Isochrony and rhythmic interaction in ape duetting.

How did rhythm originate in humans, and other species? One cross-cultural universal, frequently found in human music, is isochrony: when note onsets repeat regularly like the ticking of a clock. Another universal consists in synchrony (e.g. when individuals coordinate their notes so that they are sung at the same time). An approach to biomusicology focuses on similarities and differences across species, trying to build phylogenies of musical traits. Here we test for the presence of, and a link between, isochrony and synchrony in a non-human animal. We focus on the songs of one of the few singing primates, the lar gibbon (Hylobates lar), extracting temporal features from their solo songs and duets. We show that another ape exhibits one rhythmic feature at the core of human musicality: isochrony. We show that an enhanced call rate overall boosts isochrony, suggesting that respiratory physiological constraints play a role in determining the song's rhythmic structure. However, call rate alone cannot explain the flexible isochrony we witness. Isochrony is plastic and modulated depending on the context of emission: gibbons are more isochronous when duetting than singing solo. We present evidence for rhythmic interaction: we find statistical causality between one individual's note onsets and the co-singer's onsets, and a higher than chance degree of synchrony in the duets. Finally, we find a sex-specific trade-off between individual isochrony and synchrony. Gibbon's plasticity for isochrony and rhythmic overlap may suggest a potential shared selective pressure for interactive vocal displays in singing primates. This pressure may have convergently shaped human and gibbon musicality while acting on a common neural primate substrate. Beyond humans, singing primates are promising models to understand how music and, specifically, a sense of rhythm originated in the primate phylogeny.

White-handed gibbons (Hylobates lar) alter ranging patterns in response to habitat type.

Small apes are often characterized as inhabiting small home ranges and being dependent on evergreen forest due to their dietary specialization on ripe fruits. Yet few primate studies, particularly those with gibbons, have considered intraspecific variations in ranging behaviors in response to local ecological conditions. This study examines Endangered white-handed gibbon (Hylobates lar) ranging patterns in a heterogeneous landscape. We conducted 13 months of behavioral observations on four white-handed gibbon groups living in Huai Kha Khaeng Wildlife Sanctuary in western Thailand, and combine these data with group location and transect-based productivity data. We compare home range area, site fidelity, and microhabitat preferences. Home range (HR) area varied considerably among the four groups (17-61 hectares). Site fidelity was higher in one of the groups with more evergreen forest in the HR (0.72 ± 0.1) than one of the groups with very little evergreen forest in the habitat (0.47 ± 0.07). While groups with more evergreen forest in the HR preferred evergreen forest areas, groups with very little evergreen forest within the HR demonstrated less preference for evergreen forest areas. We conclude that gibbons at this site exhibit a considerable degree of behavioral variation in response to local ecological conditions. These findings suggest that while gibbons exhibit significant ecological flexibility, this flexibility may be limited by habitat type and key food resources.

Loss and vulnerability of lowland forests in mainland Southeast Asia.

Despite containing extraordinary levels of biodiversity, lowland (<200 m asl) tropical forests are extremely threatened globally. Southeast Asia is an area of high species richness and endemicity under considerable anthropogenic threat with, unfortunately, scant focus on its lowland forests. We estimated extent of lowland forest loss from 1998 to 2018, including inside protected areas and determined the vulnerability of this remaining forest. Maximum likelihood classification techniques were used to classify Landsat images to estimate lowland forest cover in 1998 and 2018. We used Bayesian belief networks with 20 variables to evaluate vulnerability of the forest that remained in 2018. Analyses were conducted at two spatial scales: landscape patch (analogous to ecoregion) and country level. Over 20 years, >120,000 km2 of forest (50% of forest present in 1998) was lost. Of the 14 lowland forest patches, 6 lost >50% of their area. At the country scale, Cambodia had the greatest deforestation (>47,500 km2 ). In 2018, 18% of the lowlands were forested, and 20% of these forests had some formal protection. Approximately 50% of the lowland forest inside protected areas (c. 11,000 km2 ) was also lost during the study period. Most lowland forest remaining is highly vulnerable; eight landscape patches had >50% categorized as such. Our results add to a growing body of evidence that the presence of protected areas alone will not prevent further deforestation. We suggest that more collaborative conservation strategies with local communities that accommodate conservation concessions specifically for lowland forests are urgently needed to prevent further destruction of these valuable habitats.

Pérdida y Vulnerabilidad de los Bosques de Tierras Bajas en la Parte Continental del Sudeste Asiático Resumen A pesar de que contienen niveles extraordinarios de biodiversidad, los bosques tropicales de tierras bajas (<200 m snm) se encuentran bajo amenazas extremas en todo el mundo. El sudeste de Asia es un área con una riqueza alta de especies y endemismos bajo amenazas antropogénicas considerables, desafortunadamente, con un enfoque exiguo sobre sus bosques de tierras bajas. Estimamos la extensión de la pérdida de bosques de tierras bajas desde 1998 hasta 2018, incluyendo aquellos bosques que se encuentran dentro de áreas protegidas, y determinamos la vulnerabilidad del bosque que permanece. Usamos técnicas de clasificación de la probabilidad máxima para clasificar imágenes Landsat y así estimar la cobertura de bosque de tierras bajas en 1998 y 2018. Usamos redes de opinión bayesiana con 20 variables para evaluar la vulnerabilidad del bosque que permanecía en pie en 2018. Los análisis fueron realizados a dos escalas espaciales: a nivel de fragmento de paisaje (análogo a la ecorregión) y a nivel de país. A lo largo de 20 años, se perdieron >120,000 km2 de bosque (50% del bosque presente en 1998). De los 14 fragmentos de bosque de tierras bajas, seis perdieron >50% de su área. A la escala de país, Camboya tuvo la mayor deforestación (>47,500 km2 ). En 2018, el 18% de las tierras bajas contaban con bosque y el 20% de estos bosques tenían algún tipo de protección formal. Aproximadamente el 50% del bosque de tierras bajas que se encuentra dentro de áreas protegidas (aprox. 11,000 km2 ) también se perdió durante el periodo de estudio. La mayoría del bosque de tierras bajas que todavía permanece tiene una vulnerabilidad muy alta; ocho de los fragmentos de paisaje tenían >50% categorizado de tal manera. Nuestros resultados se suman a un cuerpo creciente de evidencia de que la sola presencia de las áreas protegidas no va a prevenir una mayor deforestación. Sugerimos que se necesitan urgentemente más estrategias de conservación colaborativa con comunidades locales que acomoden las concesiones de conservación específicamente para los bosques de tierras bajas para prevenir una mayor destrucción de estos hábitats tan valiosos.

COVID-19 Highlights the Need for More Effective Wildlife Trade Legislation.

Zoonosis-based epidemics are inevitable unless we revisit our relationship with the natural world, protect habitats, and regulate wildlife trade, including live animals and non-sustenance products. To prevent future zoonoses, governments must establish effective legislation addressing wildlife trade, protection of habitats, and reduction of the wildlife-livestock-human interface.

Northern pigtailed macaques rely on old growth plantations to offset low fruit availability in a degraded forest fragment.

Space-use and foraging strategies are important facets to consider in regard to the ecology and conservation of primates. For this study, we documented movement, ranging, and foraging patterns of northern pigtailed macaques (Macaca leonina) for 14 months in a degraded habitat with old growth Acacia and Eucalyptus plantations at the Sakaerat Biosphere Reserve in northeastern Thailand. We used hidden Markov models and characteristic hull polygons to analyze these patterns in regard to fruit availability. Macaques' home range (HR) was 599 ha and spanned through a natural dry-evergreen forest (DEF), and plantation forest. Our results showed that active foraging increased with higher fruit availability in DEF. Macaques changed to a less continuous behavioral state during periods of lower fruit availability in DEF, repeatedly moving from foraging to transiting behavior, while extending their HR further into plantation forest and surrounding edge areas. Concomitantly, macaques shifted their diet from fleshy to dry fruit such as the introduced Acacia species. Our results showed that the diet and movement ecology adaptations of northern pigtailed macaques were largely dependent on availability of native fruits, and reflected a "high-cost, high-yield" foraging strategy when fresh food was scarce and dry fruit was available in plantation forest. Conversely, wild-feeding northern pigtailed macaque populations inhabiting pristine habitat approached a "low-cost, low-yield" foraging strategy. Our results outline the effects of habitat degradation on foraging strategies and show how a flexible species can cope with its nutritional requirements.

Slow loris density in a fragmented, disturbed dry forest, north-east Thailand.

Primate survival in disturbed forests can be governed by a complex of forest variables. For nocturnal arboreal primates, determining these ecological features is notoriously difficult but is critically important for their conservation. Here we assessed the effects of forest type, food availability, human disturbance, and forest structure on the nocturnal Bengal slow loris (Nycticebus bengalensis) in Sakaerat Biosphere, north-east Thailand, a small disturbed fragment containing dry evergreen, dry dipterocarp, and plantation forests. Distance sampling revealed plantation forest had the highest density estimate (27 loris/km2 ) followed by dry evergreen forest (17 loris/km2 ), while dry dipterocarp forest only had four detections. Based on forest type selection analyses, loris had a positive association with sap and fruit-flower productivity which was highest in plantation forest compared to the natural dry evergreen or dry dipterocarp forests. Furthermore, forest structure selection analysis indicated loris preferred denser canopies. Loris presence was positively associated with canopy height, canopy connections, tree trunk vegetation cover, and canopy density. The higher loris density found in the plantations, as also reported by other studies, was associated with dense vegetation structure and higher food productivity, particularly sap. However, the important structural features found in the plantation forest are strongly dependent on forest maturity, and the reduced longevity of such exotic tree species may limit the conservation importance of plantation forest, merely acting as a short-term alternative to natural habitat.

Foraging strategies underlying bird egg predation by macaques: A study using artificial nests.

Bird egg predation is widespread in non-human primates. Although nest predation is often described as opportunistic, little is known about foraging strategies and nest detection in primates. Since it is the prevalent cause of nest failure in the tropics, birds select nest sites within specific microhabitats and use different nest types to increase nesting success. Identifying the nests targeted by the northern pigtailed macaques (Macaca leonina), an omnivorous cercopithecine species, and known nest predator, will shine light on nest foraging strategies in primates. The aim of this research was to reveal if nest predation is a selective or opportunistic feeding behavior. We studied, using artificial nests and camera traps, the influence of nest type (open-cup vs. cavity), microhabitat (i.e., understory density, canopy cover, canopy height, ground cover, and presence vs. absence of thorns and lianas), and nest height, on nest predation by a troop of northern pigtailed macaques in the Sakaerat Biosphere Reserve (Thailand), a degraded environment. In our study, macaque predation on artificial nests was high; out of the 200 nests that were set up, 112 were plundered by macaques. Although predation rates decreased with nest height, nest type, and microhabitat had no significant effect on predation by macaques. Nest detectability and accessibility did not affect predation rates. Macaques actively searched for nests in different microhabitats, suggesting that nest predation by this primate might be considered a selective feeding behavior in this degraded habitat. Consequently, nest predation by this primate might have important conservation implications on the population dynamics of forest-dwelling bird species. Behavior observation methods, such as instantaneous scan sampling, may underestimate nest predation by primates, a furtive and cryptic behavior.

Ranging and site fidelity in northern pigtailed macaques (Macaca leonina) over different temporal scales.

Space-use patterns are crucial to understanding the ecology, evolution, and conservation of primates, but detailed ranging data are scarce for many species, especially those in Southeast Asia. Researchers studying site fidelity to either home ranges or core areas have focused mainly on territorial species, whereas less information is available for non-territorial species. We analyzed the ranging patterns and site fidelity of one wild troop of northern pigtailed macaques over 16 months at different temporal scales. We used characteristic hull polygons in combination with spatial statistics to estimate home ranges and core areas. The total home range and core areas were 449 ha and 190 ha, respectively. Average daily path length was 2,246 m. The macaques showed a high defendabili--ty index according to the expected ranging of a non-territorial species in which movement does not theoretically permit the defense of a large territory. Overall, the study troop ranged more extensively than conspecific groups and closely related species studied elsewhere. These differences may reflect variable troop size, degree of terrestriality and habitat characteristics, but could also reflect methodological differences. The location, size and shape of home ranges and core areas, and extent of daily path lengths changed on a monthly basis resulting in low site fidelity between months. The macaques also showed clear shifts in the location of daily home ranges with low site fidelity scores between consecutive days. Daily home range and daily path length were related to seasonality, with greater values during the fruit-abundant period. Low site fidelity associated with lack of territoriality is consistent with macaques structuring their movement based on available food sources. However, ranging patterns and site fidelity can also be explained by macaques feeding on the move, a foraging strategy that hinders frequent and long visits to the same location.

Sleeping site selection and presleep behavior in wild pigtailed macaques.

Several factors are likely to control sleeping site selection and presleep behavior in nonhuman primates, including predation risk and location of food resources. We examined the effects of these factors on the sleeping behavior of northern pigtailed macaques (Macaca leonina). While following a troop living in the surroundings of the Visitor Center of Khao Yai National Park (Thailand), we recorded the physical characteristics and location of each sleeping site, tree, the individuals' place in the tree, posture, and behavior. We collected data for 154 nights between April 2009 and November 2010. The monkeys preferred tall sleeping trees (20.9 ± SD 4.9 m) and high sleeping places (15.8 ± SD 4.3 m), which may be an antipredator strategy. The choice of sleeping trees close to the last (146.7 ± SD 167.9 m) or to the first (150.4 ± SD 113.0 m) feeding tree of the day may save energy and decrease predation risk when monkeys are searching for food. Similarly, the choice of sleeping sites close to human settlements eases the access to human food during periods of fruit scarcity. Finally, the temporal pattern of use of sleeping sites, with a preference for four of the sleeping sites but few reuses during consecutive nights, may be a trade-off between the need to have several sleeping sites (decreasing detection by predators and travel costs to feeding sites), and the need to sleep in well-known sites (guaranteeing a faster escape in case of predator attack).

Density and microhabitat use of Bengal slow loris in primary forest and non-native plantation forest.

The extent of planted forests has greatly increased in the tropics, but their conservation value while assumed to be low, is largely unknown. We compared the density and microhabitat selection of a nocturnal arboreal primate, the Bengal slow loris (Nycticebus bengalensis), in mostly undisturbed, evergreen tropical forest to those in 15-18 year old Acacia/Leucaena plantations with significant secondary regrowth, and <15 year old plantations with little regrowth. Based on estimates derived from distance sampling, loris densities in older plantations were nearly identical to primary forest (4.26 vs. 4.00 lorises per square kilometer), although encounter rates were three times higher in the older plantations probably owing to the lower detection probability in the more complex vegetation of the primary forest. The mean density estimate for the younger plantation was one-third of the above habitats (1.27 lorises per square kilometer), although not statistically different. Lorises tended to use larger diameter and taller trees, with a greater crown depth than randomly sampled trees, and tended to avoid habitats with sparsely crowned trees. The older plantations had trees with lower basal area and shorter stems than the primary forest; however, the older plantations contained higher densities of Bauhinia lianas, a commonly eaten food source and did not contain the red giant flying squirrel (Petaurista petaurista), a potential competitor. Although it is unknown whether the Bengal slow loris would persist without the presence of primary forest in the landscape, we suggest that older plantations have conservation value for at least selected species and as such, could be better managed to increase this value.

Selection of sleeping trees in pileated gibbons (Hylobates pileatus).

Selection and use patterns of sleeping sites in nonhuman primates are suggested to have multiple functions, such as predation avoidance, but they might be further affected by range defense as well as foraging constraints or other factors. Here, we investigate sleeping tree selection by the male and female members of one group of pileated gibbons (Hylobates pileatus) at Khao Ang Rue Nai Wildlife Sanctuary, Thailand. Data were collected on 113 nights, between September 2006 and January 2009, yielding data on 201 sleeping tree choices (107 by the female and 94 by the male) and on the characteristics of 71 individual sleeping trees. Each sleeping tree and all trees > or =40 cm diameter at breast height (DBH) in the home range were assessed (height, DBH, canopy structure, liana load) and mapped using a GPS. The gibbons preferentially selected tall (mean=38.5 m), emergent trees without lianas. The majority of the sleeping trees (53.5%) were used only once and consecutive reuse was rare (9.5%). Sleeping trees were closer to the last feeding tree of the evening than to the first feeding tree in the morning, and sleeping trees were located in the overlap areas with neighbors less often than expected based on time spent in these areas. These results suggest avoidance of predators as the main factor influencing sleeping tree selection in pileated gibbons. However, other non-mutually exclusive factors may be involved as well.

Sterile pyuria in a population of wild white-handed gibbons (Hylobates lar).

Urinalysis is an emerging method for monitoring the health and energy balance of wild primates. Here, we report the first urinalysis of wild gibbons. We used multi-reagent test strips to monitor the health status of 52 individual white-handed gibbons (Hylobates lar) inhabiting Khao Yai National Park, Thailand. Most urinary reference values were within normal ranges; however, regardless of age- and sex-class or monthly fruit productivity, we found unexpectedly high rates of urinary leukocytes (50% and 90% of individuals in 2001-2003 and 2006, respectively). In contrast to previous studies of African apes, this finding is coupled with the near absence of urinary nitrites, demonstrating pervasive levels of sterile pyuria. This result is the first reported case of sterile pyuria in a population of wild primates. The etiology of human sterile pyuria is diverse, but in all cases it is diagnostic of systemic inflammation. We discuss the potential causes of sterile pyuria in the gibbons of Khao Yai.

Home-range characteristics and the influence of seasonality on female reproduction in white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand.

A three-year (2001-2003) study was carried out on the home range characteristics of seven wild white-handed gibbon (Hylobates lar) groups focusing on the spatio-temporal distribution of food resources at Khao Yai National Park in northeastern Thailand. These results were combined with 23 years (1980-2003) of reproductive performance data on seven females from the same focal groups. Reproductive performance was equal among females with regard to birth, weaning and maturation ratios, and independent of variation in food availability. Offspring mortality, however, was significantly positively correlated with home-range size. In addition, there was an increase in offspring mortality just after weaning, suggesting that the increase in the daily distance traveled by juveniles contributed to this mortality. Conceptions clustered during the first half of the year when food production was at its peak, which presumably allowed females to accumulate sufficient body reserves to resume ovarian cycling. Our results place Khao Yai gibbons closer to Cercopithecidae than great apes in terms of the temporal pattern of reproductive events, though gestation, lactation, inter-birth interval, and offspring maturation are considerably longer in gibbons, placing them closer to the other apes. Our findings underline the unique phylogenetic position of these small-bodied apes in terms of reproductive patterns in primates.