Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Necropsies disclose a low helminth parasite diversity in periurban howler monkeys.

Primate-parasite interactions are often investigated via coprological studies given ethical and conservation restrictions of collecting primate hosts. Yet, these studies are inadequate to recover adult helminths for taxonomic identification and to accurately assess their prevalence, intensity, abundance, and site of infection. Fresh carcasses found in anthropogenic landscapes come as informative and reliable alternatives. In this study, we identified the helminths of brown howler monkeys (Alouatta guariba clamitans) and their sites of infection, and measured their prevalence, intensity, and abundance of infection. We necropsied 18 adult males, 11 adult females, and 7 juvenile males that died in conflicts with the anthropogenic environment (domestic dog attacks, n = 11; electrocutions and road-kills, n = 10 each; unknown, n = 5) in periurban landscapes of southern Brazil between 2013 and 2019. We found three nematodes (Trypanoxyuris minutus, Dipetalonema gracile, and Parabronema bonnei) and one cestode (Bertiella cf. studeri), a diversity estimated to account for a sampling completeness of 99%. Prevalence ranged from 3% for P. bonnei to 100% for T. minutus. Mean abundance ranged from 2 (D. gracile and B. cf. studeri) to 55,116 (T. minutus) and mean intensity of infection ranged from 4 (B. cf. studeri) to 55,116 (T. minutus). Trypanoxyuris minutus sex ratio was strongly male-biased. The intensity of infection with T. minutus was higher in juvenile males and adult females than in adult males. The low parasite diversity and the helminths' mode of transmission are compatible with howlers' arboreality and folivorous-frugivorous diet. The howlers were not infected with soil-transmitted helminth parasites of humans and domestic animals on the ground and probably did not eat invertebrates to complement the diet. Given the lack of evidence of howler health problems, we suggest that the causes of death of the necropsied howlers are the major threats to the long-term conservation of the species at the study periurban landscapes.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Flower consumption, ambient temperature and rainfall modulate drinking behavior in a folivorous-frugivorous arboreal mammal.

Water is vital for the survival of any species because of its key role in most physiological processes. However, little is known about the non-food-related water sources exploited by arboreal mammals, the seasonality of their drinking behavior and its potential drivers, including diet composition, temperature, and rainfall. We investigated this subject in 14 wild groups of brown howler monkeys (Alouatta guariba clamitans) inhabiting small, medium, and large Atlantic Forest fragments in southern Brazil. We found a wide variation in the mean rate of drinking among groups (range = 0-16 records/day). Streams (44% of 1,258 records) and treeholes (26%) were the major types of water sources, followed by bromeliads in the canopy (16%), pools (11%), and rivers (3%). The type of source influenced whether howlers used a hand to access the water or not. Drinking tended to be evenly distributed throughout the year, except for a slightly lower number of records in the spring than in the other seasons, but it was unevenly distributed during the day. It increased in the afternoon in all groups, particularly during temperature peaks around 15:00 and 17:00. We found via generalized linear mixed modelling that the daily frequency of drinking was mainly influenced negatively by flower consumption and positively by weekly rainfall and ambient temperature, whereas fragment size and the consumption of fruit and leaves played negligible roles. Overall, we confirm the importance of preformed water in flowers to satisfy the howler's water needs, whereas the influence of the climatic variables is compatible with the 'thermoregulation/dehydration-avoiding hypothesis'. In sum, we found that irrespective of habitat characteristics, brown howlers seem to seek a positive water balance by complementing the water present in the diet with drinking water, even when it is associated with a high predation risk in terrestrial sources.

Successful adoption of an orphan infant in a wild group of brown howler monkeys.

The rarity of infant adoption in wild primates compromises our understanding of its consequences for the participating individuals. We report the first case of successful infant adoption in a wild group of brown howler monkeys (Alouatta guariba clamitans). We evaluated the potential costs of the behavior for the adoptive mother by comparing her activity budget and diet before and after the adoption. On 18 June 2013, a domestic dog killed the mother of a 2-month-old male infant (Victorio) as she attempted to cross a canopy gap. Victorio was immediately rescued from her belly by a researcher and released in a climber near another infant-carrying female (Sofia, his likely grandmother). Sofia recovered him 2 min later. She carried and breastfed both infants during the next 4 weeks, when her own infant disappeared. We monitored Victorio until he reached adulthood in March 2018. Sofia fed more (mainly on immature leaves) when she nursed only Victorio than when nursing only her own or both infants. Assuming that the disappearance of Sofia's own infant was unrelated to the adoption of Victorio, we conclude that his successful adoption may contribute to Sofia's inclusive fitness if he sires his own infants.

Howler monkey tolerance to habitat shrinking: Lifetime warranty or death sentence?

Habitat loss and fragmentation are major threats to the conservation of nonhuman primates. Given that species differ in their responses to fragmented landscapes, identifying the factors that enable them to cope with altered environments or that cause their extirpation is critical to design conservation management strategies. Howler monkeys (Alouatta spp.) are good models for studying the strategies of tolerant arboreal taxa and how they cope with spatial restriction, because they live in habitats ranging from vast pristine forests to small disturbed fragments and orchards. While some aspects of their ecology and behavior are conserved, others vary in predictable ways in response to habitat shrinking and decreasing resource availability. We argue that the ability of individual howler monkeys to inhabit low-quality environments does not guarantee the long-term persistence of the small populations that live under these conditions. Their local extirpation explains why few forest fragments below a given area threshold are frequently inhabited in landscapes where recolonization and gene flow are compromised by long isolation distances or less permeable matrices. In sum, howlers' ability to cope with habitat restriction at the individual level in the short-term may mask the inevitable fate of isolated populations, thereby compromising the persistence of the species at a regional scale in the long-term if howlers' need for protection in large forests is undervalued.

Assessing the influence of biotic, abiotic, and social factors on the physiological stress of a large Neotropical primate in Atlantic forest fragments.

Wildlife physiological responses to environmental and human-related stressors provide useful clues on animal welfare. Non-invasive biomarkers, such as fecal glucocorticoid metabolites (fGCM), allow researchers to assess whether variations in habitat quality, behavior, and climate influence the animals' physiological stress. We examined the role of fragment size, ambient temperature, ripe fruit availability and consumption, percentage of records moving, sex, female reproductive state, and group composition as predictors of the level of fGCM in adult brown howler monkeys (Alouatta guariba clamitans) inhabiting three small (<10 ha) and three large (>90 ha) Atlantic Forest fragments in southern Brazil. We collected bimonthly behavioral data and fecal samples from adult individuals over three years, and used a multimodel inference framework to identify the main predictors of fGCM. We found that the mean (±SD) fGCM in the study groups ranged from 57 ±â€¯49 ng/g to 93 ±â€¯58 ng/g, which were within the known range for howler monkeys. We found 10 best models including five of the 17 tested variables. Sex and reproductive state were the only variables included in all these models. We found that fGCM was higher in nursing females (mean ±â€¯SD = 104 ±â€¯73 ng/g) than in non-nursing females (64 ±â€¯55 ng/g) and males (53 ±â€¯40 ng/g, P < 0.05) and that it decreased with increasing ripe fruit consumption and minimum temperature. However, fragment size did not predict fGCM concentration (groups in small fragments = 71 ±â€¯58 ng/g vs. groups in large fragments = 63 ±â€¯54 ng/g, P > 0.05). We conclude that factors related to the energetic balance of individuals play major roles in modulating the physiological stress of brown howler monkeys. Future studies should investigate the consequences of higher levels of stress hormones on howler monkey health and demography.

Surviving in the urban-rural interface: Feeding and ranging behavior of brown howlers (Alouatta guariba clamitans) in an urban fragment in southern Brazil.

Wild primates that live in urban areas face extreme threats that are less frequent in nonurban fragments, such as the presence of dangerous matrix elements (e.g., roads, power lines, buildings, and a high density of domestic dogs near food patches), that could influence their movements, feeding behavior, and survival. However, the scarcity of studies addressing this issue hinders our understanding of the behavioral adjustments that favor the survival of primates in urban areas. For 12 months, we studied a six-individual group of brown howlers (Alouatta guariba clamitans) in an urban fragment to determine (i) their diet richness and its relationships with food availability, (ii) their daily path length (DPL) and the matrix elements used during movement, and (iii) the main ecological drivers of the DPL. Sampling effort totaled 72 days, 787 hr, and 3,224 instantaneous scans. We found that the diet of brown howlers contained 35 plant species (including seven cultivated crops) belonging to 33 genera and 21 families. The consumption of fruits and young leaves was directly related to their temporal availability. The average DPL (446 m) was smaller than that reported for groups of howlers inhabiting large nonurban fragments. To move between food patches, animals used three main matrix elements: trees, power lines, and roofs. The number of plant species used during the day was the main driver of DPL. Our findings highlighted that the generalist-opportunistic diet of brown howlers and their ability to move across the anthropogenic matrix using artificial elements such as power lines, roofs, and wildlife crossings represent a remarkable part of their behavioral repertory in Lami. However, there are potential costs associated with these strategies, namely, electrocution and predation by domestic dogs. Thus, it is urgent to further investigate how these behaviors could affect the long-term survival of these animals.

Quantity and quality of seed dispersal by a large arboreal frugivore in small and large Atlantic forest fragments.

Seed dispersal is a key process driving the structure, composition, and regeneration of tropical forests. Larger frugivores play a crucial role in community structuring by dispersing large seeds not dispersed by smaller frugivores. We assessed the hypothesis that brown howler monkeys (Alouatta guariba clamitans) provide seed dispersal services for a wide assemblage of plant species in both small and large Atlantic forest fragments. Although fruit availability often decreases in small fragments compared with large ones, we predicted that brown howlers are efficient seed dispersers in quantitative and qualitative terms in both forest types given their high dietary flexibility. After a 36-month study period and 2,962 sampling hours, we found that howlers swallowed and defecated intact the vast majority of seeds (96%-100%) they handled in all study sites. Overall, they defecated ca. 315,600 seeds belonging to 98 species distributed in eight growth forms. We estimated that each individual howler dispersed an average of 143 (SD = 49) seeds >2 mm per day or 52,052 (SD = 17,782) seeds per year. They dispersed seeds of 58% to 93% of the local assemblages of fleshy-fruit trees. In most cases, the richness and abundance of seed species dispersed was similar between small and large fragments. However, groups inhabiting small fragments tended to disperse a higher diversity of seeds from rarely consumed fruits than those living in large fragments. We conclude that brown howlers are legitimate seed dispersers for most fleshy-fruit species of the angiosperm assemblages of their habitats, and that they might favor the regeneration of Atlantic forest fragments with the plentiful amount of intact seeds that they disperse each year.

Fruit availability drives the distribution of a folivorous-frugivorous primate within a large forest remnant.

Understanding the ecological factors that influence the presence, abundance, and distribution of species within their habitats is critical for ensuring their long-term conservation. In the case of primary consumers, such as most primates, the availability and richness of plant foods are considered key drivers of population density at these variables influence the spatial distribution of social units within a finer, habitat patch level scale. We tested the hypothesis that the spatiotemporal availability and richness of plant foods, drive the spatial distribution of brown howler monkeys (Alouatta guariba clamitans) at a fine spatial scale. We established five line transects (2.6-4.3 km long) to census the population of brown howlers in Morro São Pedro, a 1,200 ha Atlantic forest remnant in southern Brazil, every 2 weeks from January to June 2015. We used data from tree inventories performed in sighting and control plots, and phenological surveys of 17 top food tree species to estimate bi-weekly food availability. We recorded a total of 95 sightings. The number of sightings per sampling period ranged from 2 to 12. The availability of fruit (ripe and unripe) was higher in sighting than in control plots, whereas leaf availability and the richness of food tree species was similar. We conclude that the spatial distribution of fruiting trees and the availability of fruit drive the pattern of habitat use, and spacing of brown howler groups in Morro São Pedro.

Feeding Strategies of Brown Howler Monkeys in Response to Variations in Food Availability.

Primates display varying degrees of behavioral flexibility that allow them to adjust their diet to temporal changes in food availability. This trait might be critical for the survival of folivorous-frugivorous species inhabiting small forest fragments, where the availability of food resources tends to be lower than in large fragments and continuous forests. However, the scarcity of studies addressing this issue hampers our understanding of the adaptive behaviors that favor the survival of these primates in low-quality habitats. We conducted a 36-mo study testing the hypothesis that brown howler monkeys (Alouatta guariba clamitans) are able to adjust their diet in response to local and seasonal changes in resource availability. We compared the diet of six free-ranging groups inhabiting three small (<10 ha) and three large (>90 ha) Atlantic forest fragments in southern Brazil and estimated the temporal availability of their top food species (i.e., those species that together contribute ≥80% of total feeding records). We found that brown howlers exploited similarly rich diets in small (45, 54, and 57 plant species) and large (48, 51, and 56 species) fragments. However, intermonth diet similarity was higher for groups in small fragments, where howlers also fed on plant items from nine alien species. Fruits and leaves were the most consumed plant items in both small (42% and 49% of feeding records, respectively) and large (51% and 41%, respectively) fragments. The consumption of young leaves was higher in small than in large fragments, whereas the consumption of other plant items did not show a pattern related to fragment size. Regarding the contribution of growth forms as food sources, only the exploitation of palms showed a pattern related to fragment size. Palms contributed more to the diet of groups inhabiting large fragments. The availability of seasonal food items-ripe fruits and young leaves-influenced their consumption in both habitat types. Therefore, brown howlers cope with local and seasonal fluctuations in food availability by opportunistically exploiting resources. We believe that this feeding flexibility is a key component of the phenotypic plasticity that enables howlers to thrive in disturbed habitat patches, where periods of scarcity of preferred foods shall be more common.

Parturition and potential infanticide in free-ranging Alouatta guariba clamitans.

Parturition is a key process of mammalian reproduction that is rarely documented in New World monkeys because it often occurs at night. However, diurnal births have been recorded in several species. In howler monkeys (Alouatta spp.) they have often been observed during prolonged resting periods. Similarly, infanticide is a behavior observed quite infrequently. Infanticide in howler monkeys is often inferred from infant deaths or disappearances after group takeovers by nonresident male(s). Here we report the first observation of parturition and birth-related behaviors in the brown howler monkey (Alouatta guariba clamitans) and the likely attack on the infant that caused its death. The mother was a multiparous female that lived in a ca. 3-ha Atlantic forest fragment in southern Brazil with nine group mates. The behavior ("all occurrences") sampling method was used to record birth-related behaviors and social interactions. The parturition occurred during the day of 27 October 2013 during a feeding session. The female showed no sign of contraction or birth delivery posture. Parturition began apparently after matrix rupture and release of the amniotic fluid. Expulsion of the newborn occurred between 1 and 3 min later (the exact moment of delivery was not observed). Then, the female held and licked the newborn and began to ingest the placenta and the umbilical cord. The other group members continued feeding and had no interaction with the parturient during the preparturition and parturition events. The infant died ca. 35 days later as a consequence of injuries to his forehead and face, potentially caused by a conspecific bite. Because the adult and subadult males chased the female in the day that the infant's wounds were detected, we believe that one of them might have been the aggressor. We discuss this putative case of infanticide in light of the potential motivation of each male.

Dietary flexibility of the brown howler monkey throughout its geographic distribution.

Habitat loss and fragmentation constrain the survival of most forest-living mammals, particularly strictly arboreal primates. Because fragment size directly affects food availability, primate survival in small fragments may depend on dietary flexibility. Here, we review the literature on the diet of 29 wild groups of Alouatta guariba clamitans inhabiting forest fragments in Brazil and Argentina. We identify general feeding patterns and analyze the influence of fragment size and latitude on diet composition. Brown howlers presented a diet composed of 402 plant species belonging to 227 genera and 80 families. Rarefaction curves suggest that the richness of top food species is similar among groups living in larger (>100 ha), medium (11-100 ha) or small (1-10 ha) fragments. On average, only 12% of the plant species used as food sources by a given group was also consumed by groups from other sites. The shorter the distance between sites, the higher the diet similarity among groups. Despite their diet flexibility, brown howlers spent >80% of the total feeding records on 6-24 species belonging to genera such as Ficus, Zanthoxylum, and Eugenia. Leaves and fruits were the plant items most consumed (65% and 22% of the total feeding records, respectively). Leaf consumption was not affected by fragment size, but it was inversely related to latitude, which may be linked to an increase in the concentration of secondary metabolites in leaves at higher latitudes. We suggest that the ability of brown howlers to exploit a large number of plant food species, including native and exotic trees, shrubs, vines, and lianas, is an important trait that contributes to their survival in highly fragmented habitats along the Atlantic forest. Similar meta-analyses of data from other howler species are necessary to test whether such dietary flexibility is a genus-wide pattern.

Wood consumption by Geoffroyi's spider monkeys and its role in mineral supplementation.

Wood consumption is a rare behavior in frugivorous primates; however, it can be necessary for nutritional balancing as it may provide macro and/or micronutrients that are scarce in the most frequently eaten items (fruits). We tested this hypothesis in six spider monkey (Ateles geoffroyi) communities inhabiting continuous and fragmented rainforests in Lacandona, Mexico. We investigated the importance of both live and decayed wood in the diet of the monkeys, and assessed if wood consumption is related to the nutritional composition of these items. In general, wood consumption was focused on trees of Licania platypus (Chrysobalanaceae) and Ficus spp. (Moraceae), and was similar in continuous forest and in fragments (mean ± SD; 24±20% vs 18±16% of total feeding time, respectively), but marginally higher in females than in males (16±14% vs 5±4%, respectively). Live and decayed wood were both poorer in lipids, proteins, total nonstructural carbohydrates, and total digestible nutrients compared to mature and immature fruits. Moreover, decayed wood of L. platypus showed consistently higher levels of sodium and calcium compared to fruits. In conclusion, our findings suggest that wood from decaying trees of L. platypus and Ficus spp. and young branch piths of L. platypus represents an important source of sodium and/or calcium in the diet of spider monkeys, particularly in the case of females. The protection of decaying trees within forests and fragments is therefore necessary for the appropriate management and conservation of this endangered primate species.

Influence of climatic variables, forest type, and condition on activity patterns of Geoffroyi's spider monkeys throughout Mesoamerica.

Understanding how species cope with variations in climatic conditions, forest types and habitat amount is a fundamental challenge for ecologists and conservation biologists. We used data from 18 communities of Mesoamerican spider monkeys (Ateles geoffroyi) throughout their range to determine whether their activity patterns are affected by climatic variables (temperature and rainfall), forest types (seasonal and nonseasonal forests), and forest condition (continuous and fragmented). Data were derived from 15 published and unpublished studies carried out in four countries (Mexico, El Salvador, Costa Rica, and Panama), cumulatively representing more than 18 years (221 months, >3,645 hr) of behavioral observations. Overall, A. geoffroyi spent most of their time feeding (38.4 ± 14.0%, mean ± SD) and resting (36.6 ± 12.8%) and less time traveling (19.8 ± 11.3%). Resting and feeding were mainly affected by rainfall: resting time increased with decreasing rainfall, whereas feeding time increased with rainfall. Traveling time was negatively related to both rainfall and maximum temperature. In addition, both resting and traveling time were higher in seasonal forests (tropical dry forest and tropical moist forest) than in nonseasonal forests (tropical wet forest), but feeding time followed the opposite pattern. Furthermore, spider monkeys spent more time feeding and less time resting (i.e., higher feeding effort) in forest fragments than in continuous forest. These findings suggest that global climate changes and habitat deforestation and fragmentation in Mesoamerica will threaten the survival of spider monkeys and reduce the distributional range of the species in the coming decades.

Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions.

Here we review all published articles and book chapters, as well as unpublished theses and data of Ateles geoffroyi diet to (1) summarize the literature; (2) synthesize general feeding patterns; (3) document plant taxonomic similarity in diet across study sites; and (4) suggest directions for future research and conservation priorities. We found 22 samples from five countries: Mexico, Guatemala, El Salvador, Costa Rica and Panama. Tropical wet forest is the most studied habitat (N=13 samples), followed by tropical dry forest (6) and tropical moist forest (3). Most samples have been carried out in large protected forests. In spite of showing an overall high dietetic diversity (364 species, 76 families), A. geoffroyi concentrated the majority of feeding time on a few species in the families Moraceae and Fabaceae. At all study sites fruits were the most common food item in the diet followed by leaves. Furthermore, a greater variety of food items and less fruit were consumed in forest fragments. These findings suggest that fruit shortage in fragments results in primates using foods of presumably lower energetic content such as leaves. Similarity in diet was higher among groups geographically closer to each other than among distant groups, showing that the floristic and phenological characteristics of the forest can influence diet composition. We conclude that several years of data are required to fully describe the dietary list of A. geoffroyi at any one site, as studies of the same group over different years shared as little as 56% of species. As most populations of A. geoffroyi live in highly fragmented landscapes, it is crucial to carry out studies in these areas to evaluate (1) changes in diet and activity patterns that may negatively affect survival; and (2) habitat attributes that may favor their persistence in altered landscapes.

Do seasonal changes in light availability influence the inverse leafing phenology of the neotropical dry forest understory shrub Bonellia nervosa (Theophrastaceae)?

In tropical dry forests most plants are deciduous during the dry season and flush leaves with the onset of the rains. In Costa Rica, the only species displaying the opposite pattern is Bonellia nervosa. To determine if seasonal changes in light availability are associated with the leaf and reproductive phenology of this species, we monitored leaf production, survival, and life span, as well as flower and fruit production from April 2000 to October 2001 in Santa Rosa National Park. Leaf flushing and flower bud production took place shortly after the autumnal equinox when day length starts to decrease. Leaves began expansion at the end of the wet season, and plants reached 70 % of their maximum leaf area at the beginning of the dry season, maintaining their foliage throughout the entire dry period. Leaf shedding occurred gradually during the first three months of the wet season. Leaf flushing and shedding showed high synchrony, with leaf numbers being related to light availability. Maximum leaf production coincided with peaks in radiation during the middle of the dry season. Decreasing day length induces highly synchronous flower bud emergence in dry forest species, but this is the first study indicating induction of leaf flushing by declining day length.

Do seasonal changes in light availability influence the inverse leafing phenology of the neotropical dry forest understory shrub Bonellia nervosa (Theophrastaceae)?

In tropical dry forests most plants are deciduous during the dry season and flush leaves with the onset of the rains. In Costa Rica, the only species displaying the opposite pattern is Bonellia nervosa. To determine if seasonal changes in light availability are associated with the leaf and reproductive phenology of this species, we monitored leaf production, survival, and life span, as well as flower and fruit production from April 2000 to October 2001 in Santa Rosa National Park. Leaf flushing and flower bud production took place shortly after the autumnal equinox when day length starts to decrease. Leaves began expansion at the end of the wet season, and plants reached 70 % of their maximum leaf area at the beginning of the dry season, maintaining their foliage throughout the entire dry period. Leaf shedding occurred gradually during the first three months of the wet season. Leaf flushing and shedding showed high synchrony, with leaf numbers being related to light availability. Maximum leaf production coincided with peaks in radiation during the middle of the dry season. Decreasing day length induces highly synchronous flower bud emergence in dry forest species, but this is the first study indicating induction of leaf flushing by declining day length.

En los bosques tropicales secos la mayoría de las plantas pierden sus hojas durante la estación seca y las producen con el inicio de las lluvias. En Costa Rica la única especie que muestra el patrón fenológico inverso es Bonellia nervosa. Para determinar si los cambios estacionales en la disponibilidad de luz estaban asociados con la fenología foliar y reproductiva en esta especie, monitoreamos la producción y sobrevivencia de hojas, así como la producción de flores y frutos de abril del 2000 a octubre del 2001 en el Parque Nacional Santa Rosa. La producción de hojas y botones florales ocurrió poco después del equinoccio de otoño, cuando el fotoperíodo comenzó a disminuir. Las hojas comenzaron a expandirse a finales de la estación lluviosa, y las plantas alcanzaron 70 % de su área foliar máxima al inicio de la estación seca, manteniendo las hojas durante todo el período seco. La caída de hojas tuvo lugar gradualmente durante los primeros tres meses de la estación lluviosa. La producción y caída de hojas mostró alta sincronía, estando el número de hojas relacionado con la disponibilidad de luz. La producción máxima de hojas coincidió con picos en la radiación a mediados de la estación seca. La disminución del fotoperíodo induce alta sincronía en producción de botones florales en especies del bosque seco, pero este es el primer estudio que reporta la inducción de producción de hojas debido a la disminución en el fotoperíodo.

Is the inverse leafing phenology of the dry forest understory shrub Jacquinia nervosa (Theophrastaceae) a strategy to escape herbivory?

In the dry forest of Santa Rosa National Park, Costa Rica, the understory shrub Jacquinia nervosa presents an inverse pattern of phenology that concentrates vegetative growth and reproduction during the dry season. In this study, we tested the [quot ]escape from herbivory[quot ] hypothesis as a potential explanation for the inverse phenological pattern of J. nervosa. We monitored leaf, flower and fruit production in 36 adult plants from October 2000 to August 2001. Leaves of six randomly selected branches per plant were marked and monitored every two weeks to measure the cumulative loss in leaf area. To analyze pre-dispersal seed predation we collected 15 fruits per plant and counted the total number of healthy and damaged seeds, as well as the number and type of seed predators found within the fruits. Leaf, flower, and fruit production occurred during the first part of the dry season (end of November to February). The cumulative herbivory levels were similar to those observed in other tropical dry forest tree species that concentrate leaf production during the wet season, and were concentrated on young leaves, which lost an average of 36.77 % of their area (SD = 34.35 %, N = 195). Chewing beetles of the genus Epicauta (Meloidae) were the most important herbivores. In mature leaves, most of the damage was caused by the beetle Coptocycla rufonotata (Chrysomelidae). Fruits took 4 months to develop during the dry season (January-March 2001) but continue increasing in size well into the first 3 months of the wet season (May-July). Average seed number per ripe fruit was 9 (SD = 5, N = 500). Seed predation in mature fruits was 42 % (SD = 47 %, N = 122). Most seeds were damaged by moth larvae of the family Tortricidae. Only 3 % of the flowers became fruits. This was influenced by the low level of flower synchrony (0.38+/-0.26, N = 36 plants), but neither leaf synchrony (0.88+/-0.06, N = 36 plants) nor plant size influenced fruit numbers. The significa...

Analizamos la hipótesis de “escape de la herbivoría” como explicación para la fenología foliar inversa del arbusto de sotobosque del bosque seco Jacquinia nervosa, el cual produce sus hojas durante la estación seca y se mantiene sin ellas durante la estación lluviosa. Medimos la producción de hojas, flores y frutos, el daño por herbivoría en hojas y semillas, y la fauna de herbívoros en 36 plantas adultas de octubre del 2000 a agosto del 2001 en Santa Rosa, Costa Rica. La herbivoría foliar acumulada durante la estación seca fue similar a la herbivoría de otras especies que concentran la producción foliar en la estación lluviosa. En las hojas maduras la mayor parte del daño fue causado por el escarabajo Coptocycla rufonotata (Chrysomelidae). La depredación de semillas predispersión fue de 42 % (DE= 47 %, N= 122) y es causada por larvas de polilla de la familia Tortricidae. Los niveles de daño indican que la fenología foliar de J. nervosa no coincide con la hipótesis de “escape”. Considerando la fuerte estacionalidad del bosque seco y el carácter heliófito de J. nervosa, es probable que esta estrategia fenológica evolucionara en respuesta a cambios estacionales en la disponibilidad y calidad de la luz, y duración del fotoperíodo.

Is the inverse leafing phenology of the dry forest understory shrub Jacquinia nervosa (Theophrastaceae) a strategy to escape herbivory?

In the dry forest of Santa Rosa National Park, Costa Rica, the understory shrub Jacquinia nervosa presents an inverse pattern of phenology that concentrates vegetative growth and reproduction during the dry season. In this study, we tested the "escape from herbivory" hypothesis as a potential explanation for the inverse phenological pattern of J. nervosa. We monitored leaf, flower and fruit production in 36 adult plants from October 2000 to August 2001. Leaves of six randomly selected branches per plant were marked and monitored every two weeks to measure the cumulative loss in leaf area. To analyze pre-dispersal seed predation we collected 15 fruits per plant and counted the total number of healthy and damaged seeds, as well as the number and type of seed predators found within the fruits. Leaf, flower, and fruit production occurred during the first part of the dry season (end of November to February). The cumulative herbivory levels were similar to those observed in other tropical dry forest tree species that concentrate leaf production during the wet season, and were concentrated on young leaves, which lost an average of 36.77 % of their area (SD = 34.35 %, N = 195). Chewing beetles of the genus Epicauta (Meloidae) were the most important herbivores. In mature leaves, most of the damage was caused by the beetle Coptocycla rufonotata (Chrysomelidae). Fruits took 4 months to develop during the dry season (January-March 2001) but continue increasing in size well into the first 3 months of the wet season (May-July). Average seed number per ripe fruit was 9 (SD = 5, N = 500). Seed predation in mature fruits was 42 % (SD = 47 %, N = 122). Most seeds were damaged by moth larvae of the family Tortricidae. Only 3 % of the flowers became fruits. This was influenced by the low level of flower synchrony (0.38+/-0.26, N = 36 plants), but neither leaf synchrony (0.88+/-0.06, N = 36 plants) nor plant size influenced fruit numbers. The significant damaged produced by insect herbivores in young leaves, fruits, and seeds, as well as the low reproductive index observed in J. nervosa, shows that the inverse leafing phenology of this species is not consistent with the "escape hypothesis" since J. nervosa was considerably attacked during the dry season. Considering the strong seasonality of the tropical dry forest and the heliophyte character of J. nervosa, it is more likely that this phenological strategy evolved in response to seasonal fluctuations in light availability, light quality, and daylength.