Ungulate biomass in relation to feeding strategy within Amazonian forests

Summary The relationship between diet and biomass was examined in the Amazonian ungulates (red brocket deer, grey brocket deer, collared peccary, white-lipped peccary, and lowland tapir) of Northeastern Peru. Tropical forest ungulates have lower biomasses than savanna or grassland ungulates, because in tropical forests the majority of primary production occurs in the canopy, well out of reach from terrestrial herbivores. Within the Amazonian ungulates, species that supplement their diet with animal material, namely the peccaries, obtain a greater crude and metabolic biomass, and higher reproductive rates than the purely herbivorous species. Omnivory appears to help terrestrial herbivores inhabiting closed canopy forests overcome some effects of food limitation.     

Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest

In Neotropical forests, mammals act as seed dispersers and predators. To prevent seed predation and promote dispersal, seeds exhibit physical or chemical defenses. Collared peccaries (Pecari tajacu) cannot eat some hard seeds, but can digest chemically defended seeds. Central American agoutis (Dasyprocta punctata) gnaw through hard‐walled seeds, but cannot consume chemically defended seeds. The objectives of this study were to determine relative peccary and agouti abundances within a lowland forest in Costa Rica and to assess how these two mammals affect the survival of large seeds that have no defenses (Iriartea deltoidea, Socratea exorrhiza), physical defenses (Astrocaryum alatum, Dipteryx panamensis), or chemical defenses (Mucuna holtonii) against seed predators. Mammal abundances were determined over 3 yrs from open‐access motion‐detecting camera trap photos. Using semi‐permeable mammal exclosures and thread‐marked seeds, predation and dispersal by mammals for each seed species were quantified. Abundances of peccaries were up to six times higher than those of agoutis over 3 yrs, but neither peccary nor agouti abundances differed across years. Seeds of A. alatum were predominantly dispersed by peccaries, which did not eat A. alatum seeds, whereas non‐defended and chemically defended seeds suffered high levels of predation, mostly by peccaries. Agoutis did not eat M. holtonii seeds. Peccaries and agoutis did not differ in the distances they dispersed seeds. This study shows that seed fates are contingent upon many factors such as seed defenses, frugivore–granivore abundances, and seed‐handling capabilities. Mammal–seed interactions are complex; the outcomes of these interactions depend on the inherent characteristics of seeds and their potential dispersers.     

Mosaic evolution of ruminant stomach lysozyme genes

The genomes of ruminant artiodactyls, such as cow and sheep, have approximately 10 lysozyme genes, 4 of which are expressed in the stomach. Most of the duplications of the lysozyme genes occurred 40-50 million years ago, before the divergence of cow and sheep. Despite this, the coding regions of stomach lysozyme genes within a species (e.g., cow, sheep, or deer) are more similar to each other than to lysozyme genes in other ruminants. This observation suggests that the coding regions of the stomach lysozyme genes have evolved in a concerted fashion. Our previous characterization of 3 cow stomach lysozyme genes suggested that it was only the coding exons that had participated in concerted evolution. To determine whether the introns and flanking regions of ruminant stomach lysozyme genes are evolving in a concerted or a divergent fashion, we have isolated and characterized 2 sheep stomach lysozyme genes. Comparison of the sequences of the sheep and cow stomach lysozyme genes clearly shows that the introns and flanking regions have evolved, like the 3' untranslated region of the mRNAs, in a divergent manner. Thus, if the four coding exons are evolving by concerted evolution, then a mosaic pattern of concerted and divergent evolution is occurring in these genes. The independent concerted evolution of coding exons of the ruminant stomach lysozyme gene may have assisted in the accelerated adaptive evolution of the lysozyme to new function in the early ruminant.     

Concerted evolution of ruminant stomach lysozymes. Characterization of lysozyme cDNA clones from sheep and deer

Contradictory evolutionary histories of ruminant lysozymes have been predicted by analysis of genomic blots (Irwin, D.M., Sidow, A., White, R., and Wilson, A.C. (1989) in The Immune Response to Structurally Defined Proteins: The Lysozyme Model (Smith-Gill, S.J., and Sercarz, E.E., eds) pp. 73-85, Adenine Press, Guilderland, NY) and sequences of cow stomach lysozyme cDNAs (Irwin, D.M., and Wilson, A.C. (1989) J. Biol. Chem. 264, 11387-11393). Genomic blots indicate that the amplification of the lysozyme gene family occurred 40-50 million years ago, while the cDNA sequences imply that the stomach genes began diverging from one another after the splitting of the deer and cow lineages, 25 million years ago. To resolve this contradiction, we characterized 111 stomach lysozyme cDNAs from two additional ruminant species: domestic sheep and axis deer. The cDNA sequences of the coding region of mature lysozyme together with the 3'-untranslated region were obtained from abomasum (true stomach) mRNA with the use of the polymerase chain reaction. The two primers for amplifying the cDNA were a lysozyme-specific primer, encoding a conserved sequence at the amino terminus of mature stomach lysozyme, and oligo(dT) as a general mRNA primer. Comparison of the cDNA sequences from these species to one another and to those of the cow revealed that different parts of the ruminant stomach lysozyme genes have had different evolutionary histories. The 3'-untranslated region has evolved in a divergent fashion since the original duplications 40-50 million years ago, supporting the genomic blot interpretation; by contrast, the coding region has evolved in a concerted fashion, that is, the multiple sequences within a species have evolved in unison. The 3'-untranslated portion of the lysozyme genes appears to have escaped from concerted evolution due to inability to initiate concerted evolution, rather than due to reduced sequence similarity. The process of concerted evolution in stomach lysozymes may have had roles both in adapting lysozyme to the stomach environment in early ruminants as well as in retarding amino acid sequence evolution in the well adapted lysozyme of modern ruminants.     

Interspecific association between an ungulate and a carnivore or a primate

In the Brazilian Pantanal, we observed collared peccaries (Pecari tajacu) associating with South American coatis (Nasua nasua) 13 times and three times with black howler monkeys (Alouatta caraya). The scansorial coati drop fruit whilst feeding that both collared peccaries and other coatis consume. Young coatis were also observed chewing on the pulp left over from seeds spat out by collared peccaries who had removed the hard exocarp. Both species react to each other’s alarm calls. Peccaries also benefited from the fruits dropped by black howler monkeys. Ecologically, coatis are omnivores; but taxonomically, they are carnivores. To our knowledge, the collared peccary/coati association is the first report of an interspecific association between an ungulate and a carnivore.     

Reproductive biology of female Amazonian brocket deer in northeastern Peru

The aim of this study was to provide information on the reproductive biology of brocket deer. Hence, we analyzed female reproductive tracts collected by rural hunters from 1991 to 1998 in the Tamshiyacu-Tahuayo Communal Reserve, northeastern Peruvian Amazon. We characterized the basic reproductive biology of brocket deer, analyzed whether the distributions of conceptions and births are aseasonal, and compared their reproductive productivity in two different areas subject to heavy and slight hunting pressures, respectively. We found that: (1) red and gray brocket deer did not differ in ovulation, fertilization, and pregnancy rates; (2) average number of fetuses per birth was 1.2 for red brocket deer and one for gray brocket deer; (3) sex of fetuses suggests a male biased sex ratio for both species; (4) neither species shows reproductive seasonality; and (5) gross productivity does not differ between heavily and slightly hunted areas. Our results indicate that brocket deer exhibit reproductive characteristics similar to their conspecifics in other parts of their native distribution range.     

Diet of peccaries (Tayassu tajacu and T. pecari) in a dry forest of Venezuela

The diets of Tayassu tajacu and T. pecari were assessed by means of direct observations, stomach content, and faecal analyses. The study was conducted in a dry forest located in the central Llanos region, Venezuela, where both species coexist. Peccaries were observed during one week of every month from August 1986 to May 1987. Fruits and seeds of Pithecellobium saman and Guazuma ulmifolia and roots and stems of Cissus rhombifolia comprised most of the diet of both peccary species. Proportions of these items differed significantly between species. There was no Acacia macracantha in stomachs nor in faeces of T. tajacu , but it was one of the most important items found in stomachs of T. pecari. Leaves appeared in all stomachs but in very low proportions (<1%). Insect pupae and larvae were found in small quantities. Results suggest that peccaries behave as frugivores and seed predators as most seed remains appeared cracked. Differences in the diet and behavioural traits described elsewhere may allow these similar species to coexist in the tropical dry forest of central Venezuela.     

Can remnant frugivore species effectively disperse tree seeds in secondary tropical rain forests?

Seed dispersal by frugivores in tropical rain forests is important for maintaining viable tree populations. Over the years, vertebrate assemblages in tropical forests have been altered by anthropogenic disturbances, leading to concerns about the ability of remnant vertebrates to substitute for the lost or declining vertebrate populations. We compared vertebrate composition and frugivore visitation rates as an indirect measure of rate of seed dispersal in three tropical rain forests in Uganda, namely Mabira, Budongo and Kibale Forests. Mabira is highly disturbed, Kibale is little and Budongo is intermediate. The aim was to determine whether vertebrate assemblages in differentially disturbed forests had comparable abilities to disperse seeds and whether tree species were equally vulnerable to loss of seed dispersers. Assemblages of forest generalist species were similar in all forests, but specialists were less abundant in the heavily disturbed forest. Remnant frugivores in the heavily disturbed forest were mainly small-bodied species that spat seeds beneath fruiting trees compared to large-bodied species observed in the less disturbed forests that ingested and carried away the seeds. We postulate that the quantity of seeds dispersed in heavily disturbed forests is much reduced due to low visitation rates of frugivores and the absence of large frugivores that consume large quantities of fruit. The quality of seed dispersal is affected as well by the distance over which seeds are moved. Assessment of vulnerability of trees shows no evidence for disperser substitution for trees producing large fruits. Fruit trees with low nutritional contents and digestibility were least visited in frugivore-impoverished forests. The loss of large specialist frugivores is likely to affect recruitment of many trees, especially of species that cannot establish beneath adult conspecifics.     

Effects of seed size and frugivory degree on dispersal by Neotropical frugivores

Large vertebrates are important elements of mutualistic interactions and provide positive impacts on plant population and community dynamics. Despite the increasing interest on vertebrate frugivory we are still not able to disentangle the real contribution of seed dispersal to Neotropical forest functioning. Consuming fruits does not imply effective seed dispersal and many variables, such as seed size and animal diet, may influence the outcome of plant-animal interactions. Here, we performed a comprehensive literature search on seed dispersal by Neotropical vertebrates (with a focus on primates) to closely approach their role as seed dispersers, hypothesizing frugivory degree and seed size as main drivers of fruit handling behavior and diversity of dispersed seeds. We found that the great majority of seeds manipulated by Neotropical primates, with exception to the seed predators pitheciins, were swallowed and passed intact through their gut. Larger seeds (>12 mm) tended of being ingested exclusively by primates and other large vertebrates, such as tapirs and peccaries. Furthermore, primate feeding guild had a great influence on the richness and sizes of seeds dispersed, as primarily frugivores dispersed more species and had higher probabilities of ingesting larger seeds when compared to other feeding guilds. Organizing available knowledge and filling the main knowledge gaps allowed us to validate common sense assumptions and ultimately draw new conclusions about the role played by primates together with other major frugivores in Neotropical forests.     

Who really ate the fruit? A novel approach to camera trapping for quantifying frugivory by ruminants

Tropical forest ruminants disperse several plants; yet, their effectiveness as seed dispersers is not systematically quantified. Information on frequency and extent of frugivory by ruminants is lacking. Techniques such as tree watches or fruit traps adapted from avian frugivore studies are not suitable to study terrestrial frugivores, and conventional camera traps provide little quantitative information. We used a novel time-delay camera-trap technique to assess the effectiveness of ruminants as seed dispersers for Phyllanthus emblica at Mudumalai, southern India. After being triggered by animal movement, cameras were programmed to take pictures every 2 min for the next 6 min, yielding a sequence of four pictures. Actual frugivores were differentiated from mere visitors, who did not consume fruit, by comparing the number of fruit remaining across the time-delay photograph sequence. During a 2-year study using this technique, we found that six terrestrial mammals consumed fallen P. emblica fruit. Additionally, seven mammals and one bird species visited fruiting trees but did not consume fallen fruit. Two ruminants, the Indian chevrotain Moschiola indica and chital Axis axis, were P. emblica’s most frequent frugivores and they accounted for over 95% of fruit removal, while murid rodents accounted for less than 1%. Plants like P. emblica that are dispersed mainly by large mammalian frugivores are likely to have limited ability to migrate across fragmented landscapes in response to rapidly changing climates. We hope that more quantitative information on ruminant frugivory will become available with a wider application of our time-delay camera-trap technique.     

Tooth chipping can reveal the diet and bite forces of fossil hominins

Mammalian tooth enamel is often chipped, providing clear evidence for localized contacts with large hard food objects. Here, we apply a simple fracture equation to estimate peak bite forces directly from chip size. Many fossil hominins exhibit antemortem chips on their posterior teeth, indicating their use of high bite forces. The inference that these species must have consumed large hard foods such as seeds is supported by the occurrence of similar chips among known modern-day seed predators such as orangutans and peccaries. The existence of tooth chip signatures also provides a way of identifying the consumption of rarely eaten foods that dental microwear and isotopic analysis are unlikely to detect.     

Pulp–seed attachment is a dominant variable explaining legitimate seed dispersal: a case study on woolly monkeys

Seed dispersal is a mutualistic interaction in which frugivores gain nutrients and plants gain when seeds are transported to adequate places for establishment. However, this relationship is prone to deceit, for example, when frugivores spit-out seeds in the proximity of parental trees. Still, few hypotheses have offered explanations on why deceiving strategies are not widespread. In this study, I explore the importance of how difficult it is to mechanically separate the nutritious pulp from the seeds, as a factor that can explain the chance a seed has of being dispersed by woolly monkeys (Lagothrix lagothricha). I completed 1,440 h of focal animal follows during 2 years in order to quantify the chances plant species have of being dispersed. To do so, I evaluated the residuals from the relationship between the number of seeds manipulated and seeds dispersed by a population of woolly monkeys in Tinigua Park (Colombia). For 74 fruit species, I estimated how difficult it is to separate pulp from seeds as the time needed to separate the parts. An exponential model showed that this variable was able to predict 38% of the variation on dispersal probability, demonstrating that, when it is difficult to separate the pulp from the seeds, the probability of legitimate dispersal increases. However, when fruit parts were easy to separate, there was more variation in the outcome. My results suggest that many plants have evolved mechanisms (e.g., small seeds embedded in pulp, strong attachment, irregular seed surface, and thin pulp layer) that preclude deceit by frugivores.     

Adaptive foraging tactics of greater short-nosed fruit bats on a spiny shrub and its effect on seed dispersal

Journal of Ethology - Many plant species have seeds embedded in their fleshy pulp to attract frugivores, which enhances the chance of seed dispersal. However, some tropical plants are evolved with...     

Correlated evolution of diaspore traits and potential frugivore-mediated selection in a fleshy-fruited tropical lineage (Artabotrys,Annonaceae)

Dispersal syndromes are often defined by reference to fruit traits that are associated with distinct frugivore guilds. Studies rarely examine the relationship between seed traits and frugivores or test the alternative hypothesis that traits are shaped by climatic variables. We assess whether the evolution of seed size and physical defense are correlated with dispersal-related traits and climatic variables in Artabotrys, a fleshy-fruited tropical lineage. Diaspore traits and WorldClim bioclimatic variables were compiled for 43 species. Correlated evolution was evaluated using phylogenetic regression and model-fitting approaches. The best-fitting multioptima Ornstein-Uhlenbeck model suggests that lineages with smooth testa and thin pericarp (SP) have evolved toward smaller seeds with a thinner testa, whereas lineages with rough testa and/or thick pericarp have evolved toward larger seeds with a thicker testa. A smooth testa facilitates spitting and/or swallowing of intact seeds while fruits with thin pericarp may be preferentially consumed by frugivores with less destructive oral processing, enabling lower investment in seed physical defense in SP lineages. Moreover, small seeds are more likely to be swallowed intact with a food bolus. The effect of climate on seed size and physical defense is equivocal and warrants further investigation.     

Function,size and form of the gastrointestinal tract of the collared <Emphasis Type="Italic">Pecari tajacu</Emphasis> (Linnaeus 1758) and white-lipped peccary <Emphasis Type="Italic">Tayassu pecari</Emphasis> (Link 1795)

The peccary digestive tract is characterised by an elaborate forestomach. In order to further characterise the digestive function of peccaries, we report body mass, digestive organ mass, content mass of the gastrointestinal tract compartments and their length and width, as well as liver, parotis and mandibular gland mass. Our data on eleven collared and four white-lipped peccaries suggest that peccaries have a small relative stomach volume compared to other foregut fermenters, which implies a comparatively lower fermentative capacity and thus forage digestibility. The forestomach could enable peccaries to deal, in conjunction with their large parotis glands, with certain plant toxins (e.g. oxalic acid). The finding of sand being trapped in the forestomach blindsacs could indicate a disadvantage of the peccary forestomach design. The relevance of the forestomach to peccaries remains enigmatic.     

Forest disturbance and seasonal food availability influence a conditional seed dispersal mutualism

The interaction between granivorous scatterhoarding mammals and plants is a conditional mutualism: scatterhoarders consume seeds (acting as predators), but the movement of seed by scatterhoarders may contribute to dispersal (acting as mutualists). Understanding the ecological factors that shape this relationship is highly relevant in anthropogenically disturbed tropical forests where large‐bodied frugivores are extirpated. In such forests, large‐seeded trees that once depended on these frugivores for dispersal may now only have scatterhoarders as prospective dispersers. We studied Carapa oreophila (Meliaceae) in an Afromontane forest, to test the hypotheses that the proportion of seeds immediately consumed or hoarded (dispersed) would vary over a disturbance gradient. Temporal replication also afforded exploration of how habitat effects might vary with food availability. Using a Bayesian framework, we demonstrate that seeds were more likely to be hoarded in less disturbed forest, irrespective of temporal variation in food abundance. In contrast, forest disturbance only appeared to increase seed predation in temporal replicates that coincided with sustained food availability. These results highlight the potential variability in the dynamics between plants and scatterhoarders over fine temporal scales, elucidating possible ecological scenarios where scatterhoarders might act as mutualists (contributing positively to plant recruitment). Our study also fills important knowledge gaps about the importance of scatterhoarders as dispersers in tropical forests depleted of large‐bodied frugivores, particularly in Africa where scatterhoarding mutualisms have not been extensively studied.     

Differential Responses to Hunting in Two Sympatric Species of Brocket Deer (Mazama americana and M. nana)

Hunting by humans may affect the abundance and activity patterns of game species. We examined the effect of hunting on the abundance and activity patterns of sympatric red brocket deer Mazama americana and dwarf brocket deer M. nana . We conducted four camera-trap surveys (158 sampling stations, 10,244 trap-days, total area sampled 1200 km²) in three areas within the Atlantic Forest of Misiones, Argentina, that differ in protection and hunting pressure. We used logistic regression and tests of independence to evaluate if protection, hunting pressure, and other independent variables affect the probability of recording each species and their recording rate. We used the Mardia–Watson–Wheeler test to examine if the daily activity pattern differs between species and changes with hunting pressure. Red brocket deer were more frequently recorded (397 records, 58% of stations) than dwarf brocket deer (100 records, 37% of stations). The probability of recording red brockets was higher in areas with better protection and increased with the distance to the main accesses used by poachers. The probability of recording dwarf brockets was higher in areas with low protection. Red brockets were more nocturnal than dwarf brockets, a difference that may reduce interspecific competition. However, red brockets were more diurnal in the best-protected areas, suggesting that they can adjust their activity to local hunting pressure. Hunting has opposite effects on the abundance of these deer and may facilitate their coexistence. Hunting should be carefully controlled or managed to ensure the conservation of these little known species.     

Parasites of the collared peccary from Texas

Results of a survey of the parasites of the collared peccary (Dicotyles tajacu angulatus) in Texas are presented. Three ectoparasites, Amblyomma cajennense, Dermacentor variabilis, and Pulex porcinus were very common on peccaries from south Texas, but less common or absent in arid west Texas. Sucking lice, Pecaroecus javalii, were common on peccaries from west Texas, but were not found in south Texas. The known range of this louse in Texas is extended into the Big Bend area. Two ticks, Amnblyomma inornatumn and Haemaphysalis leporis-palustris, were found infrequently. Five of nine species of endoparasites found in this survey (Dirofilaria acutiuscula, Parabronema pecatriae, Parostertagia heterospiculum, Physocephalus sp., and Texicospirura turki) were prevalent. Three species, D. acutiuscula, Gongylonema baylisi, and Fascioloides magna, are reported from North American peccaries for the first time. The geographic distribution of the large American liver fluke, F. magna, coincided with an area where the parasite is enzootic in white-tailed deer. It is concluded that parasitism was of little importance in population control of peccaries during the period of the study.     

Reproductive biology of the wild red brocket deer (Mazama americana) female in the Peruvian Amazon

Knowledge of the reproductive biology is critical for the development of management strategies of the species both in captivity and in the wild, and to address conservation concerns regarding the sustainable use of a species. The present report characterizes some aspects of the reproductive biology of the wild red brocket deer inhabiting the North-eastern Peruvian Amazon region, based on the anatomical and histological examination of the female reproductive organs of 89 wild adult females in different reproductive states. The red brocket deer female presented ovarian follicular waves involving the synchronous growth of a cohort of an average 25 follicles but only one follicle generally survived and continued development, reaching maturity at 4mm. Mean ovulation rate was 1.14 and litter size was 1 fetus. Females presented a low rate of reproductive wastage of 14.3% of embryos. Among the 89 adult females studied, 41 (46.1%) were pregnant and 48 (53.9%) were non-pregnant females. In the Northeastern Peruvian Amazon, conceptions occurred year-round in the red brocket deer but there were peaks in the rate of conception. Estimated yearly reproductive production was 0.76-0.82 young per adult female. Most pregnant females in advanced stage of pregnancy had at least one active CL, suggesting the persistence of CL throughout gestation.     

Seed mass and the evolution of fleshy fruits in angiosperms

Fleshy fruits, like drupes and berries, have evolved many times through angiosperm history. Two hypotheses suggest that fleshy fruit evolution is related to changes in the seed mass fitness landscape. The reduced dispersal capability following from an increase in seed mass may be counterbalanced by evolution of traits mediating seed dispersal by animals, such as fleshy fruits. Alternatively, increasing availability and capabilities of frugivores promote evolution of fleshy fruits and allow an increase in seed size. Both these hypotheses predict an association between evolution of fleshy fruits and increasing seed size. We investigated patterns of fruit and seed evolution by contrasting seed mass between fleshy and non‐fleshy fruited sister clades. We found a consistent association between possession of fleshy fruits and heavier seeds. The direction of fruit type change did not alter this pattern; seed mass was higher in clades where fleshy fruits evolved and lower in clades where non‐fleshy fruits evolved, as compared to their sister clades. These patterns are congruent with the predictions from the two hypotheses, but other evidence is needed to distinguish between them. We emphasize the need to integrate studies of seed disperser effectiveness, seed morphology, and plant recruitment success to better understand the frugivores’ role in fleshy fruit evolution.