John R. Poulsen

Are Plant Populations Seed Limited? A Critique and Meta‐Analysis of Seed Addition Experiments

We examine the relative importance of processes that underlie plant population abundance and distribution. Two opposing views dominate the field. One posits that the ability to establish at a site is determined by the availability of suitable microsites (establishment limitation), while the second asserts that recruitment is limited by the availability of seeds (seed limitation). An underlying problem is that establishment and seed limitation are typically viewed as mutually exclusive. We conducted a meta‐analysis of seed addition experiments to assess the relative strength of establishment and seed limitation to seedling recruitment. We asked (1) To what degree are populations seed and establishment limited? (2) Under what conditions (e.g., habitats and life‐history traits) are species more or less limited by each? (3) How can seed addition studies be better designed to enhance our understanding of plant recruitment? We found that, in keeping with previous studies, most species are seed limited. However, the effects of seed addition are typically small, and most added seeds fail to recruit to the seedling stage. As a result, establishment limitation is stronger than seed limitation. Seed limitation was greater for large‐seeded species, species in disturbed microsites, and species with relatively short‐lived seed banks. Most seed addition experiments cannot assess the relationship between number of seeds added and number of subsequent recruits. This shortcoming can be overcome by increasing the number and range of seed addition treatments.

COMPARATIVE SEED SHADOWS OF BIRD-, MONKEY-, AND WIND-DISPERSED TREES

Although spatial patterns of seed distribution are thought to vary greatly among plant species dispersed by different vectors, few studies have directly examined this assumption. We compared patterns of seed rain of nine species of trees disseminated by large birds, monkeys, and wind in a closed canopy forest in Cameroon. We used maximum-likelihood methods to fit seed rain data to four dispersal functions: inverse power, negative exponential, Gaussian, and Student t. We then tested for differences in dispersal characteristics (1) among individuals within species, and (2) among species dispersed by the same vector. In general, an inverse power function best described animal-dispersed species and the Gaussian and Student t functions best described wind-dispersed species. Animal-dispersed species had longer mean dispersal distances than wind-dispersed species, but lower fecundities. In addition to these distinct differences in average dispersal distance and functional form of the seed shadow between animal- and wind-dispersed species, seed shadows varied markedly within species and vector, with conspecifics and species within vector varying in their dispersal scale, fecundity, and clumping parameters. Dispersal vectors determine a significant amount of variation in seed distribution, but much variation remains to be explained. Finally, we demonstrate that most seeds, regardless of vector, fall directly under the parent canopy. Long-distance dispersal events (>60 m) account for a small proportion of the seed crop but may still be important in terms of the absolute numbers of dispersed seeds and effects on population and community dynamics.

A long-term evaluation of fruiting phenology: importance of climate change

Within the last decade the study of phenology has taken on new importance because of its contribution to climate-change research. However, phenology data sets spanning many years are rare in the tropics, making it difficult to evaluate possible responses of tropical communities to climate change. Here we use two data sets (1970-1983 and 1990-2002) to describe the fruiting patterns of the tropical tree community in Kibale National Park, Uganda. To address variation in spatial patterns, we describe fruiting over 2-3 y among four sites each separated by 12-15 km. Presently, the Kibale region is receiving c. 300 mm more rain than it did at the start of the century, droughts are less frequent, the onset of the rainy season is earlier, and the average maximum monthly temperature is 3.5 ◦ C hotter than it was 25 y ago. The 1990-2002 phenology data illustrated high temporal variability in the proportion of the populations fruiting. Interannual variation in community-wide fruit availability was also high; however, the proportion of trees that fruited has increased over the past 12+ y. At the species level a variety of patterns were exhibited; however, a number of the most common species currently rarely fruit, and when they do, typically < 4% of the individuals take part in fruiting events. Combining the data set from 1990 to 2002 with that from 1970 to 1983 for specific species again reveals an increase in the proportion of trees fruiting between 1990 and 2002; however, the proportion of the populations fruiting decreased during the earlier period. When one examines particular species over this whole period a variety of patterns are evident. For example, Pouteria altissima exhibited a relatively regular pattern of fruiting during the 1970s; however, it rarely fruited in the 1990s. Contrasting phenological patterns at four sites revealed that at the community level the fruiting patterns of only one of the six pair-wise site combinations were correlated. Relationships between rainfall and fruiting were variable among sites. Contrasting changes in fruiting patterns over the 30 y with differences among the four sites varying in rainfall, suggests that the changes observed in fruiting may be due to climate change. Responses to this climate change are likely complex and will vary among species. However, for some species, current conditions appear unsuitable for fruiting.

DIFFERENTIAL RESOURCE USE BY PRIMATES AND HORNBILLS: IMPLICATIONS FOR SEED DISPERSAL

Arboreal frugivores, such as primates and hornbills, are important seed dis- persers for many tropical plant species, yet the degree to which they use the same resources is unknown. If primates and hornbills consume the same fruit species, they may be redundant in their roles as seed dispersers, and the loss of one of these taxa may be compensated for by the other. To examine resource use by tropical frugivores, we quantified the feeding habits of two hornbill species, Ceratogymna atrata and C. cylindricus, and five primate species, Colobus guereza, Lophocebus albigena, Cercopithecus pogonias, C. cephus, and C. nictitans, in the lowland rainforest of south-central Cameroon. Based on over 2200 feeding observations recorded between January and December 1998, we characterized the diets and estimated dietary overlap among frugivore species. Previous studies have cal- culated dietary overlap by counting the number of diet species that two animals share, often leading to inflated estimates of overlap. Our method incorporated the proportional use of diet species and fruit availability into randomization procedures, allowing a clearer as- sessment of the actual degree of overlap. This added complexity of analysis revealed that, although the diets of a hornbill and a primate species may have as many as 36 plant species in common, actual dietary overlap is low. These results suggested that there are distinct hornbill and primate feeding assemblages, with primates consuming a greater diversity of plant species and higher levels of nonfruit items like leaves and seeds. Using Correspon- dence Analysis, we also identified two primate assemblages, separated largely by degree of frugivory and folivory. In addition, we found that hornbills feed at significantly higher strata in the forest canopy and eat fruits of different colors than primates. Averaged across the year, overlap between groups (hornbill-primate) was significantly lower than combined within-group overlap (primate-primate and hornbill-hornbill), showing that primates and hornbills have dissimilar diets and are not redundant as seed dispersers. In equatorial Africa, primate populations face greater declines than hornbill populations because of hunting. It is unlikely that seed dispersal by hornbills will compensate for the loss of primates in maintaining forest structure.

Logging concessions can extend the conservation estate for Central African tropical forests.

The management of tropical forest in timber concessions has been proposed as a solution to prevent further biodiversity loss. The effectiveness of this strategy will likely depend on species-specific, population-level responses to logging. We conducted a survey (749 line transects over 3450 km) in logging concessions (1.2 million ha) in the northern Republic of Congo to examine the impact of logging on large mammal populations, including endangered species such as the elephant (Loxodonta africana), gorilla (Gorilla gorilla), chimpanzee (Pan troglodytes), and bongo (Tragelaphus eurycerus). When we estimated species abundance without consideration of transect characteristics, species abundances in logged and unlogged forests were not different for most species. When we modeled the data with a hurdle model approach, however, analyzing species presence and conditional abundance separately with generalized additive models and then combining them to calculate the mean species abundance, species abundance varied strongly depending on transect characteristics. The mean species abundance was often related to the distance to unlogged forest, which suggests that intact forest serves as source habitat for several species. The mean species abundance responded nonlinearly to logging history, changing over 30 years as the forest recovered from logging. Finally the distance away from roads, natural forest clearings, and villages also determined the abundance of mammals. Our results suggest that logged forest can extend the conservation estate for many of Central Africas most threatened species if managed appropriately. In addition to limiting hunting, logging concessions must be large, contain patches of unlogged forest, and include forest with different logging histories.

Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes

• It has long been believed that plant species from the tropics have higher levels of traits associated with resistance to herbivores than do species from higher latitudes. A meta-analysis recently showed that the published literature does not support this theory. However, the idea has never been tested using data gathered with consistent methods from a wide range of latitudes. • We quantified the relationship between latitude and a broad range of chemical and physical traits across 301 species from 75 sites world-wide. • Six putative resistance traits, including tannins, the concentration of lipids (an indicator of oils, waxes and resins), and leaf toughness were greater in high-latitude species. Six traits, including cyanide production and the presence of spines, were unrelated to latitude. Only ash content (an indicator of inorganic substances such as calcium oxalates and phytoliths) and the properties of species with delayed greening were higher in the tropics. • Our results do not support the hypothesis that tropical plants have higher levels of resistance traits than do plants from higher latitudes. If anything, plants have higher resistance toward the poles. The greater resistance traits of high-latitude species might be explained by the greater cost of losing a given amount of leaf tissue in low-productivity environments.

Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon

Multiple species of primate disperse seeds and differentially contrib- ute to the seed rain in tropical forests. The goal of this study was to examine seed dispersal by a primate community of five monkey and two ape species in the Dja Reserve, Cameroon. The density of primates in the reserve was calculated to be 77 individuals km −2 . Analysis of 5789 faecal clumps demonstrated that 40% of monkey and 74% of ape faecal clumps possessed whole seeds. Six of the seven focal species acted as seed dispersers; faecal clumps passed by the black-and-white colobus (Colobus guereza) did not contain any whole seeds during the study. Seed passage trials on four captive monkey species showed monkeys to have an average seed passage time of 22 hours and defecation rate of five times per day. From the above results, the primate community was estimated to defecate 1129 seeds km −2 d −1 . Seeds passed by the primate community came from 125 species of trees, lianas and shrubs, equivalent to at least 34% of the known tree flora. Rarefaction curves indicated that additional collection effort would identify more seed species passed by primates. Germination studies demonstrated that primate-passed seeds are viable. The number of seeds and plant species dispersed suggests that the primate community plays an important role in the maintenance of forest structure.

Fruiting trees as dispersal foci in a semi-deciduous tropical forest.

Quantification of seed rain patterns is an initial step toward explaining variation in plant recruitment, and consequently, organization of forest communities. Spatially contagious patterns of seed deposition, where seeds are patchily dispersed with some sites receiving relatively high densities and others receiving low densities of seeds, may be a common phenomenon for which we have very little knowledge. For example, prior feeding events by frugivores (monkeys and birds) combined with transport and dispersal of seeds to other fruiting trees may result in the contagious deposition of non-conspecific seeds below them. Here, we examined whether fruiting trees act as dispersal foci in the semi-deciduous tropical rainforest of the Dja Reserve, Cameroon. Seed rain was sampled below the canopies of nine tree species: three typically dispersed by large, frugivorous birds, three dispersed by monkeys, and three dispersed by wind. We found no evidence that monkeys generate spatially contagious patterns of seed rain under fruiting trees at which they feed. However, we found that rates of deposition of non-conspecific seeds and species richness of seeds delivered by birds (hornbills and turacos) were significantly greater during fruiting than non-fruiting periods, and significantly greater under fruiting individuals of bird-dispersed tree species than under fruiting individuals of monkey- or wind-dispersed tree species. Additionally, during fruiting periods, the composition of non-conspecific seed rain under bird-dispersed tree species was more similar to other bird-dispersed trees than to monkey- or wind-dispersed tree species. The contagious dispersal of non-conspecific seeds to fruiting, bird-dispersed trees leads to higher seed densities under fruiting trees than those caused by local seed production. Non-conspecific seeds deposited in high densities may experience increased seed mortality even far from parent trees if predators are generalists. Alternatively, in the absence of complete density-dependent mortality, contagious seed dispersal could result in associations among species dispersed by the same dispersal agent.

Plants as Reef Fish: Fitting the Functional Form of Seedling Recruitment

The life histories of many species depend first on dispersal to local sites and then on establishment. After dispersal, density‐independent and density‐dependent mortalities modify propagule supply, determining the number of individuals that establish. Because multiple factors influence recruitment, the dichotomy of propagule versus establishment limitation is best viewed as a continuum along which the strength of propagule or establishment limitation changes with propagule input. To evaluate the relative importance of seed and establishment limitation for plants, we (1) describe the shape of the recruitment function and (2) use limitation and elasticity analyses to quantify the sensitivity of recruitment to perturbations in seed limitation and density‐independent and density‐dependent mortality. Using 36 seed augmentation studies for 18 species, we tested four recruitment functions against one another. Although the linear model (accounting for seed limitation and density‐independent mortality) fitted the largest number of studies, the nonlinear Beverton‐Holt model (accounting for density‐dependent mortality) performed better at high densities of seed augmentation. For the 18 species, seed limitation constrained population size more than other sources of limitation at ambient conditions. Seedling density reached saturation with increasing seed density in many studies, but at such high densities that seedling density was primarily limited by seed availability rather than microsite availability or density dependence.

Urban mockingbirds quickly learn to identify individual humans.

Practically all animals are affected by humans, especially in urban areas. Although most species respond negatively to urbanization, some thrive in human-dominated settings. A central question in urban ecology is why some species adapt well to the presence of humans and others do not. We show that Northern Mockingbirds (Mimus polyglottos) nesting on the campus of a large university rapidly learn to assess the level of threat posed by different humans, and to respond accordingly. In a controlled experiment, we found that as the same human approached and threatened a nest on 4 successive days, mockingbirds flushed from their nest at increasingly greater distances from that human. A different human approaching and threatening the nest identically on the fifth day elicited the same response as the first human on the first day. Likewise, alarm calls and attack flights increased from days 1–4 with the first human, and decreased on day 5 with the second human. These results demonstrate a remarkable ability of a passerine bird to distinguish one human from thousands of others. Also, mockingbirds learned to identify individual humans extraordinarily quickly: after only 2 30-s exposures of the human at the nest. More generally, the varying responses of mockingbirds to intruders suggests behavioral flexibility and a keen awareness of different levels of threat posed by individuals of another species: traits that may predispose mockingbirds and other species of urban wildlife to successful exploitation of human-dominated environments.