Keystone Plant Resources Research Articles

Tree visitation and potential seed dispersal of keystone Ficus species by vertebrates in an urban mosaic landscape in eastern South Africa

Globally with the human population increase, urban expansion has increased, impacting biodiversity and ecosystem functions. Visitation of fruiting trees by vertebrate frugivores can influence the persistence of fleshy fruited trees and so further maintain frugivore communities in transformed landscapes. Figs (Ficus spp.) have been recognised as keystone plant resources that support diverse frugivorous vertebrate communities. Our main objective was to identify the frugivorous vertebrates visiting fruiting Ficus trees in an urban mosaic landscape of Durban, Ethekwini Municipality, KwaZulu-Natal, South Africa, using camera traps focused on focal fig trees. We quantified the diurnal and nocturnal frugivore visitation rates and levels of interactions. We analysed frugivore visits to 12 individual trees of five Ficus species between 2019 and 2020. During 3888 h, we recorded a total of 4,071 videos from camera traps with 10,016 visits and levels of interactions of three main vertebrate taxa (8958 fruit bat visits, 808 bird visits and 250 monkey visits). These were in five Ficus species (F. burkei, F. lutea, F. natalensis, F. sur and F. sycomorus). Of the bird species visiting, we identified a total of 34 species, but some species were unidentified. We recorded a total of 8958 visits by Wahlberg's epauletted fruit bats Epomophorus wahlbergi, and 250 visits by vervet monkeys Chlorocebus pygerythrus. The latter tended to stay for prolonged periods in the trees feeding. Our data showed the importance of fruiting fig trees for vertebrate frugivores in the urban mosaic landscape. This highlights the conservation implications of figs as keystone resources in the urban mosaic landscape. Our findings support the planting and conservation of native Ficus tree species in transformed urban mosaic landscapes for the persistence of forest species biodiversity.

Detectability of the Critically Endangered Araucaria angustifolia Tree Using Worldview-2 Images, Google Earth Engine and UAV-LiDAR

The Brazilian Atlantic Forest is a global biodiversity hotspot and has been extensively mapped using satellite remote sensing. However, past mapping focused on overall forest cover without consideration of keystone plant resources such as Araucaria angustifolia. A. angustifolia is a critically endangered coniferous tree that is essential for supporting overall biodiversity in the Atlantic Forest. A. angustifolia’s distribution has declined dramatically because of overexploitation and land-use changes. Accurate detection and rapid assessments of the distribution and abundance of this species are urgently needed. We compared two approaches for mapping Araucaria angustifolia across two scales (stand vs. individual tree) at three study sites in Brazil. The first approach used Worldview-2 images and Random Forest in Google Earth Engine to detect A. angustifolia at the stand level, with an accuracy of >90% across all three study sites. The second approach relied on object identification using UAV-LiDAR and successfully mapped individual trees (producer’s/user’s accuracy = 94%/64%) at one study site. Both approaches can be employed in tandem to map remaining stands and to determine the exact location of A. angustifolia trees. Each approach has its own strengths and weaknesses, and we discuss their adoptability by managers to inform conservation of A. angustifolia.

The community structure of bird assemblages on urban strangler figs

AbstractFigs have been regarded as keystone plant resources that support diverse tropical vertebrate frugivore communities. Planting or conserving large fig trees, such as stranglers, have therefore been proposed for enhancing urban biodiversity. We compared the diversity and community structure of bird assemblages on strangler figs with non‐fig urban trees as well as between the fruiting and non‐fruiting fig trees in an urban setting in Singapore. The total bird abundance across all the fig trees when in fruit was 4.5‐fold higher than on non‐fig trees and 3.5‐fold higher than when the same fig trees were not fruiting, but only attracted two more species. On individual trees, after accounting for the presence of mistletoes, tree height, the area covered by buildings, road lane density, and the distance to natural vegetation, mean diversity was not different between non‐fig trees and fig trees when they were not in fruit. On the other hand, when fruiting, each fig tree on average had 1.4 more species, 3 more counts of non‐native birds, and 1.6 more counts of insectivorous birds than when not fruiting. There was significant compositional turnover between non‐fig trees and non‐fruiting fig trees, while community dispersion was significantly lower among fig trees in fruit. Our results demonstrate that fig trees provide fruit and non‐fruit resources for birds in an urban landscape but do not necessarily support more diverse total bird assemblages than non‐fig trees. Instead, bird communities on fruiting urban figs would be highly homogeneous and dominated by a few species.Abstract in Malay is available with online material.

Isolation and characterization of microsatellites for the neotropical dioecious palm Chamaedorea tepejilote (Arecaceae) and cross-amplification in other Chamaedorea species.

Palms are important components of tropical and subtropical ecosystems and have even been considered keystone plant resources that can support a large array of pollinators and frugivores. Palms are also economically important. Chamaedorea tepejilote Liebm. is a widely distributed palm with important bioeconomic potential for food, traditional medicine and ornamental purposes. Eighteen microsatellite primers were developed for C. tepejilote. Polymorphism and genetic diversity were evaluated in 71 individuals from four populations in Costa Rica. Thirteen loci were polymorphic and the number of alleles in the pooled sample ranged between 5 and 20, the average number of alleles was 10.61. Average observed heterozygosity was Ho=0.607±0.04 (SD) and the average expected heterozygosity was He=0.600±0.03. The exclusion probability of the combined 13 loci, was PE=0.998. We tested transferability of the markers in the congeneric C. costaricana, C. pinnantifrons and C. macrospadix. Dioecious species are common in tropical forests; however, few studies have analyzed gene flow patterns in these species. The markers developed for C. tepejilote are an important tool to quantify gene flow patterns and the distribution of genetic diversity within populations. This information will be useful for the development of conservation and management practices of this dioecious tropical palm species.

Searching for keystone plant resources in fruit‐frugivore interaction networks across the Neotropics

AbstractIdentifying keystone plant resources (KPR) is a contentious issue in ecology and conservation. Despite recent advances provided by mutualistic networks, we still lack studies addressing large‐scale identification of keystone plants. We developed a novel quantitative framework for the large‐scale identification of KPR that combines centrality and effects of simulated removals on networks properties. We built a database with 38 fruit–frugivore networks comprising 6,180 pairwise interactions from Neotropical forest and non‐forest ecosystems ranging from sea level to 2,500 m a.s.l.. Effects of random removal simulations and removal of keystone taxa candidates on nestedness, modularity and niche overlap were assessed. Furthermore, we tested whether changes in network descriptors responded to both latitudinal and elevational gradients. From a total of 373 genera on networks, only species in six genera were ranked as keystone candidates. The simulated removal of species in Miconia (Melastomataceae), Cecropia (Urticaceae) and Byrsonima (Malpighiaceae) led to significant changes in nestedness, modularity and niche overlap, suggesting that these plants play important roles in maintaining the structure of Neotropical fruit–frugivore interaction networks, regardless of latitude or elevation. Our results confirm the keystone role of previously recognized taxa, recognize overlooked ones, providing support for their role at a biogeographical scale, and partially challenge taxa traditionally identified as keystone resources for frugivores. Our study has implications for conservation and restoration of Neotropical ecosystems and provides a new framework for large‐scale identification of keystones in other types of ecological networks.Abstract in Spanish is available with online material.

Floristic Diversity of Nawabganj Bird Sanctuary – A Wetland in Upper Gangetic Plains of Uttar Pradesh, India

This paper reports qualitative and quantitative floristic analysis of composition, diversity and nature of plant communities occurring in the Nawabganj Bird Sanctuary, Uttar Pradesh (India), based on survey, identification and quantification. The keystone plant resources are Acacia nilotica and Prosopis juliflora located in the three islands of the central pond which act as nest-site resources by the Asian openbill storks, the most dominant and regular migratory birds and integral components for sanctuary sustenance.

Identifying keystone plant resources in an Amazonian forest using a long-term fruit-fall record

Abstract:The keystone plant resources (KPR) concept describes certain plant species in tropical forests as vital to community stability and diversity because they provide food resources to vertebrate consumers during the season of scarcity. Here, we use an 8-y, continuous record of fruit fall from a 1.44-ha mature forest stand to identify potential KPRs in a lowland western Amazonian rain forest. KPRs were identified based on four criteria: temporal non-redundancy; year-to-year reliability; abundance of reproductive-size individuals and inferred fruit crop size; and the variety of vertebrate consumers utilizing their fruit. Overall, seven species were considered excellent KPRs: two of these belong to the genusFicus, confirming that this taxon is a KPR as previously suggested.Celtis iguanaea(Cannabaceae) – a canopy liana – has also been previously classified as a KPR; in addition,Pseudomalmea diclina(Annonaceae),Cissus ulmifolia(Vitaceae),Allophylus glabratus(Sapindaceae) andTrichilia elegans(Meliaceae) are newly identified KPRs. Our results confirm that a very small fraction (<5%) of the plant community consistently provides fruit for a broad set of consumers during the period of resource scarcity, which has significant implications for the conservation and management of Amazonian forests.

Avian frugivory inMiconia(Melastomataceae): contrasting fruiting times promote habitat complementarity between savanna and palm swamp

Abstract:Species ofMiconiaare considered keystone plant resources for frugivorous birds in Neotropical forests, but for other ecosystems little of their ecological role is known. The fruiting phenology and the composition of frugivores of fourMiconiaspecies in savanna and palm swamp from the Brazilian Neotropical savanna were studied in three sites from November 2005 to May 2011. The hypothesis tested was that plants from different habitats share their frugivores and consequently promote links between habitats. Through focal plant observations (30–50 h per species in each site), 668 visits by 47 species of birds were recorded and plants from different habitats shared most of the frugivores (49–97%). The fruiting ofMiconia chamissoisin the palm swamp during the period of fruit scarcity (dry season) was accompanied by an enhancement in the frugivore bird richness and abundance in this habitat, providing indirect evidence of resource tracking. Bird species which primarily dwell in savanna recorded consuming fruits in palm swamps during the resource-scarce season is taken as evidence of landscape supplementation.Miconiaassemblage studied here seems to promote a link between two adjacent habitats in the Neotropical savanna from Central Brazil, a link which is likely to be common in this naturally patchy ecosystem.

PARROT NESTING IN SOUTHEASTERN PERU: SEASONAL PATTERNS AND KEYSTONE TREES

Parrots that inhabit tropical lowland forests are difficult to study, are poorly known, and little information is available on their nesting habits, making analysis of community-wide nesting patterns difficult. I present nesting records for 15 species of psittacids that co-occur in southeastern Peru. The psittacid breeding season in this area lasted from June to April, with smaller species nesting earlier than larger species. Why smaller species bred earlier is uncertain, though it may be related to interspecific competition for nest sites or variations in food availability. This study identified two keystone plant resources used by nesting parrots: Dipteryx micrantha (Fabaceae) and Mauritia flexuosa (Arecaceae). Local threats to these plant species are discussed.

Fragmentation Effects on Diversity of Wasp Community and Its Impact on Fig/Fig Wasp Interaction in Ficus racemosa L.

Abstract: Habitat fragmentation usually results in alteration of species composition or biological communities. However, little is known about the effect of habitat fragmentation on the fig/fig wasp system. In this study, we compared the structure of a fig wasp community and the interaction between figs and fig wasps of Ficus racemosa L. in a primary forest, a locally fragmented forest and a highly fragmented forest. Our results show that, in the highly fragmented forest, the proportion of pollinator wasps is lower and the proportion of non-pollinator wasps is higher compared with the primary forest and locally fragmented forest. The proportion of fruits without pollinator wasps in mature fruits is also greatly increased in the highly fragmented forest. The proportion of galls in all female flowers increases in the highly fragmented forest, whereas the proportion of viable seeds does not change considerably. The disruption of groups of fig trees results in a decrease in pollinator wasps and even might result in the extinction of pollinator wasps in some extreme cases, which may transform the reciprocal interaction between figs and fig wasps into a parasite/host system. Such an effect may lead to the local extinction of this keystone plant resource of rain forests in the process of evolution, and thereby, may change the structure and function of the tropical rain forest. ( Managing editor: Ya-Qin HAN)

Fig wasp dispersal and the stability of a keystone plant resource in Borneo.

The stability of interactions in remaining rainforest fragments is an issue of considerable concern for conservation. Figs are a pre-eminent tropical keystone resource because of their importance for wildlife, but are dependent on tiny (1-2 mm) species-specific wasps for pollination. To investigate fig wasp dispersal I trapped insects at various heights (5-75 m) in an isolated fragment (ca. 4500 ha) of Bornean rain forest. Fig wasps constituted the majority of captures above the canopy (pollinators 47%, non-pollinators 5%). However, genera were not evenly represented. There were 50% more species of monoecious fig pollinator than there were host species in the fragment, indicating some must have arrived from forests with different assemblages of figs at least 30 km away. Dioecious fig pollinators were poorly represented suggesting more limited dispersal, which could account for higher endemism and vulnerability to catastrophic disturbance in these figs. Diurnal activity and flight height also varied among genera. Most non-pollinating fig wasps were very rare.

Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods

Keystone plants that produce seasonally critical trophic resources comprise one of the main classes of keystone species, yet no studies have attempted to examine the ecological attributes that might help us recognize them and evaluate their importance in species-rich plant assemblages. In this paper the concept of keystone plant resources is reviewed using potential candidates proposed in the literature for neotropical forest sites. A poorly known example of a potential keystone resource—the gums produced by mature pods of two emergent tree species (Parkia nitida and P. pendula, Leguminosae: Mimosoideae)—is described for primates and other arboreal vertebrates in Amazonian forests. In particular, the fruiting phenology, tree density, patterns of vertebrate consumption, and nutritional quality of Parkia gums in Amazonian terra firme forests are considered. Putative neotropical keystone resources are then divided into four intersecting ecological attributes defining their community-wide importance to vertebrate frugivores: (1) temporal redundancy, (2) degree of consumer specificity, (3) reliability, and (4) abundance. From a vertebrate perspective, keystone plants are here defined as those producing reliable, low-redundancy resources that are consumed by a large proportion of the bird and mammal assemblage with which they coexist. Plant populations proposed to date as keystone species range widely across two of these four variables, which may disqualify most putative taxa (including Parkia spp.) from a more formal definition of keystone resources. Other importance attributes, the context-dependent role, the taxonomic refinement, and removal effects of the keystone plant resource concept as applied to tropical forests are also discussed.

The breeding structure of a tropical keystone plant resource

Despite the recognized importance of maintaining viable populations of keystone plant resources in tropical wildlife parks and forested preserves, the critical question of what constitutes effective breeding units of these species has not been directly addressed. Here we use paternity analysis techniques to reconstruct the genotypes of pollen donor trees and to estimate pollen dispersal distances and breeding population size parameters for Panamanian populations of seven species of monoecious strangler figs (Ficus, Moraceae), a particularly widespread and influential group of keystone producers1,2,3. Despite the minute size (1–2 mm) and short lifespan (2–3 d) of the species-specific wasp pollinators (Agaonidae, Chalcidoidea), pollen dispersal was estimated to occur routinely over distances of 5.8–14.2 km between widely spaced host trees. As a result of such extensive pollen movement, breeding units of figs comprise hundreds of intermating individuals distributed over areas of 106–632 km2, an order of magnitude larger than has been documented for any other plant species. Moreover, these results should be generalizable to the 350 or so monoecious fig species that share this pollination system4. The large areal extent of breeding units of these keystone plant resources has important implications for our understanding of both the evolution of tropical biodiversity and its maintenance by applied conservation efforts.

Reproductive and Genetic Consequences of Forest Fragmentation: Two Case Studies of Neotropical Canopy Trees

Large areas of continuous tropical forests are rapidly becoming fragmented as a result of human activities, prompting a growing need for information on the reproductive and genetic responses of tree species to disturbance. Here we review the literature on pollen dispersal in continuous forest stands in order to identify factors expected to enhance or to inhibit interfragment pollen flow. We then describe two empirical studies of the effects of fragmentation on pollen flow in Neotropical populations of Spondias mombin (Anacardiaceae) and five monoecious species of Ficus (Moraceae). In S. mombin, small fragment populations suffered significant reductions in germination rate and fruit production relative to large fragment and continuous forest populations. Nevertheless, 90-100% of the progeny produced in the small fragments were the product of pollen gene flow originating from forest stands located over 80-1000 m away. In contrast to S. mombin, which is relatively abundant and pollinated by a variety of small insects, the strangler fig species studied were relatively rare and pollinated by species-specific wasps that are both small and short-lived. Paternity analyses revealed these highly coevolved pollinators to be effective agents of pollen movement over very long distances, routinely dispersing 6-14 km to receptive host trees. Because of such extensive pollen flow, breeding populations of figs were estimated to consist of hundreds of intermating individuals distributed over 108-632 km2, an area substantially larger than has been documented for any other plant species. The observed patterns of dispersal in S. mombin and Ficus demonstrate the potential for ecologically and evolutionarily significant pollinator and pollen movement among populations occurring in both disturbed and continuous forest environments. Moreover, given the integral relationship of figs, as keystone plant resources, to other plant and animal species, the extensive spatial scale of fig breeding units demonstrates how the conservation of biodiversity in spatially isolated reserves may be dependent on the preservation of forest elements in a surrounding fragmented landscape.

Ingestion of Ficus enormis seeds by howler monkeys (Alouatta fusca) in Brazil: effects on seed germination

Figs (Ficus spp.) have been considered keystone resources for Neotropical frugivores. Such keystone plant resources are characterized by playing important roles in sustaining frugivores through periods of general food scarcity (Terborgh 1986). Many birds and mammals consume figs and disperse their seeds (e.g. Coates-Estrada & Estrada 1986). Howler monkeys (Alouatta spp., Cebidae) are important consumers of figs (Milton 1980). Although it has been accepted that frugivores allow the passage of fig seeds undamaged through their digestive tracts (Janzen 1979, but see Janzen 1981), few quantitative studies exist on the effect of dispersers upon the germination of fig seeds (Coates-Estrada & Estrada 1986, Midya & Brahmachary 1991, Utzurrum & Heideman 1991). Here I report the effect of brown howlers (Alouattafusca Geoffroy) on the germination success of Ficus enormis (Mart. ex Miq.) Miq. This fig species is a strangler tree reaching heights of approximately 15 m, and producing globe syconia (12.70 ?1.02 mm long, 12.82 ?1.19 mm wide, N = 30) which turn brown when mature. Field observations were conducted in the Reserva de Santa Genebra, a tropical upland semideciduous forest (Morellato 1991) in Campinas, Sdo Paulo (220 49' S 470 07' W) between April and June 1992. Ficus enormis fruits at this site are consumed mainly by Alouattafusca, Cebus apella, Artibeus lituratus, Sciurus ingrami (Galetti 1992), and the toucan Ramphastos toco Muller (pers. obs.). Primate faecal samples were collected from the forest leaf litter, mostly below one single fig tree. Seeds used in the germination tests were selected at random from the faeces defecated by a group of five howler monkeys. Seeds used in control germination trials were also randomly chosen from fruits dropped to the ground during primate feeding bouts in the fig crown. The seeds were sown on

Predation on palm nuts ( Syagrus romanzoffiana) by squirrels ( Sciurus ingrami) in south-east Brazil

Although Terborgh (1986) suggested that palm nuts are a 'keystone plant resource' for frugivore communities in tropical forests, few studies exist on seed ecology of palm fruit crop (Bradford & Smith 1977, Pifiero etal. 1984, Vandermeer et ali. 1979). Janzen (1983) suggested that seed predators have a major impact on the structure of plant communities in tropical forests. Squirrels are regarded as important seed dispersers and seed predators (Glanz et ail. 1982, Janzen 1972) depending on the habitat and the fruit availability. These rodents frequently consume hard nuts and their distribution may be related to the distribution of food sources such as palms (Glanz 1982). This paper investigates the utilization of the fruits of the 'geriva', ySyagrus romnanZoffiana (Cham.) Glassmnan by squirrels in a tropical upland semideciduous forest in south-east Brazil. Field observations were made from August 1988 to May 1990 in the 250 ha Santa Genebra Reserve in Campinas (22? 49' S, 470 07' W), Sao Paulo State, Brazil. The climate of the region is characterized by one dry (April to September) and one rainy (October to March) season; annual rainfall during the study period was 1366 mm. The feeding assemblage that utilizes Sjyagruis fruits in Santa Genebra is composed of squirrels Seiinrus ingrami Thomas, a small species about 34 cm in length (H. Bergallo, unpub.), capuchin monkeys Cebus apella Linne and brown howler monkeys Aloucattafiusca Ihering. &yagrus rotinanzofJiana is a common palmi in semideciduous forests in south-east Brazil (H. F. Leitao-Filho, pers. comm.). The fruit is an ovoid drupe 2.5 cm in diameter, with a soft exocarp and woody endocarp. Individuals of this species produce fruit all the year round, each plant producing two bunches at a timie.

Are Figs Always Keystone Resources for Tropical Frugivorous Vertebrates? A Test in Gabon

This paper evaluates the suggestion of Terborgh (1986) that figs constitute “keystone plant resources” for frugivorous mammals and birds in African rain forests as they appear to do in South America and Asia. From studies of the diets of monkeys and other mammals and birds in Gabon, we show that figs are infrequently eaten by most species, and are always eaten in small amounts. Figs in Gabon occur at very low densities and have unpredictable fruiting patterns and relatively low crown production. Thus, fig fruits are not staple foods and cannot sustain most populations of frugivorous species during periods of low fruit availability. In Gabon, monkeys and large birds depend on the fruit of two species of Myristicaceae and of one species of Annonaceae. These regularly bear ripe fruit during the lean period and are abundantly consumed. Figs occur in such distant patches that they are mainly fed on by wide—ranging animals such as large frugivorous bats.