Demography of the understory herb Heliconia acuminata (Heliconiaceae) in an experimentally fragmented tropical landscape.

Habitat fragmentation remains a major focus of research by ecologists decades after being put forward as a threat to the integrity of ecosystems. While studies have documented myriad biotic changes in fragmented landscapes, including the local extinction of species from fragments, the demographic mechanisms underlying these extinctions are rarely known. However, many of them-especially in lowland tropical forests-are thought to be driven by one of two mechanisms: (1) reduced recruitment in fragments resulting from changes in the diversity or abundance of pollinators and seed dispersers or (2) increased rates of individual mortality in fragments due to dramatically altered abiotic conditions, especially near fragment edges. Unfortunately, there have been few tests of these potential mechanisms due to the paucity of long-term and comprehensive demographic data collected in both forest fragments and continuous forest sites. Here we report 11 years (1998-2009) of demographic data from populations of the Amazonian understory herb Heliconia acuminata (LC Rich.) found at Brazil's Biological Dynamics of Forest Fragments Project (BDFFP). The data set comprises >66,000 plant × year records of 8586 plants, including 3464 seedlings established after the first census. Seven populations were in experimentally isolated fragments (one in each of four 1-ha fragments and one in each of three 10-ha fragments), with the remaining six populations in continuous forest. Each population was in a 50 × 100 m permanent plot, with the distance between plots ranging from 500 m to 60 km. The plants in each plot were censused annually, at which time we recorded, identified, marked, and measured new seedlings, identified any previously marked plants that died, and recorded the size of surviving individuals. Each plot was also surveyed four to five times during the flowering season to identify reproductive plants and record the number of inflorescences each produced. These data have been used to investigate topics ranging from the way fragmentation-related reductions in germination influence population dynamics to statistical methods for analyzing reproductive rates. This breadth of prior use reflects the value of these data to future researchers. In addition to analyses of plant responses to habitat fragmentation, these data can be used to address fundamental questions in plant demography and the evolutionary ecology of tropical plants and to develop and test demographic models and tools. Though we welcome opportunities to collaborate with interested users, there are no restrictions on the use of this data set. However, we do request that those using the data for teaching or research purposes inform us of how they are doing so and cite this paper and the data archive when appropriate. Any publication using the data must also include a BDFFP Technical Series Number in the Acknowledgments. Authors can request this series number upon the acceptance of their article by contacting the BDFFP's Scientific Coordinator or E. M. Bruna.

Interactions between plant size and canopy openness influence vital rates and life-history tradeoffs in two neotropical understory herbs.

UNLABELLED: • PREMISE OF THE STUDY: For tropical forest understory plants, the ability to grow, survive, and reproduce is limited by the availability of light. The extent to which reproduction incurs a survival or growth cost may change with light availability, plant size, and adaptation to shade, and may vary among similar species.• METHODS: We estimated size-specific rates of growth, survival, and reproduction (vital rates), for two neotropical understory herbs (order Zingiberales) in a premontane tropical rainforest in Costa Rica. During three annual censuses we monitored 1278 plants, measuring leaf area, number of inflorescences, and canopy openness. We fit regression models of all vital rates and evaluated them over a range of light levels. The best fitting models were selected using Akaike's Information Criterion.• KEY RESULTS: All vital rates were significantly influenced by size in both species, but not always by light. Increasing light resulted in higher growth and a higher probability of reproduction in both species, but lower survival in one species. Both species grew at small sizes but shrank at larger sizes. The size at which shrinkage began differed among species and light environments. Vital rates of large individuals were more sensitive to changes in light than small individuals.• CONCLUSIONS: Increasing light does not always positively influence vital rates; the extent to which light affects vital rates depends on plant size. Differences among species in their abilities to thrive under different light conditions and thus occupy distinct niches may contribute to the maintenance of species diversity.

Active pollinator choice by Heliconia 'fits the bill'.

A new study documents that a tropical plant only reproduces when pollen has been deposited by a visitor capable of extracting nectar from its deep flowers. Large, long-billed hummingbirds generally carry greater quantities of, and more genetically diverse, pollen. Thus, plants can exert more active partner choice than previously considered possible.

Interaction intimacy of pathogens and herbivores with their host plants influences the topological structure of ecological networks in different ways.

UNLABELLED: • PREMISE OF THE STUDY: Over the past two decades an interest in the role that plant-animal mutualistic networks play in the organization and dynamic of biodiversity has steadily risen. Despite the ecological, evolutionary, and economic importance of plant-herbivore and plant-pathogen antagonistic relationships, however, few studies have examined these interactions in an ecological network framework.• METHODS: We describe for the first time the topological structure of multitrophic networks involving congeneric tropical plant species of the genus Heliconia (Heliconiaceae, Zingiberales) and their herbivores and pathogens in the state of Pernambuco, Brazil. We based our study on the available literature describing the organisms (e.g., insects, mites, fungi, and bacteria) that attack 24 different species, hybrids, and cultivated varieties of Heliconia.• KEY RESULTS: In general, pathogen- and herbivore-Heliconia networks differed in their topological structure (more modular vs. more nested, respectively): pathogen-Heliconia networks were more specialized and compartmentalized than herbivore-Heliconia networks. High modularity was likely due to the high intimacy that pathogens have with their host plants as compared with the more generalized feeding modes and behavior of herbivores. Some clusters clearly reflected the clustering of closely related cultivated varieties of Heliconia sharing the same pathogens.• CONCLUSIONS: From a commercial standpoint, different varieties of the same Heliconia species may be more susceptible to being attacked by the same species of pathogens. In summary, our study highlights the importance of interaction intimacy in structuring trophic relationships between plants and pathogens in the tropics.

Pollinator recognition by a keystone tropical plant.

Understanding the mechanisms enabling coevolution in complex mutualistic networks remains a central challenge in evolutionary biology. We show for the first time, to our knowledge, that a tropical plant species has the capacity to discriminate among floral visitors, investing in reproduction differentially across the pollinator community. After we standardized pollen quality in 223 aviary experiments, successful pollination of Heliconia tortuosa (measured as pollen tube abundance) occurred frequently when plants were visited by long-distance traplining hummingbird species with specialized bills (mean pollen tubes = 1.21 ± 0.12 SE) but was reduced 5.7 times when visited by straight-billed territorial birds (mean pollen tubes = 0.20 ± 0.074 SE) or insects. Our subsequent experiments revealed that plants use the nectar extraction capacity of tropical hummingbirds, a positive function of bill length, as a cue to turn on reproductively. Furthermore, we show that hummingbirds with long bills and high nectar extraction efficiency engaged in daily movements at broad spatial scales (∼1 km), but that territorial species moved only short distances (<100 m). Such pollinator recognition may therefore affect mate selection and maximize receipt of high-quality pollen from multiple parents. Although a diffuse pollinator network is implied, because all six species of hummingbirds carry pollen of H. tortuosa, only two species with specialized bills contribute meaningfully to its reproduction. We hypothesize that this pollinator filtering behavior constitutes a crucial mechanism facilitating coevolution in multispecies plant-pollinator networks. However, pollinator recognition also greatly reduces the number of realized pollinators, thereby rendering mutualistic networks more vulnerable to environmental change.

Tropical forest fragmentation limits pollination of a keystone understory herb.

Loss of native vegetation cover is thought to be a major driver of declines in pollination success worldwide. However, it is not well known whether reducing the fragmentation of remaining vegetation can ameliorate these negative effects. We tested the independent effects of composition vs. configuration on the reproductive success of a keystone tropical forest herb (Heliconia tortuosa). To do this we designed a large-scale mensurative experiment that independently varied connected forest-patch size (configuration) and surrounding amount of forest (composition). In each patch, we tested whether pollen tubes, fruit, and seed set were associated with these landscape variables. We also captured hummingbirds as an indication of pollinator availability in a subset of patches according to the same design. We found evidence for an effect of configuration on seed set of H. tortuosa, but not on other aspects of plant reproduction; proportion of seeds produced increased 40% across the gradient in patch size we observed (0.64 to > 1300 ha), independent of the amount of forest in the surrounding landscape at both local and landscape scales. We also found that the availability of pollinators was dependent upon forest configuration; hummingbird capture rates increased three and one-half times across the patch size gradient, independent of forest amount. Finally, pollinator availability was strongly positively correlated with seed set. We hypothesize that the effects of configuration on plant fitness that we observed are due to reduced pollen quality resulting from altered hummingbird availability and/or movement behavior. Our results suggest that prioritizing larger patches of tropical forest may be particularly important for conservation of this species.

Pollinator-mediated selection in a specialized hummingbird-Heliconia system in the Eastern Caribbean.

Phenotypic matches between plants and their pollinators often are interpreted as examples of reciprocal selection and adaptation. For the two co-occurring plant species, Heliconia bihai and H. caribaea in the Eastern Caribbean, we evaluated for five populations over 2 years the strength and direction of natural selection on corolla length and number of bracts per inflorescence. These plant traits correspond closely to the bill lengths and body masses of their primary pollinators, female or male purple-throated carib hummingbirds (Eulampis jugularis). In H. bihai, directional selection for longer corollas was always significant with the exception of one population in 1 year, whereas selection on bract numbers was rare and found only in one population in 1 year. In contrast, significant directional selection for more bracts per inflorescence occurred in all three populations of the yellow morph and in two populations of the red morph of H. caribaea, whereas significant directional selection on corolla length occurred in only one population of the red morph and one population of the yellow morph. Selection for longer corollas in H. bihai may result from better mechanical fit, and hence pollination, by the long bills of female E. jugularis, their sole pollinator. In contrast, competition between males of E. jugularis for territories may drive selection for more bracts in H. caribaea. Competitive exclusion of female E. jugularis by territorial males also implicates pollinator competition as a possible ecological mechanism for trait diversification in these plants.

Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape.

Seed dispersal is a crucial component of plant population dynamics. Human landscape modifications, such as habitat destruction and fragmentation, can alter the abundance of fruiting plants and animal dispersers, foraging rates, vector movement, and the composition of the disperser community, all of which can singly or in concert affect seed dispersal. Here, we quantify and tease apart the effects of landscape configuration, namely, fragmentation of primary forest and the composition of the surrounding forest matrix, on individual components of seed dispersal of Heliconia acuminata, an Amazonian understory herb. First we identified the effects of landscape configuration on the abundance of fruiting plants and six bird disperser species. Although highly variable in space and time, densities of fruiting plants were similar in continuous forest and fragments. However, the two largest-bodied avian dispersers were less common or absent in small fragments. Second, we determined whether fragmentation affected foraging rates. Fruit removal rates were similar and very high across the landscape, suggesting that Heliconia fruits are a key resource for small frugivores in this landscape. Third, we used radiotelemetry and statistical models to quantify how landscape configuration influences vector movement patterns. Bird dispersers flew farther and faster, and perched longer in primary relative to secondary forests. One species also altered its movement direction in response to habitat boundaries between primary and secondary forests. Finally, we parameterized a simulation model linking data on fruit density and disperser abundance and behavior with empirical estimates of seed retention times to generate seed dispersal patterns in two hypothetical landscapes. Despite clear changes in bird movement in response to landscape configuration, our simulations demonstrate that these differences had negligible effects on dispersal distances. However, small fragments had reduced densities of Turdus albicollis, the largest-bodied disperser and the only one to both regurgitate and defecate seeds. This change in Turdus abundance acted together with lower numbers of fruiting plants in small fragments to decrease the probability of long-distance dispersal events from small patches. These findings emphasize the importance of foraging style for seed dispersal and highlight the primacy of habitat size relative to spatial configuration in preserving biotic interactions.

Effects of forest fragmentation on the seedling recruitment of a tropical herb: assessing seed vs. safe-site limitation.

Studies simultaneously evaluating the importance of safe-site and seed limitation for plant establishment are rare, particularly in human-modified landscapes. We used spatially explicit neighborhood models together with data from 10 0.5-ha mapped census plots in a fragmented landscape spanning 1000 km2 to (1) evaluate the relative importance of seed production, dispersal, and safe-site limitation for the recruitment of the understory herb Heliconia acuminata; and (2) determine how these processes differ between fragments and continuous forests. Our analyses demonstrated a large degree of variation in seed production, dispersal, and establishment among and within the 10 study plots. Seed production limitation was strong but only at small spatial scales. Average dispersal distance was less than 4 m, leading to severe dispersal limitation at most sites. Overall, safe-site limitation was the most important constraint on seedling establishment. Fragmentation led to a more heterogeneous light environment with negative consequences for seedling establishment but had little effect on seed production or dispersal. These results suggest that the effects of fragmentation on abiotic processes may be more important than the disruption of biotic interactions in driving biodiversity loss in tropical forests, at least for some functional groups. These effects may be common when the matrix surrounding fragments contains enough tree cover to enable movement of dispersers and pollinators.

Water use in four model tropical plant associations established in the lowlands of Costa Rica

We examined soil water use patterns of four model plant associations established in the North Caribbean lowlands of Costa Rica by comparing the stable hydrogen isotope composition, δD, in xylem sap and in soil water at different depths, under rainy and dry conditions. Four 5-year-old model plant associations composed of 2 tree species (Hyeronima alchorneoides and Cedrela odorata) having different architecture and phenology were studied. Average tree height was 8.9 and 7.6 m, respectively. Each tree species was grown in monoculture and in polyculture with 2 perennial monocotyledons (Euterpe oleracea and Heliconia imbricata). Maximum rooting depth at the time of δD determination was ~ 2 m for almost all species. Most roots of all species were concentrated in the upper soil layers. Stomatal conductance to water vapor (gS) was higher in the deciduous C. odorata than in the evergreen H. alchorneoides; within each species, gS did not differ when the trees were grown in mono or in polyculture. During the rainy season, gradients in soil water δD were not observed. Average rainy season xylem sap δD did not differ among members of the plant combinations tested (-30 ‰), and was more similar to δD values of shallow soil water. Under dry conditions, volumetric soil water content declined from 50 to ~ 35%, and modest gradients in soil water δD were observed. xylem sap δD obtained during dry conditions was significantly lower than rainy season values. xylem sap δD of plants growing in the four associations varied between -9 and -22‰, indicating that shallow water was predominantly absorbed during the dry period too. Differences in xylem sap δD of trees and monocots were also detected, but no significant patterns emerged. The results suggest that: a) the plant associations examined extracted water predominantly from shallow soil layers (<1 m), b) the natural isotopic variation in soil and plant water at the study site was low, and c) the plant mixes obtain water from more than a single soil layer simultaneously. Temporal factors were important in determining the competition and complementary relations observed among the trees and the perennial monocots. Under the prevailing environmental conditions, water use in these plant associations was determined largely by species-specific attributes such as biomass allocation to fine roots, phenology, and canopy architecture, and to a lesser extent by water limitations. Rev. Biol. Trop. 56 (4): 1947-1957. Epub 2008 December 12.

Examinamos los patrones de uso de agua del suelo de cuatro asociaciones vegetales establecidas en el Caribe norte de Costa Rica, comparando la composición isotópica del hidrógeno, δD, en la savia del xilema y en el agua del suelo en condiciones lluviosas y secas. Estudiamos cuatro asociaciones de cinco años de edad compuestas por dos árboles (Hyeronima alchorneoides y Cedrela odorata) con diferente arquitectura y fenología, cultivados en mono y policultivo con dos monocotiledóneas perennes (Euterpe oleracea y Heliconia imbricata). Las excavaciones mostraron que la profundidad máxima de las raíces fue de 2 m para casi todas las especies, y que la mayor densidad de raíces se encontraba en la superficie del suelo. La conductividad estomática (gS) fue mayor en el árbol caducifolio (C. odorata) que en el perennifolio (H. alchorneoides); dentro de cada especie, gS no difirió cuando los árboles fueron cultivados en mono o en policultivo. Los resultados sugieren que: a) las asociaciones examinadas extrajeron agua predominantemente de las capas superficiales del suelo (<1 m), b) la variación natural en el acceso al agua del suelo por parte de las especies, y en las propiedades del suelo, fue baja, y c) las combinaciones de plantas obtuvieron agua de varias capas del perfil del suelo simultáneamente. Los factores relacionados con el tiempo fueron importantes en la determinación de las relaciones de competencia y complementariedad observadas entre los árboles y las monocotiledóneas perennes. En las condiciones ambientales prevalecientes, el uso del agua por parte de estas asociaciones de plantas fue determinado más por atributos, como la asignación de biomasa a las raíces finas, la fenología, y las propiedades del dosel, que por limitaciones en la disponibilidad de agua.

Water use in four model tropical plant associations established in the lowlands of Costa Rica.

We examined soil water use patterns of four model plant associations established in the North Caribbean lowlands of Costa Rica by comparing the stable hydrogen isotope composition, deltaD, in xylem sap and in soil water at different depths, under rainy and dry conditions. Four 5-year-old model plant associations composed of 2 tree species (Hyeronima alchorneoides and Cedrela odorata) having different architecture and phenology were studied. Average tree height was 8.9 and 7.6 m, respectively. Each tree species was grown in monoculture and in polyculture with 2 perennial monocotyledons (Euterpe oleracea and Heliconia imbricata). Maximum rooting depth at the time of 6D determination was approximately 2 m for almost all species. Most roots of all species were concentrated in the upper soil layers. Stomatal conductance to water vapor (gS) was higher in the deciduous C. odorata than in the evergreen H. alchorneoides; within each species, g, did not differ when the trees were grown in mono or in polyculture. During the rainy season, gradients in soil water 6D were not observed. Average rainy season xylem sap deltaD did not differ among members of the plant combinations tested (-30% per thousand), and was more similar to deltaD values of shallow soil water. Under dry conditions, volumetric soil water content declined from 50 to approximately 35%, and modest gradients in soil water deltaD were observed. Xylem sap deltaD obtained during dry conditions was significantly lower than rainy season values. Xylem sap deltaD of plants growing in the four associations varied between -9 and -22% per hundred, indicating that shallow water was predominantly absorbed during the dry period too. Differences in xylem sap deltaD of trees and monocots were also detected, but no significant patterns emerged. The results suggest that: (a) the plant associations examined extracted water predominantly from shallow soil layers (<1 m), (b) the natural isotopic variation in soil and plant water at the study site was low, and (c) the plant mixes obtain water from more than a single soil layer simultaneously. Temporal factors were important in determining the competition and complementary relations observed among the trees and the perennial monocots. Under the prevailing environmental conditions, water use in these plant associations was determined largely by species-specific attributes such as biomass allocation to fine roots, phenology, and canopy architecture, and to a lesser extent by water limitations.