Advances and Frontiers in Primate Seed Dispersal

Primates play important roles as seed dispersers in many tropical ecosystems, such that studies of their seed dispersal services and impacts have gained interests among primatologists and ecologists in the past few decades. In this article, we first report that the number of scientific publications on primate seed dispersal has increased rapidly over the past 20 years, based on an extensive literature review. These publications encompass diverse primate taxa from the four geographic regions where they naturally occur. We then summarize the contributions to this Special Issue, which reflect on these progresses. Finally, we provide new directions for the next decade.     

The Ecology and Evolution of Fruit Odor: Implications for Primate Seed Dispersal

Primates are now known to possess a keen sense of smell that serves them in various contexts, including feeding. Many primate species are frugivorous and provide essential seed dispersal services to a variety of plants. Studies of pollination ecology, and recently seed dispersal ecology, indicate that animal mutualist behavior exerts selection pressures that drive changes in flower and fruit traits. As a result, the use of olfaction in in primate feeding ecology may have affected the evolution of fruit odor in species that rely on primate seed dispersal. However, this hypothesis is seldom tested. Here, we summarize the available information on how primates may have affected the evolution of fruit odor. We ask what the chemistry of primate fruit odor may look like, what information fruit odor may convey, whether there are geographical differences in fruit odor, and what other factors may affect the odor of fruits consumed by primates. We identify many gaps in the available data and offer research questions, hypotheses, and predictions for future studies. Finally, to facilitate standardization in the field, we discuss methodological issues in the process of odor sampling and analysis.     

Primate Seed Dispersal and Forest Restoration: An African Perspective for a Brighter Future

Primate seed dispersal is a vital, but complex, ecological process that involves many interacting agents and plays important roles in the maintenance of old-growth forest, as well as in the development of regenerating forest. Focusing primarily on African examples, in this article we briefly review the ecological process of primate seed dispersal, highlighting understudied and contentious topics, and then we discuss how our knowledge on primate seed dispersal can promote both forest restoration and primate conservation. Though it is frequently claimed that primates are critically important for the maintenance of diverse tropical forest ecosystems, we believe that more empirical evidence is needed to support this claim. Confounding factors can often be difficult to rule out and long-term studies extending beyond the seedling or sapling stage are very rare. In addition, though primates are critical for initial seed dispersal of many tree species, spatial and temporal variation in post-deposition processes, such as secondary seed dispersal and predation by rodents, can dramatically alter the initial patterns generated by primates. However, given the need for immediate conservation action to prevent further primate extinctions, we advocate that the knowledge about primate seed dispersal be used in formulating informed conservation plans. One prominent area where this knowledge will prove extremely valuable is in forest restoration efforts. To aid in the development of such efforts, we pose five questions, the answers to which will help facilitate forest restoration becoming a useful tool in strategies designed to conserve primates.     

Primate and Dung Beetle Communities in Secondary Growth Rain Forests: Implications for Conservation of Seed Dispersal Systems

Conservation efforts are often aimed at one or a few species. However, habitat sustainability relies on ecological interactions among species, such as seed dispersal. Thus, a community-scale conservation strategy may be more valuable in some settings. We describe communities of primary (primates) and secondary (dung beetles) seed dispersers from 5 sites in the Brazilian Amazon. We estimate community biomass of these taxa and, using multivariate ordination, examine the potential for natural reforestation at each site, given the communities of seed dispersers present. Since disturbed habitat is increasingly common and increasingly the focus of conservation efforts, we also examine differences among seed disperser communities between primary forest and secondary growth at each site. Analyses of faunal biomass in different localities and habitats indicate that secondary growth receives nearly as much use by primates as primary forest; given the dominant groups of dung beetles in secondary growth, disturbed habitat should show a pattern of seed burial that is clumped and deep. Areas with high biomass of Alouatta spp. and the large nocturnal dung beetle species may have the greatest potential for natural reforestation of secondary growth particularly for large seeded species. The data suggest that knowledge of the biomass of primary and secondary dispersing fauna facilitates predictions for the likelihood of disturbed habitat to regenerate and comparisons of sites in broader geographical areas e.g., Neotropical vs. Paleotropical forests.     

Acute Chagas Disease: New Global Challenges for an Old Neglected Disease

Chagas disease is caused by infection with the protozoan Trypanosoma cruzi, and although over 100 years have passed since the discovery of Chagas disease, it still presents an increasing problem for global public health. A plethora of information concerning the chronic phase of human Chagas disease, particularly the severe cardiac form, is available in the literature. However, information concerning events during the acute phase of the disease is scarce. In this review, we will discuss (1) the current status of acute Chagas disease cases globally, (2) the immunological findings related to the acute phase and their possible influence in disease outcome, and (3) reactivation of Chagas disease in immunocompromised individuals, a key point for transplantation and HIV infection management.     

啮齿动物的贮藏行为与植物种子的扩散

绝大多数啮齿动物一方面取食大量的植物种子和果实,另一方面通过其贮食行为将植物种子和果实搬运到远离母树的地点,即扩散,并将它们分散埋藏在落叶下或浅表的土层中,从而影响种子和果实的时空分布,最后导致幼苗在有利的条件下发生和建成,实现植物更新。啮齿动物与植物种子和果实之间已广泛形成了互惠或协同进化的关系。啮齿动物的贮食行为主要通过以下几个过程对植物种子和果实的扩散产生影响：选择、搬运和埋藏以及随后对种子和幼苗存活和死亡的影响等。本综述了啮齿动物对植物种子和果实贮藏的研究结果,以期为进一步开展啮齿动物的贮食行为在植物种子和果实的扩散中的作用的研究提供参考。     

Avian Seed Dispersal of an Invasive Shrub

The incorporation of an animal-dispersed exotic plant species into the diet of native frugivores can be an important step to that species becoming invasive. We investigated bird dispersal of Lonicera maackii, an Asian shrub invasive in eastern North America. We (i) determined which species of birds disperse viable L. maackii seeds, (ii) tested the effect of gut passage on L. maackii seeds, and (iii) projected the seed shadow based on habitat use by a major disperser. We found that four native and one exotic bird species dispersed viable L. maackii seeds. Gut passage through American robins did not inhibit germination, but gut passage through cedar waxwings did. American robins moved mostly along woodlot edges and fencerows, leading us to project that most viable seeds would be defecated in such habitats, which are very suitable for L. maackii. We conclude that L. maackii has been successfully incorporated into the diets of native and exotic birds and that American robins preferentially disperse seeds to suitable habitat.     

Primate Ecology and Social Structure Vol. 1: Lorises, Lemurs and Tarsiers: Primate Ecology and Social Structure Vol. 2: New World Monkeys: Primate Ecology and Social Structure Vol. 3: Old World Monkeys and Apes

Primate Ecology and Social Structure Vol. 1: Lorises, Lemurs and Tarsiers. Robert W. Sussman. Needham Heights. MA: Pearson Custom Publishing, 1999. 284 pp.
Primate Ecology and Social Structure Vol. 2: New World Monkeys. Robert W. Sussman. Needham Heights. MA: Pearson Custom Publishing, 2000. 207 pp.
Primate Ecology and Social Structure Vol. 3: Old World Monkeys and Apes. Robert W. Sussman. Needham Heights. MA: Pearson Custom Publishing, in press.     

Primary Amoebic Meningoencephalitis Caused by Naegleria fowleri: An Old Enemy Presenting New Challenges

First discovered in 1899, Naegleria fowleri is a protist pathogen, known to infect the central nervous system and produce primary amoebic meningoencephalitis. The most distressing aspect is that the fatality rate has remained more than 95%, despite our advances in antimicrobial chemotherapy and supportive care. Although rare worldwide, most cases have been reported in the United States, Australia, and Europe (France). A large number of cases in developing countries go unnoticed. In particular, religious, recreational, and cultural practices such as ritual ablution and/or purifications, Ayurveda, and the use of neti pots for nasal irrigation can contribute to this devastating infection. With increasing water scarcity and public reliance on water storage, here we debate the need for increased awareness of primary amoebic meningoencephalitis and the associated risk factors, particularly in developing countries.     

Primate Conservation: Unmet Challenges and the Role of the International Primatological Society

In the last 40 years, threats to the survival of wild primate populations have greatly increased. Primatologists have long been aware of these threats, and since 1978 have formulated plans to safeguard threatened species. Yet an increasing number of primate species face a high to extremely high risk of extinction. I asked 14 experienced field primatologists for their views on the most serious challenges to more effective primate conservation. They listed habitat loss and hunting as the major direct threats to primate survival, and noted that these activities are driven predominantly by the growth of human populations and the tendency of people to consume resources beyond their immediate survival needs. Two factors identified as most hindering effective action were a lack of political will and insufficient funding, while the main actions recommended to mitigate threats were to undertake more awareness-raising and make protected areas more effective. Such actions have long been recommended, so why have they not worked better? Perhaps the pressures on the natural world are too great to be countered, but I suggest also that too many of the various actors involved in conservation are overly driven by materialism and self-interest. I recommend more attention to the common good and a greater emphasis on the ethical and spiritual reasons for conservation. The International Primatological Society itself could have more vigorous debates on conservation policy at its congresses, and should consider the creation of regional chapters with the aim of promoting primatology in habitat countries.     

Macaques as Seed Dispersal Agents in Asian Forests: A Review

The role of primates in seed dispersal is well recognized. Macaques (Macaca spp.) are major primate seed dispersers in Asia, and recent studies have revealed their role as seed dispersal agents in this region. Here, we review present knowledge of the traits that define the role of macaques as seed dispersers. The size of seeds in fruit influences whether macaques swallow (0.5–17.1 mm; median: 3.0), spit (1–37 mm; median: 7.6), or drop (8.2–57.7 mm; median: 20.5) them. Dispersal distances via defecation are several hundreds of meters (median: 259 m, range: 0–1300 m), shorter than those achieved by some mammals and birds in tropical and temperate regions. However, macaques disperse seeds by defecation at comparable distances to omnivorous carnivores, and further than passerines. Seed dispersal distance by spitting is much shorter (median: 20 m, range: 0–405 m) than by defecation. Among Asian primates, seed dispersal distances resulting from macaque defecation are shorter than those for gibbons and longer than those for langurs. The effects of seed ingestion on the percentage and speed of germination vary among both plant and macaque species. The degree of frugivory, fruit/seed handling methods, seed dispersal distance, microhabitats of dispersed seeds, and effects of dispersal on seed germination vary seasonally and interannually, and long-term studies of the ecological role of macaques are needed. Researchers have begun to assess the effectiveness of seed dispersal by macaques, secondary dispersal of seeds originally dispersed by macaques, and the effects of provisioning on seed dispersal. Future studies should also test the effects of social factors (such as age and rank), which have received little attention in studies of seed dispersal.     

Sociability in Old Female Japanese Monkeys: Human versus Nonhuman Primate Aging

Over a period of 20 months, 18 aged and 22 non-aged semi-free ranging female Japanese monkeys were observed, and a total of 440 hours of focal animal data were collected. The goal of the study was to investigate the reported pattern of disengagement in old female monkeys. For each subject female, two sociability scores were calculated: the total number of other animals with whom time was spent in affiliative social interaction, and the total amount of time spent in affiliative social interaction. These data were analyzed in order to determine any change in sociability based on age. No relationship was found between age and sociability. The absence of a pattern of decreased social interaction with advancing age in these monkeys is discussed in terms of the methodological differences with earlier studies. It is suggested that the life of nonhuman primates may be essentially continuous from the attainment of adulthood to death, with no recognizable social stage for the elderly, at least in terms of sociability and isolation. Menopause, awareness of mortality, and interindividual dependence are three elements of the human life course that appear to be absent in this troop of Japanese monkeys, and these are discussed as key elements that may render the later portion of the human life course to be very different from that of monkeys, and possibly from that of all other primates.     

Chemotaxis: Old and New

After describing briefly the work of Engelmann and Pfeffer about 100 years ago, the author presents the early history of bacterial chemotaxis in his laboratory since 1960. Then the report is brought up to the present by review of research in many laboratories including the author's.     

Dispersal of the Old World screw-worm fly Chrysomya bezziana

Abstract. Dispersal of the Old World screw-worm fly, Chrysomya bezziana Villeneuve, was studied in Papua New Guinea by releasing radio-isotope labelled, laboratory-reared flies and collecting their labelled egg masses from sentinel cattle. A log-linear model was developed to describe recapture rate. Distance was found to dominate the model and was represented by a bilinear ('broken-stick') term as log-distance. Further terms in the model such as attractiveness of the site (estimated from the number of non-labelled egg masses), the season of the year and a time trend were statistically significant but of minor importance. From the model, the median distance females dispersed before depositing an egg mass was 10.8 km. The maximum distance from the release site that egg masses were recovered was 100 km.
The dispersal ability of C. bezziana is discussed in terms of its impact on the prospects of eradicating this species using SIRM if an outbreak occurred in Australia.     

食干果鸟对种子传播的作用

食干果鸟对种子传播的作用鲁长虎袁力（东北林业大学,哈尔滨１５００４０）ＥｆｆｅｃｔｏｆＤｒｙ＿ｆｒｕｉｔＥａｔｉｎｇＢｉｒｄｓｔｏＳｅｅｄＤｉｓｐｅｒｓａｌ．Ｌｕｃｈａｎｇｈｕ,ＹｕａｎＬｉ（ＮｏｒｔｈｅａｓｔＦｏｒｅｓｔｒｙＵｎｉｖｅｒｓｉｔｙ,...     

Dispersal of Transgenes through Maize Seed Systems in Mexico

Objectives

Current models of transgene dispersal focus on gene flow via pollen while neglecting seed, a vital vehicle for gene flow in centers of crop origin and diversity. We analyze the dispersal of maize transgenes via seeds in Mexico, the crop''s cradle.

Methods

We use immunoassays (ELISA) to screen for the activity of recombinant proteins in a nationwide sample of farmer seed stocks. We estimate critical parameters of seed population dynamics using household survey data and combine these estimates with analytical results to examine presumed sources and mechanisms of dispersal.

Results

Recombinant proteins Cry1Ab/Ac and CP4/EPSPS were found in 3.1% and 1.8% of samples, respectively. They are most abundant in southeast Mexico but also present in the west-central region. Diffusion of seed and grain imported from the United States might explain the frequency and distribution of transgenes in west-central Mexico but not in the southeast.

Conclusions

Understanding the potential for transgene survival and dispersal should help design methods to regulate the diffusion of germplasm into local seed stocks. Further research is needed on the interactions between formal and informal seed systems and grain markets in centers of crop origin and diversification.     

Steep Decline and Cessation in Seed Dispersal by Myrmica rubra Ants

Myrmecochorous diaspores bear a nutrient-rich appendage, the elaiosome, attractive to ant workers that retrieve them into the nest, detach the elaiosome and reject the seed intact. While this interaction is beneficial for the plant partner by ensuring its seed dispersal, elaiosome consumption has various effects −positive, negative or none − on ants’ demography and survival, depending on both the ant/plant species involved. In this context, the contribution of ants to seed dispersal strongly varies according to the ant/plant pairs considered. In this paper, we investigate whether the dynamics of myrmecochory also vary on a temporal scale, for a given pair of partners: Myrmica rubra ants and Viola odorata seeds. During their first encounter with seeds, ants collect all the diaspores and eat the majority of elaiosomes. Both the harvesting effort and the elaiosome consumption decline when seeds are offered on the next week and completely cease for the following weeks. This is related to a decrease in the number of foragers reaching the food source, as well as to a reduced probability for an ant contacting a seed to retrieve it. Seed retrieval is not reactivated after seven weeks without any encounter with V. odorata seeds. By contrast, naive ant colonies only fed with fruit flies do not show a decline of prey harvesting of which the speed of retrieval even increases over the successive weeks. Myrmecochory may thus be labile at the scale of a fruiting season due to the ability of ants to steeply tune and cease for several months the harvesting of these seemingly poorly rewarding items and to maintain cessation of seed exploitation. The present study emphasizes the importance of a long-lasting follow up of the myrmecochory process, to assess the stability of this ant-plant partnership and to identify mechanisms of adaptive harvesting in ants.