trade, pastureland for cattle, dam construction, fossil fuel exploration, mining, and the construction of road networks and infrastructure to support large urban centers. Recent ecological modeling predicts that by the end of the century, the four primate‐richest countries in the world will lose 32–78% of their existing primate habitat to agricultural expansion, and nine of the top 15 primate‐richest countries are expected to have 80–100% of their primate species extinct or threatened with extinction. If we are going to save the world's primates, the time to act is now! Not only should all primate field research include a strong conservation component, but in addition we must actively join with our professional societies, zoos and research facilities, universities, conservation organizations, concerned business leaders, global citizens, like‐minded political leaders, and grassroots organizations to inform, demand and direct governments, multinational corporations, and international organizations to engage in transformational change to protect biodiversity and seek environmental justice against those entities that actively destroy our planet. As the chief academic discipline dedicated to the study of primates, we must organize and collectively move from being advocates for primate conservation to becoming activists for primate conservation. This is a call to action.     

Patterns and perceptions of wildlife crop raiding in and around Kerinci Seblat National Park, Sumatra

Crop raiding can reduce farmers' tolerance towards wildlife. Despite higher human population densities in rural areas, and more rapid conversion of forest to farmland, much less is known about crop raiding in Asia than in Africa. Over 14 months, we identified perceived and actual crop pests, and their patterns of crop raiding from farmland in and around Kerinci Seblat National Park, Sumatra. Farmers named either the wild boar Sus scrofa (80%) or the pig-tailed macaque Macaca nemestrina (20%) as the two most destructive crop pests. From 5125 crop raids by 11 species of mammal, most raids were indeed made by the wild boar (56%) and the pig-tailed macaque (19%). For all species combined, temporal crop raiding peaks were positively correlated with periods of high rainfall. Spatially, most crop raids occurred nearest to the forest edge and the local guarding strategies used were ineffective. However, raids by wild boars were more extensive than raids by pig-tailed macaques, which caused much greater crop damage (73%) than wild boars (26%), contrary to farmers' perceptions. Our research suggests that alternative mitigation strategies need to be trialed over dry and rainy seasons to identify the most effective strategies and that guarding effort should be increased during the rainy seasons and tailored towards specific crop raiding species based on their unique spatial patterns.     

The conflict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda

Forty‐seven property owners in Entebbe, Uganda were questioned about vervet monkey activities on their property. Our main objective was to investigate the interactions between humans and vervet monkeys in an agricultural area adjacent to a forest zone. Other studies have reported that farms located within 300 m of a forested boundary probably incur the greatest risk of crop‐raiding. Two other factors that may influence susceptibility to vervet crop‐raiding were also examined: the types of crops grown and the types of direct preventative measures used. The effect of these two factors on vervet crop‐raiding is not straightforward. However, the distance a property is located from the forest edge is an important factor influencing vervet crop‐raiding. Surveyed gardens 200 m from the forest edge received significantly less crop‐raiding than farms located 100 m or 50 m (P = 0.040, < α = 0.05). We suggest that the development of nonagricultural activities on land directly adjacent to forested areas may reduce vervet crop‐raiding by deterring vervets from travelling greater distances from the forest edge due to increased obstacles or risks.     

Responses to novel foods in captive chimpanzees

Hesitancy to eat novel foods hampers the immediate enlargement of the diet but serves to limit the risk of ingesting toxic foods. Neophobia has been systematically investigated in only a few primate species, in which it appears to be affected by social influences. Surprisingly, little is known about neophobia in chimpanzees. We studied the response of eight adult captive chimpanzees to 16 foods (foods commonly eaten by humans and never tasted before by chimpanzees). Each novel food was presented twice to the chimpanzee by a familiar or an unfamiliar human. Between the two trials the human ate the food face to face with the chimpanzee (demonstration). Results showed that some foods were almost unanimously accepted, whereas others were not. Moreover, there were marked interindividual differences in food acceptance and consumption; chimpanzees ranged from being almost completely neophobic to accepting almost all foods. Familiarity with the human and the human's demonstration did not affect responses to the foods. The humans' predictions concerning the chimpanzees' acceptance of the different foods were rather good; furthermore, in seven cases out of eight the humans' preferences did not correlate with their predictions on the chimpanzees' preferences. The finding that most captive chimpanzees are initially cautious toward novel foods supports the little information there is regarding this subject in wild chimpanzees. However, the lack of influence of the humans' familiarity and demonstration on the response to food by the chimpanzees calls for more naturalistic studies, in which social influences are provided by group members. Since novel stimuli provide sensory stimulation and elicit exploration and social interest, occasional presentation of novel foods could be a promising and cheap device for feeding enrichment. Zoo Biol 21:539–548, 2002. © 2002 Wiley‐Liss, Inc.