The Palenque Archaeological Zone-National Park stretches across 1771 hectares. It is located in the northern limit of the Lacandona forest in Chiapas. Palenque was one of the great Mayan cities during the classic period (250-900 BC). It reached peak development between 600 BC and 800 BC. After different conflicts and invasions, this and other Mayan towns declined and were almost completely abandoned (Mathews, 2007). Nearly 600 hectares of high evergreen forest still remain, altered but maintaining its ecological structure thanks to the local authorities in charge of preserving the archaeological zone. The monkeys thriving in the area that are a food source for dung beetles are the black howler or howler monkey, Alouatta pigra Lawrence, 1933, which is relatively abundant, and the spider monkey, Ateles geoffroyi (Kuhl, 1820).

We collected dung beetles for 24 h on 21 June 1993. Traps were set at 5 m, 10 m, 15 m, and 20 m high onto six large trees separated by almost two hundred meters between them in the forest, far from the archaeological zone. Each trap consisted of a 9 cm × 9 cm × 8 cm plastic box with a triangular opening in the lid, filled with a 2 cm-thick layer of soil and baited with 4 g of human feces or carrion (fish) (for further details, refer to Halffter and Favila, 1993). The baits remained active for 24 hours. The results reflect the total number of beetles collected in 25 traps, six baited with fish carrion and 19 with human feces (Table 1).

We constructed a database conducting a systematized search of peer-reviewed papers on the Web of Science (WoS) to collect the studies about the species of dung beetles associated with monkeys in the Neotropical region and other regions of the world. The search was conducted during the first semester of 2023, including articles published from 1980 to 2023. We search the next terms in the title, abstract, and keywords for each paper: “arboreal dung beetle*” AND “arboreal carrion beetles” AND “monkeys and dung beetles” OR “vertical stratification dung beetles” OR “perching dung beetles” OR “dung beetles and trees”. In addition, we used other search strategies to broaden the scope of the review, such as directly contacting some authors.

The WoS search retrieved 277 articles, of which we included only those meeting the following criteria: the study should analyze arboreal, perching, and/or flying behaviors of dung beetles associated with monkeys, food location, or search of mates in tropical forests. After reviewing the titles and abstracts of the full WoS search results, we selected 12 articles for a full review, which were those related to the monkeys and arboreal dung beetles, perching behavior, and dung beetles in trees. As the systematic search did not capture articles or chapters that were published before 1980 or the journal or book lacked a digital repository, we used other search strategies to broaden the scope of the review such as directly contacting some authors and including articles from the personal library of the authors.

We extracted the following data from the selected literature: a) the taxonomic identity of each dung beetles species studied (current names of species were used in case of synonyms or new combinations; b) study location, including locality and country; the environment and known food resources of each species c) flying behavior observed in different dung beetle species, including duration, location of the food or mate; d) average duration of flying behavior observed in different dung beetle species; f) nest characteristics in the trees (structure, complexity, and location relative to the base of the tree); g) male/female nesting behavior h) male/female searching behavior, perching heights.

The most frequent species collected on trees was Canthon euryscelis Bates, 1867 (418 individuals), followed by Canthon subhyalinus Harold, 1867 (387 individuals), Canthon angustatus Harold, 1867 (307 individuals), and Canthon femoralis (Chevrolat, 1834) (102 individuals) (Table 1). All these Canthon species are small and skilled fliers, suggesting a strong relationship with monkeys, but maybe also with other mammals and reptiles living on trees. Canthon euryscelis and Canthon angustatus were mostly collected at 5 m high (50.23% and 52.4%, respectively, of individuals collected in aerial traps) and 15 m high (36.12% and 35.8% respectively); however, C. euryscelis was collected more frequently at 10 m than at 20 m (11.2% and 2.4%, respectively), and the opposite occurred for C. angustatus (1.9% and 9.7%, respectively). More Canthon subhyallinus individuals were collected a 5 m (41.6%), then at 10 m (33.3%) and 15 m (23.3%) high, but were rarely caught at 20 m high (1.8%). Only a single individual of Onthophagus maya Zunino, 1981, was collected at 5 m high (Table 1).

This section outlines the information gathered about arboreal dung beetles inhabiting the tropical forests of México. This information shows that the association of a certain beetle species with monkey dung is common in a given location but varies significantly between sites. The relationship between beetles and monkey dung is strong and determines the abundance of some species in the canopy, being substantially reduced at ground level. In the tropical forests of southern Mexico, four species of Scarabaeinae (Canthon spp.) show this relationship with the monkeys Alouatta palliata (Gray, 1849), A. pigra Lawrence, 1933, and probably with Ateles geoffroyi Gray, 1866.

The relationship between dung beetles and monkeys observed in Mexico also occurs in Central America. In Panama, Howden and Young (1981) reported Canthon angustatus Harold and Canthon subyhalinus Harold caught in traps at more than 20 m high within forested areas. Canthon subyhalinus, was found on the leaves among fresh monkey dung masses. The Canthon species fall to the ground clinging to the ball, where the usual rolling process continues. For its part, Gill (1991) observed Canthon aequinoctiale Harold, 1869, at 8 m high eating monkey dung deposited on the leaves but has not been seen building food balls. This author reports highly abundant Canthon (Glaphyrocanthon) sp. associated with Callicebus monkey dung at 10 m high, along with some individuals of Sylvicanthon foveivenre (Schmit, 1920) plus a few specimens of other two Scarabaeinae species. Gill (1991) reported Canthon angustatus in a tropical forest of Panama making balls of monkey dung in the forest canopy.

For reasons not yet explained, there is a remarkable change in the dung beetle-monkey relationship in forests of southwestern Mexico, Central America, and South America. In the tropical forests of Mexico and Central America, there is a clear relationship of Canthon species with monkeys, mostly of the genus Alouatta, with differences in abundances between sites. The perching behavior is common in these Canthon species. According to Gill (1991), the two foraging behaviors observed in dung beetles in the Neotropical region are perching and flying, and differences in both behaviors may influence the dispersal ability of the species. Fast fliers are also widely distributed across South America and Central America. Comparing the geographic range of perching versus flying species during foraging will help to determine whether these two foraging behavior strategies are related.

Noriega (2011) collected Canthon smaragdulus (Fabricius, 1781) in Colombia using a new model of elevated pitfall traps baited with Alouatta seniculus dung. Later, in a study carried out in the same locality, Noriega (2012) compared the assemblages of dung beetles that reached the feces of A. seniculus and Lagothrix lagotricha (Humboldt, 1812), finding 32 species and marked differences in the species composition of beetles attracted by each dung type. Subsequently, Noriega et al. (2020) collected 369 specimens of 21 dung beetle species perching on plants. These included three species of Onthophagus, seven Canthidium, two Dichotomius, two Eurysternus, two Phanaeini (Oxyternon conscipillatum (Weber, 1801) and Phanaeus chalcomelas (Perty, 1830) and five Deltochilini, including Sylvicanthon aequinoctialis (Harold, 1869). Undoubtedly, this assemblage of beetles associated with monkeys is markedly different from the ones collected in Mexico and Central America. Finally, Noriega and Vulinec (2021) summarized the information on dung beetles perching on leaves worldwide.

In the tropical forests of Peru, the relationship of dung beetles with tamarin monkeys (Seguinus myxtrax Spix and Seguinus fuscicollis Spix) was studied by Culot et al. (2011). They followed a tamarin group and collected their feces immediately after defecation. Traps baited with this dung were buried in the ground for 24 hours. These authors collected 330 beetles of 25 species of Scarabaeinae. The medium-sized-to-large species included two Canthidium, two Dichotomius, and numerous species of rollers (Deltochilini). Also in Peru, Larsen et al. (2006) captured Canthon brunneus, C. femoralis bimaculatus, C. sp., and C. subyhalinus in the canopy of a primary terra firma or a floodplain forest. In the French Guiana, Feer (2000; 2015) noted that a severe reduction of the arboreal mammal fauna may also reduce the Scarabaeinae fauna (refer to Nichols et al., 2009).

Vulinec (2002) examined beetles associated with monkeys in Peru, the Amazonas, and Rondonia (Brazil). She estimated that primates eat between 25% and 40% of the biomass produced by the forest, being they an essential element in the food chain. When a part of the forest is cleared, the populations of Scarabaeinae beetles also decrease. Alouatta palliata is a diurnal monkey frequently observed on fig trees (Gill, 1991). Its feces attract multiple species, including hundreds of individuals of C. angustatus, which form a dense cloud that covers the area where monkeys thrive. The stinking, greenish-yellow dung is defecated in the forest canopy, falling onto the vegetation as a cascade. This excrement is transported by beetles as firm balls that are rolled in the canopy until they fall to the ground with the beetles clinging to them. Once on the ground, beetles form male-female pairs that keep rolling the food ball.

Halffter and Matthews (1966) published the first review on the ecology and behavior of the Scarabaeinae, including several of the first publications addressing the relationship between dung beetles and monkeys (or, where appropriate, other mammals). Thus, according these authors Luederwaldt (1922) reported individuals of Canthon (Glaphyroncanthon) quadrigutatus (Olivier) in Tapajos, Brazil, on both monkey feces and a recently hunted monkey, with about ten specimens around the anus. The monkey was reported as corresponding to Alouatta sp by Pereira and Martínez (1956). According to these authors, C. subhyalinus was collected from another monkey, Callicebus brunnens Wager, in Guapó, Brazil.

Vaz de Mello and Louzada (1997) reported the capture in Viçosa, Minas Gerais, Brazil, of 22 specimens of Sylvicanthon foveiventris (Schmidt) (a Canthonina beetle) in traps baited with human feces at 10 m high in the forest, in addition to Canthon (Glaphyrocanthon) sp., Parahyboma furcatum (Laporte, 1840), and Canthidum sp. The forest is home to a rich fauna of Scarabaeinae, including the beetles that thrive on the ground. Although illustrative, the publications reviewed for South America are punctual and in quantity and quality. Some of the beetle species associated with monkeys in Mexico are also found in South America, but other arboreal beetle species in this region are larger than Canthon species (Vaz de Mello and Louzada, 1997).

Published works on African dung beetles are scarce. Walter (1983) studied the beetle-monkey relationship in Gabon, specifically in the Mpassa forest. This was the first study addressing the Scarabaeinae in the canopy of African forests. Traps were placed at 3 m, 5 m, 10 m, and 21 m high in dense, humid, evergreen forests. The traps were wooden squares (50 cm × 50 cm) affixed horizontally at the heights indicated. The lid had a central orifice, which attracted the specimens into the baited trap. Walter collected five species at different heights (Table 2). Similar to our sampling in Mexico, he observed few abundant species. The three most common species were collected mainly at 5 m and 10 m high. All the beetle species caught are small. Sisyphus does not exceed 5 mm in length and Onthophagus is 3.5 mm in length; the exception was O. mpassa, which is 7.2 mm in length. Onthophagus ahenominas (4 specimens) and O. mppasa were the rarest species. The other three beetle species were abundant. Arboreal Sisyphus species make the ball in the canopy, and before leaving it, the ball remains attached to a leaf or a branch, not falling to the ground. Onthophagus species cannot bury their eggs in trees. Thus, eggs are scattered among the dung in the canopy. The association of these beetle species with monkeys and the canopy has made them lose the nesting habit throughout evolution, returning to a highly primitive form, similar to the most primitive Scarabaeinae. Walter (1981) described that Sisyphus arboreus makes balls and rolls them in the canopy of forest trees. In addition, four species of Onthophagus use dung excreted in situ. These fascinating data from Walter are the first to report an Onthophagus species as a roller of an elaborate ball.

The comments by Hanski and Cambefort (1991) on the Scarabaeinae-monkey relationship in Africa do not fully coincide with those by Walter (1985). The information reported by Hanski and Cambefort (1991) was recorded from the Makukon forests and referred to three species collected between 10 m and 20 m high. A Sisyphus individual was observed rolling a dung ball in the canopy. They also reported that Onthophagus, unable to dig in the canopy, accumulates dung and litter to form a mass that protects the eggs.

The relationship between beetles and monkeys in Africa mentioned above is consistent with our observations in Mexico: very few important beetle species are highly abundant at different heights in forest trees. These findings contrast markedly with the reports for South America and the cases mentioned below, where multiple species are associated with monkey dung.

In the Madagascar forest, the small roller beetle Arachnodes gandi was observed making nests at ground level and 50 cm high (Vadon, 1947). According to Vadon (1947), A. gandi makes a dung ball in the canopy, which falls to the ground, and the beetle continues rolling it as described for other rollers.

This region hosts multiple species of dung beetles, some of which are very large, associated with monkeys of many different taxa. By contrast, in Mexico and Central America this role is played by the Canthonini, which are also abundant in other areas of the Neotropics.

In the Western Ghats, a global biodiversity hotspot in southwestern India, Sabu and Nithya (2016) collected Caccobius gallinus Arrow, Caccobius meridionalis Boucomont, Onthophagus vladimiri Frey, Onthophagus furcillifer Bates, and Onthophagus centricornis (Fabricius) in pitfall traps set at approximate 15 m height attached to a rope. These authors consider that the lower abundance of arboreal primates in this region explains the low abundance of arboreal dung beetles. However, the abundance and diversity of arboreal dung beetles are higher in dry forests because the rainy season is very short and, as a consequence, dung is available in the canopy for longer periods than in the wet forest (Sabu and Nithya, 2016). These authors also proposed that arboreal dung beetles are a more recent group than beetles that forage and reproduce on the ground. Phylogenetic studies are necessary to test this hypothesis.

We have relatively abundant information from the tropical forests of Borneo, which are home to populations of 10 primate species, including colobins, orangutans, gibbons, and two macaque species. Davis et al. (1997) reported having collected 2378 beetles in traps at 5 m and 10 m high. A curious phenomenon has been observed in Borneo, contrasting with observations in other tropical forests: arboreal beetles have not been mostly collected in the primary (undisturbed) forest. Instead, they are collected in high abundances in managed forests or plantations (refer to Davis and Sutton, 1998). According to these authors, the percentage of beetle species caught is distributed as follows: 1.72% in primary forests, 22.32% in managed forests, and 75.96% in forest plantations. According to Davis and Sutton (1998), arboreal beetles are absent on the ground but abundant at 5 m and up to 20 meters high, with some individuals being spotted at 25 m high. This unusual importance of managed forests and plantations was again mentioned by Davis et al. (2000) for Sabah-Borneo. The beetles considered “forest specialists” are primarily found in plantations. In fact, 14 of the 40 species of dung beetles found in plantations are endemic to Borneo.

The importance of the edge of tropical forests in Borneo is the opposite of their role in other tropical forests. Borneo is relatively well studied, and the beetles that dominate in its forests and plantations are taxonomically different from those in other areas. In Borneo, Deltochilini species are not rollers; instead, dung beetle assemblages are dominated by groups that are typically diggers. Davis et al. (2000) highlighted this remarkable shift in behavior.

Davis (1993) pointed out that the use of dung excreted by monkeys (or other arboreal mammals) and carrion by the Scarabaeinae is possible when these food types are available in the canopy in sufficient amounts and with continued supply. This, along with the existence of tall trees, favors the presence of arboreal dung beetles. Given the competitive nature between species that is common in tropical forests, the existence of arboreal beetles highlights the competition for one of their main resources: monkey feces. Borneo is characterized by the diversity of the resources exploited by beetles (Abdul Rahman et al., 2021). The genus Onthophagus, which comprises most beetle species (632) in Sabah Malasyan, Borneo, includes six fruit-eating species, among them one that consumes fruits while these still are hanging from tree branches (the other fruit-eating beetles consume fruits that have fallen to the ground) (Davis and Sutton, 1997). Perching, which occurs in many species, is a food-searching strategy and a thermoregulation mechanism (Davis, 1993). Onthophagus displays the same type of association described by Walter in Africa. When Andrew J. David worked on the subject from 1990 to 1993, he shared with one of us (Halffter) original information (notes and drawings) on the Scarabaeinae inhabiting trees in Borneo from a collecting campaign in Sabah (Borneo, Malay) in 1990. He found three arboreal Onthophagus species associated with primates. Onthophagus nanus was described as the most abundant arboreal beetle species, and it was observed rolling — a truly exceptional behavior for a burrower like Onthophagus. A pair of beetles roll a “ball” (a piece of dung) in the way typically reported for many rollers, such as Canthon species: the male pushes the “ball” forward with his hind legs while the female remains on top of it, serving as a counterweight and favoring the rolling of the food ball.

Two articles Tregidgo et al. (2010), from Malaysia, and Rahman et al. (2021), from Singapore), confirm several of the findings just mentioned: the importance of Onthophagus and Caccobius as arboreal beetles (especially in secondary forests). Both species show the morphological adaptations mentioned above: very long metatarsals, spurs on the metatarsals, and tarsi of the hind legs adapted to hold the foliage better. Among Onthophagus, O. deliencis is particularly abundant, making and rolling dung balls in the forest canopy.

Several species of Macropocopris Arrow (an Onthophagini genus from Australia) have modified tarsal nails that allow them to attach to hair, especially in the anal region (cited by Halffter and Matthews, 1966: 43-44; Hanski and Cambefort, 1991). When a feces pellet is defecated, the beetle falls with it to the ground, where it is used to build the nest.