A metapopulation approach to the analysis of long‐term changes in the epiphyte vegetation on the host tree Annona glabra

Question: Do vascular epiphyte species have a metapopulation structure? What are the qualitative and quantitative long‐term changes of the complete vascular epiphyte vegetation in a particular host tree species? Location: Lowland forest on Barro Colorado Island (9° 10’ N, 79°51’ W), Republic of Panama. Methods: In 1994 and 2002 we conducted a census of all vascular epiphytes growing on more than 1000 Annona glabra trees (= patches). Epiphyte species abundances were recorded at the tree level in each census. Results: The number of epiphyte individuals increased from ca. 15 000 to ca. 23 700 individuals during the census interval while the species composition on Annona glabra as a whole was rather stable. There was a strong positive relationship between occurrence in patches and local abundance of the species, and between species richness and host tree stand size. The dynamics of local populations of a given species were uncorrelated to each other; small and large local populations of most species had the same probability to go extinct. The frequency distribution of species on all host trees was not bimodal, but on a subset of heavily colonized host tree stands it was. Numbers of species and individuals were correlated with tree size which was not due to a correlation of tree size and tree age. Conclusions: As far as the most abundant epiphyte species with metapopulation structures are concerned, these species belong to diverse families, e. g. Orchidaceae, Bromeliaceae and Polypodiaceae. Even ca. 80 years after the initial establishment of the host tree species in the study area epiphytes are still in the stage of initial colonization and have not reached a steady state as indicated by the strong increase in individuals and the ongoing colonization of empty trees.     

Post‐Dispersal Seed Removal and Germination Selected Tree Species Dispersed by Cebus capucinus on Barro Colorado Island,Panama1

Dispersal quality, an important component of seed disperser effectiveness, may strongly affect the rate of plant recruitment. Here we evaluated the quality of Cebus monkey dispersal by comparing the secondary removal fate and germination of fresh and Cebus‐ingested seeds of nine tree species on Barro Colorado Island, Panama. Overall, rates of secondary seed removal by vertebrates were low, with most Cebus defecations remaining undisturbed for extended periods on the forest floor. Only four of 30 feces were completely buried by dung beetles, and we found significantly higher vertebrate removal of defecated seeds than control seeds for only one species, Cordia bicolor. Seed germination varied greatly between plant taxa. Seeds of 3 out of 9 species showed significantly higher percent germination after monkey gut passage than control fresh seeds. Germination times tended to be shorter for defecated than for control seeds but were significantly different only for one of nine species, Cecropia insignis. Low rates of seed removal from Cebus feces, coupled with high germination probabilities, suggest high dispersal effectiveness for Cebus and contrasts strongly with patterns of post‐dispersal seed fate recorded for other primate species.     

Seasonal Foraging Activity and Bait Preferences of Ants on Barro Colorado Island, Panama1

A yearlong arboreal baiting survey of ants was conducted during 1983 on Barro Colorado Island, Panama. Because of a severe El Nino event, the 1983 dry season in Panama was exceptionally long and dry with a distinct boundary between the dry and wet seasons. Baits, located on tree trunks, attracted both terrestrial and arboreal ants, allowing comparisons between the two groups. Species composition at baits changed dramatically with season. Baits were primarily occupied by arboreal species during the dry season, while wet season baits were occupied mostly by terrestrial species. Arboreal and terrestrial ants differed markedly in their preferences for protein‐ or carbohydrate‐based baits; arboreal ants preferred protein‐based baits and terrestrial ants preferred carbohydrate‐based baits. Foraging preference for protein suggests that protein resources were limiting for arboreal ants, particularly during the dry season, and that carbohydrate resources were limiting for terrestrial ants. Fundamental differences in arboreal and terrestrial habitats may promote the differences in foraging strategies observed during an annual cycle in a seasonal tropical forest.     

Photosynthetic induction and leaf carbon gain in the tropical understorey epiphyte,Aspasia principissa

Gas exchange of the understorey epiphyte Aspasia principissa was studied in fluctuating light conditions both in the laboratory and in the field, testing the hypothesis that vascular epiphytes differ from most terrestrial understorey plants in showing a higher priority for water conservation. Consequently, a slow response of stomatal conductance to sudden increases in incident photon flux density (PFD) was expected, as was a fast loss of induction after such a light fleck. Results were only partly consistent with these expectations. Full induction of photosynthesis was indeed very slow and was not reached before, respectively, 40 and 60 min of saturating PFD in the field and the laboratory. In contrast, kinetics of induction loss were comparable with those of most terrestrial species studied to date. The overall impact of light flecks on in situ carbon gain again fulfilled expectations, being rather limited: the observed carbon gain was only approx. 66% of the potential carbon gain estimated from a square-wave response model. It is concluded that in the drought-prone epiphytic habitat of a moist lowland forest, water conservation takes priority over carbon gain, which severely limits the use of light flecks for CO(2) fixation in vascular epiphytes.     

Water relations of five tropical tree species on Barro Colorado Island,Panama

Summary Diurnal curves of xylem pressure potential (P) and leaf conductance (C) were measured for five tree species of the lowland tropical forest on Barro Colorado Island, Panama. Measurements were taken just before and just after the beginning of the rainy season. The species studied were: Cordia alliodora, Faramea occidentalis, Heisteria concinna, Macquira costaricana, and Trichilia cipo.For all species, predawn (base P) and daytime values of P increased markedly after the beginning of the rainy season. Diurnal patterns of C were quite diverse. C. alliodora showed a decline in C during the day whereas F. occidentaus, H. concinna, and M. costaricana showed little change. Conductance of the last three species was lower before the first rains. T. cipo exhibited more complicated behavior for P and C. Before the rainy season, low values of base P and midday P were observed (-26 bars and-39 bars, respectively). Conductance was also low. After the first rains, base P increased to-4 bars. At this time, midday P and C appeared to respond to vapor pressure deficit (VPD), being less on a day with high VPD than on a day with low VPD.     

The Butterflies of Barro Colorado Island,Panama: Local Extinction since the 1930s

Few data are available about the regional or local extinction of tropical butterfly species. When confirmed, local extinction was often due to the loss of host-plant species. We used published lists and recent monitoring programs to evaluate changes in butterfly composition on Barro Colorado Island (BCI, Panama) between an old (1923–1943) and a recent (1993–2013) period. Although 601 butterfly species have been recorded from BCI during the 1923–2013 period, we estimate that 390 species are currently breeding on the island, including 34 cryptic species, currently only known by their DNA Barcode Index Number. Twenty-three butterfly species that were considered abundant during the old period could not be collected during the recent period, despite a much higher sampling effort in recent times. We consider these species locally extinct from BCI and they conservatively represent 6% of the estimated local pool of resident species. Extinct species represent distant phylogenetic branches and several families. The butterfly traits most likely to influence the probability of extinction were host growth form, wing size and host specificity, independently of the phylogenetic relationships among butterfly species. On BCI, most likely candidates for extinction were small hesperiids feeding on herbs (35% of extinct species). However, contrary to our working hypothesis, extinction of these species on BCI cannot be attributed to loss of host plants. In most cases these host plants remain extant, but they probably subsist at lower or more fragmented densities. Coupled with low dispersal power, this reduced availability of host plants has probably caused the local extinction of some butterfly species. Many more bird than butterfly species have been lost from BCI recently, confirming that small preserves may be far more effective at conserving invertebrates than vertebrates and, therefore, should not necessarily be neglected from a conservation viewpoint.     

Intragroup Social Relationships of Male Alouatta palliata on Barro Colorado Island,Republic of Panama

We examined social and spatial relations of adult males in one group of mantled howling monkeys (Alouatta palliata) on Barro Colorado Island (BCI) in central Panama to document patterns of association. Beyond the existence of an alpha male, we could not distinguish any linear dominance hierarchy among the 6 study males. All males copulated with estrous females. Our findings contrast with reports of intragroup male behavior in Costa Rican howlers. Study males engaged in little or no affiliative or agonistic behavior with one another, but engaged in significantly more such interactions with females. The alpha male, the oldest male and a younger male were most frequently in association with females. Of group males, the oldest male associated significantly more with other males. Overall, male behavior in mantled howling monkeys on BCI generally followed the van Hooff and van Schaik (1994) model of male relationships. The low incidence of intragroup social interactions of any type in the focal males may reflect the energetic costs of social behavior. We suggest that intragroup social relationships among mantled howler males are structured by more subtle means than overt physical interactions, possibly including vocal communication, relationships with individual group females, and kinship.     

Rainfall and parasitic wasp (Hymenoptera: Ichneumonoidea) activity in successional forest stages at Barro Colorado Nature Monument, Panama, and La Selva Biological Station, Costa Rica

1 In 1997, we ran two Malaise insect traps in each of four stands of wet forest in Costa Rica (two old‐growth and two 20‐year‐old stands) and four stands of moist forest in Panama (old‐growth, 20, 40 and 120‐year‐old stands). 2 Wet forest traps caught 2.32 times as many ichneumonoids as moist forest traps. The average catch per old‐growth trap was 1.89 times greater than the average catch per second‐growth trap. 3 Parasitoids of lepidopteran larvae were caught in higher proportions in the wet forest, while pupal parasitoids were relatively more active in the moist forest. 4 We hypothesize that moisture availability is of key importance in determining parasitoid activity, community composition and trophic interactions.     

Nutrient Dynamics of Soil Derived from Different Parent Material on Barro Colorado Island,Panama1

I compared the concentrations of N, P, and S in both litter and mineral soil (0–15 cm depth) from three old‐growth, tropical moist forests on Barro Colorado Island (BCI), Panama. Each site was on a different substrate (i.e., parent material), but otherwise had similar climate, vegetation, and topography. There were no site differences in concentrations of N and S for either litter or soil. Concentrations of litter P and soil‐extractable P were greater for the andesite (igneous rock) site than for two sites on different sedimentary rocks; however, concentrations of several other litter and soil P fractions did not differ among sites. Patterns in soil P fractions suggested advanced soil development to the point that parent material has little control of P dynamics. Litter samples from each site, leached in the laboratory, released similar amounts of N, P, and S to the soil, indicating no differences in rates of turnover in the litter and in fluxes from litter into the mineral soil among sites. I expected more site differences in soil nutrient dynamics given vastly different parent materials and soil types (i.e., Oxisol vs. Alfisol) and very shallow soil on BCI that brings the parent material close to the plant root zone. Erosion and soil mixing may explain the uniformity in soil nutrient dynamics across the sites.     

Symbiotic Relationships of Legumes and Nodule Bacteria on Barro Colorado Island,Panama: A Review

New data on 129 bacterial isolates were analyzed together with prior samples to characterize community-level patterns of legume–rhizobial symbiosis on Barro Colorado Island (BCI), Panama. Nodules have been sampled from 24 BCI legume species in 18 genera, representing about one quarter of the legume species and one half of the genera on the island. Most BCI legumes associated exclusively with nodule symbionts in the genus Bradyrhizobium, which comprised 86.3% of all isolates (315 of 365). Most of the remaining isolates (44 of 365) belonged to the β-proteobacterial genus Burkholderia; these were restricted to two genera in the legume subfamily Mimosoideae. Multilocus sequence analysis indicated that BCI Bradyrhizobium strains were differentiated into at least eight lineages with deoxyribonucleic acid divergence of the same magnitude as found among currently recognized species in this bacterial genus. Two of these lineages were widely distributed across BCI legumes. One lineage was utilized by 15 host species of diverse life form (herbs, lianas, and trees) in 12 genera spanning two legume subfamilies. A second common lineage closely related to the taxon B. elkanii was associated with at least five legume genera in four separate tribes. Thus, BCI legume species from diverse clades within the family frequently share interaction with a few common lineages of nodule symbionts. However, certain host species were associated with unique symbiont lineages that have not been found on other coexisting BCI legumes. More comprehensive sampling of host taxa will be needed to characterize the overall diversity of nodule bacteria and the patterns of symbiont sharing among legumes in this community.     

Population ecology of the white-nosed coati (Nasua narica) on Barro Colorado Island, Panama

The white-nosed coati, Nasua narica , is a common Neotropical carnivore with a social structure of band-living adult females and solitary adult males. A coati population on Barro Colorado Island, Panama, was studied over a four-year period by mark-recapture, radiotelemetry. and direct observation of habituated individuals. The population density was approximately 51.5 individuals/km² and the sex ratio was 1:1. Band size varied from six to 26 individuals (mean = 15.3) with extensive fluctuation within and between years. Mean foraging group size was smaller (7.2 individuals) than population group size, and fluctuated with food availability, synchronous parturition, and the emigration of mature males. Mean home-range size of six bands was 0.33 km², and ranges of adjacent bands overlapped from 0–66%. One band fissioned during the study; however, the resulting bands did not disperse from the original home range. Seven adult males had a mean home-range size of 0.37 km², each extensively overlapping the home ranges of several other males. Observations of 10 adult males whose natal bands were known indicate that when males disperse they do not simultaneously leave the band's home range. Rather, their home ranges remain within or broadly overlapping those of their natal bands. This dispersal pattern is unusual within the order Carnivora.     

Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island, Panama

Sequences of 16S rRNA and partial 23S rRNA genes and PCR assays with genotype-specific primers indicated that bacteria in the genus Burkholderia were the predominant root nodule symbionts for four mimosoid legumes (Mimosa pigra, M. casta, M. pudica, and Abarema macradenia) on Barro Colorado Island, Panama. Among 51 isolates from these and a fifth mimosoid host (Pithecellobium hymenaeafolium), 44 were Burkholderia strains while the rest were placed in Rhizobium, Mesorhizobium, or Bradyrhizobium. The Burkholderia strains displayed four distinct rRNA sequence types, ranging from 89% to 97% similarity for 23S rRNA and 96.5-98.4% for 16S rRNA. The most common genotype comprised 53% of all isolates sampled and was associated with three legume host species. All Burkholderia genotypes formed nodules on Macroptilium atropurpureum or Mimosa pigra, and sequencing of rRNA genes in strains re-isolated from nodules verified identity with inoculant strains. Sequence analysis of the nitrogenase alpha-subunit gene (nifD) in two of the Burkholderia genotypes indicated that they were most similar to a partial sequence from the nodule-forming strain Burkholderia tuberum STM 678 from South Africa. In addition, a PCR screen with primers specific to Burkholderia nodB genes yielded the expected amplification product in most strains. Comparison of 16S rRNA and partial 23S rRNA phylogenies indicated that tree topologies were significantly incongruent. This implies that relationships across the rRNA region may have been altered by lateral gene transfer events in this Burkholderia population.     

Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama

Habitat fragmentation may influence genetic variability through reductions in population size and the physical isolation of conspecifics. We explored the effects of these factors on genetic diversity in a population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island (BCI), Panama. The study population was established in 1914 when an unknown number of resident individuals were isolated from the surrounding mainland by damming of the Río Chagres to create the Panama Canal. Analyses of 10 microsatellite loci indicated that, despite this isolation, the howler monkeys on BCI exhibit levels of genetic diversity (H _S = 0.584 ± 0.063) among the highest reported for any species of Alouatta. These data also revealed that although relatedness among adults in a social group was significantly greater than zero, the BCI population is not highly genetically structured. Tests for genetic bottlenecks based on departures from equilibrium expectations failed to reveal evidence of a recent reduction in population size. In contrast, coalescent modeling indicated that this population has likely experienced a marked decline within the last few 100 years. These findings generate new insights into the genetic structure of A. palliata and suggest that while the formation of BCI may not have substantially reduced genetic variation in these animals, genetic diversity has been influenced by historical changes in population size.     

Comparative ecophysiology of CAM and C3 bromeliads. I. The ecology of the Bromeliaceae in Trinidad

Abstract This article deals with the physiological ecology of the Bromeliaceae, a large neotropical family containing both terrestrial and epiphytic forms, as well as many species with crassulacean acid metabolism (CAM). The article is in two parts. In the first, we review what is known of the occurrence of CAM and C₃ species in the Bromeliaceae. The photosynthetic pathways are discussed in the context of the major taxonomic divisions within the family and the great diversity of bromeliad life-forms. Of the three subfamilies, the Pitcairnioideae contain both C₃ and CAM species and are essentially all terrestrial. In contrast, the Tillandsioideae are entirely epiphytic or saxicolous, with CAM species being restricted to the genus Tillandsia, And in the Bromelioideae all species show CAM, but terrestrial and epiphytic forms are found in about equal numbers. The evidence suggests that both CAM and the epiphytic habit arose more than once in the family's evolutionary history. In the second part we consider the photosynthetic ecology of the various bromeliad life-forms in more detail using the specific example of Trinidad (West Indies). CAM bromeliads tend to be centred on the drier regions of the island and C₃ forms on the wetter areas. However, at any one site there is a marked vertical stratification of species within the forest profile. Based on the known habitat preferences of the bromeliads, six contrasting sites were selected for field studies in Trinidad. These ranged from arid coastal scrub to montane rain forest, the vegetational and climatic characteristics of which are described here. The constancy of δ¹³C values (carbon-isotope ratios) for individual CAM species in these markedly different habitats emphasized the need for ecophysiological studies to characterize environmental effects on CO₂ assimilation and transpiration. The following papers in this series present the results of a comparative investigation of gas exchange and leaf water relations of CAM and C₃ bromeliads in situ at the various sites.     

A new method for censusing animal populations: The number of Eciton burchelli army ant colonies on Barro Colorado Island,Panama

Summary A new technique for estimating the size of an animal population is described. This technique is used to provide an up to date estimate of the number of colonies of the army ant Eciton burchelli on Barro Colorado Island, Panama. There have been approximately 50 colonies of this species on Barro Colorado Island for more than thirty years. The relative constancy of this population is contrasted with the great temporal variability of other tropical insect populations.     

The cost of defeat: Capuchin groups travel further,faster and later after losing conflicts with neighbors

Although competition between social groups is central to hypotheses about the evolution of human social organization, competitive interactions among group‐mates are thought to play a more dominant role in shaping the behavior and ecology of other primate species. However, few studies have directly tested the impact of intergroup conflicts in non‐human primates. What is the cost of defeat? To address this question, the movements of six neighboring white‐faced capuchin (Cebus capucinus) social groups living on Barro Colorado Island, Panama were tracked simultaneously using an Automated Radio Telemetry System (ARTS), for a period of six months. Groups moved 13% (441 m) further on days they lost interactions compared with days they won interactions. To cover these larger distances, they traveled faster, stopped less frequently, and remained active later in the evening. Defeat also caused groups to alter their patterns of space use. Losing groups had straighter travel paths than winning groups, larger net displacements and were more likely to change their sleeping site. These results demonstrate that losing groups pay increased travel costs and suggest that they forage in low‐quality areas. They provide some of the first direct evidence that intergroup conflicts have important energetic consequences for members of competitively unsuccessful primate social groups. A better understanding of how intergroup competition impacts patterns of individual fitness is thus needed to clarify the role that this group‐level process plays in shaping the evolution of human‐ and non‐human primate behavior. Am J Phys Anthropol 152:79–85, 2013. © 2013 Wiley Periodicals, Inc.     

Spatial genetic structure of Simarouba amara Aubl. (Simaroubaceae), a dioecious, animal-dispersed Neotropical tree, on Barro Colorado Island, Panama

Simarouba amara (Simaroubaceae) is a vertebrate-dispersed, insect-pollinated Neotropical tree found in lowland moist forest from upper Mesoamerica to the Amazon basin. We assessed the spatial genetic structure of S. amara within the 50-ha Forest Dynamics Plot on Barro Colorado Island in the Republic of Panama. A total of 300 individuals were genotyped using five microsatellite loci, representing 100 individuals with a dbh>or=10 cm, 100 individuals of 1-10 cm dbh, and 100 individuals of <1 cm dbh. The 200 individuals in the two larger size classes were also genotyped with 155 AFLP loci. Spatial autocorrelation analysis using Moran's Index detected significant genotypic association at the smallest distance classes for 1-10 cm dbh (0-20 m) and >10 cm dbh (0-40 m) size categories. Significant spatial autocorrelations were detected over larger scales (0-140 m) in <1 cm dbh individuals. The relatively weak genetic structure of S. amara, in comparison to other recent studies, may be explained by pollen and seed dispersal over the 50 ha plot, overlapping seed shadows, and postrecruitment mortality.