Article

Plant conservation in the Mesoamerican biodiversity hotspot: a case study on the Piper genus in Veracruz (Mexico)

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Abstract

Maintaining floristic diversity in recognized biodiversity hotspots is a priority for ecosystem conservation. However, different taxonomical treatments often lead to over or underestimation of floristic diversity in species-rich groups, in particular in Tropical regions as Mesoamerica where floristic surveys are less detailed. Also, understanding the effects of climate changes on species distribution is an emerging question of conservation biology and ecological studies. Here, we used the species-rich genus Piper (Piperaceae) in Veracruz, as a model system to compare reported and actual species richness and to model their occurrence under a climate change scenario. We compared morphological characters of specimens preserved in three of the main Mexican herbaria and then applied new taxonomical treatments. We also used environmental niche models (ENMs) as implemented in Maxent to detect the effects of climate changes on species with different levels of habitat specificity and with specialized biotic interactions. We found that from a total of 108 Piper species reported in Veracruz, 80 were consistent to the new taxonomical treatments due to synonymy or misidentification. ENMs showed that the main determinants of Piper distribution are linked to temperature and precipitations depending on the species. Therefore, different species are likely to respond differently to climate changes. As expected, species with higher habitat specificity and species exhibiting specialized mutualisms are more likely to experience niche contractions. This study shows the importance of reconsidering species richness and of modelling species distribution including specialized ecological interactions as prerequisite for establishing conservation criteria.

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En anticipo al tratamiento detallado del género Piper L. en Honduras proveemos un nomenclátor que incluye el nombre, la cita bibliográfica de referencia y la información del tipo para cada especie aceptada. Al momento se reconocen 45 taxones con más de 100 nombres (a nivel de especie y abajo) listados en sinonimia, 58 de los cuales son nuevos. Se provee la lectotipificación para los siguientes taxones para los cuales el tipo no fue asignado al tiempo de su publicación: Piper cobanense Trelease, P. cyclophyllum Trelease, P. gracillimum Trelease, P. perinaequilongum Trelease, P. telanum Trelease, P. triumphale Trelease, P. wilsonii Trelease y P. yzabalanum C. DC. var. pubinerve Trelease.
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Phyllostomide bats are the most important consumers of Piper fruits in the Neotropics (Heithaus et al. 1975) and, in particular, Carollia perspicillata and Glossophaga soricina are the species which demonstrate distinct preferences for these fruits (Charles-Dominique 1991, Fleming 1981, Fleming et al. 1977, Marinho-Filho 1991, Palmeirim el al. 1989). This is also true of Piper arboreum Aubl. (Piperaceae) in the gallery forests of Central Brazil (Bizerril & Raw 1997).
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Aim Predictive models of species’ distributions use occurrence records and environmental data to produce a model of the species’ requirements and a map of its potential distribution. To determine regions of suitable environmental conditions and assess biogeographical questions regarding their ranges, we modelled the potential geographical distributions of two spiny pocket mice (Rodentia: Heteromyidae) in northwestern South America. Location North-western South America. Methods We used the Genetic Algorithm for Rule-Set Prediction (GARP), environmental data from GIS maps and georeferenced collection localities from a recent systematic review of Heteromys australis and H. anomalus to produce the models. Results GARP models indicate the potential presence of H. australis throughout mesic montane regions of north-western South America, as well as in some lowland regions of moderately high precipitation. In contrast, H. anomalus is predicted to occur primarily in drier areas of the Caribbean coast and rain-shadowed valleys of the Andes. Conclusions The models support the disjunct status of the population of H. australis in the Cordillera de Mérida, but predict a continuous distribution between known populations of H. anomalus in the upper Magdalena Valley and the Caribbean coast. Regions of suitable environmental conditions exist disjunct from known distributional areas for both species, suggesting possible historical restrictions to their ranges. This technique holds wide application to other study systems.
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It is commonly assumed that the geographical distributions of plants are governed mainly by abiotic variables. However, interactions with other organisms, such as pollinators, also have the potential to influence plant distributions. To investigate this, we developed niche models for 32 plant taxa that have specialized pollination systems and which are native to a biodiversity hotspot (South Africa). We found that the distributions of these taxa are best explained by a combination of biotic (pollinators) and abiotic factors, rather than by abiotic factors alone. For approximately 66% of these plant taxa, pollinator distributions were the factor that provided the best predictor of their niches. Furthermore, co-occurrence of these plants and their pollinators was generally not explained solely by shared abiotic niches, and thus probably reflects broad-scale positive ecological interactions. These results are consistent with the proposal that pollinator distributions may constrain plant distributions and highlight the general potential for species distributions to be shaped by positive interactions with other species. This has important consequences for predicting how distributions of species might change in the face of loss of their key mutualists. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
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Five Costa Rican species of Piper (Piperaceae) co-occur in evergreen forest sites at Santa Rosa National Park, Costa Rica. The species were found to have distinctive spatial distribution patterns with two species (Piper marginatum and P. pseudofuligineum) occurring in early successional sites and the others, P. amalago, P. jacquemontianum, and P. tuberculatum, occurring in less disturbed sites in dry forest, evergreen forest, and riparian forest, respectively. These habitat differences are associated with differences in seed and seedling biology and seasonal changes in the foraging behavior of the chiropteran seed dispersers of these plants. Excluding the uncommon P. tuberculatum, overall pairwise spatial overlap, measured by Pianka's (1974) symmetrical index, averaged 0.61. Relatively low phenological overlap allows the species to share animal visitors. Average pairwise flowering overlap (0.13) was about one-half the value of pairwise fruiting overlap (0.22). Responses to different rainfall cues and/or different inflorescence growth rates produce temporally separated phenological cycles. However, results of computer simulations suggest that observed phenological overlap was neither significantly lower nor significantly higher than expected by chance, for most pairs of species. Insect visitation is necessary for high seed-set, and species differ in their attractiveness to pollinators. Pairwise insect overlap (0.59) was greater than expected by chance, however. The plants also utilize the same six species of frugivorous bats as seed dispersers, and pairwise bat overlap was extremely high (0.96). Because they are important fruit sources for three common bat species, Piper species are keystone mutualists in dry tropical forests.
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I tested the hypothesis that body size significantly influences diet and habitat use in frugivorous bats of the genus Carollia (Phyllostomidae) by studying pairs or triplets of species in two Costa Rican habitats and by supplementing these data with published data from one Panamanian locality. I predicted that with an increase in body size, average size of fruit consumed increases, nutritional quality of fruit consumed decreases, and proportion of time spent feeding in second growth decreases. At each site, the smallest species of Carollia was the most common species in second-growth habitats, and its diet contained a higher proportion of nutritionally rich Piper fruits and a lower proportion of large fruits than that of larger species. A multivariate ecomorphological analysis indicated that sympatric Carollia species are similarly arrayed in niche space in wet and dry tropical forests and that sister species are farther apart in niche space than are nonsister species.
Chapter
This chapter describes variation in species composition, density, climbing mechanisms and dispersal syndromes of lianas across four principal forest types of peninsular India. The forest types include: wet evergreen forest (WEF), semi-evergreen forest (SEF), seasonal dry forest (SDF), and dry evergreen forest (DEF). The chapter compares the characteristics of Indian lianas to those reported for other forests around the world. It presents a table that summarizes the details of the 40 study sites, including the forest type, altitude, the forest stature, the mean annual rainfall, the length of the dry season and the sample design. The distribution of lianas in the four forest types showed a pronounced dominance by a limited subset of species. Five climbing mechanisms were employed by lianas in the four forest types. The lianas of SDF and DEF sites displayed four different climbing mechanisms.
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Understanding the processes determining species range limits is central to predicting species distributions under climate change. Projected future ranges are extrapolated from distribution models based on climate layers, and few models incorporate the effects of biotic interactions on species' distributions. Here, we show that a positive species interaction ameliorates abiotic stress, and has a profound effect on a species' range limits. Combining field surveys of 92 populations, 10 common garden experiments throughout the range, species distribution models and greenhouse experiments, we show that mutualistic fungal endophytes ameliorate drought stress and broaden the geographic range of their native grass host Bromus laevipes by thousands of square kilometres (~ 20% larger) into drier habitats. Range differentiation between fungal-associated and fungal-free grasses was comparable to species-level range divergence of congeners, indicating large impacts on range limits. Positive biotic interactions may be underappreciated in determining species' ranges and species' responses to future climates across large geographic scales.
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Natural-history collections in museums contain data critical to decisions in biodiversity conservation. Collectively, these specimen-based data describe the distributions of known taxa in time and space. As the most comprehensive, reliable source of knowledge for most described species, these records are potentially available to answer a wide range of conservation and research questions. Nevertheless, these data have shortcomings, notably geographic gaps, resulting mainly from the ad hoc nature of collecting effort. This problem has been frequently cited but rarely addressed in a systematic manner. We have developed a methodology to evaluate museum collection data, in particular the reliability of distributional data for narrow-range taxa. We included only those taxa for which there were an appropriate number of records, expert verification of identifications, and acceptable locality accuracy. First, we compared the available data for the taxon of interest to the “background data,” comprised of records for those organisms likely to be captured by the same methods or by the same collectors as the taxon of interest. The “adequacy”of background sampling effort was assessed through calculation of statistics describing the separation, density, and clustering of points, and through generation of a sampling density contour surface. Geographical information systems (GIS) technology was then used to model predicted distributions of species based on abiotic (e.g., climatic and geological) data. The robustness of these predicted distributions can be tested iteratively or by bootstrapping. Together, these methods provide an objective means to assess the likelihood of the distributions obtained from museum collection records representing true distributions. Potentially, they could be used to evaluate any point data to be collated in species maps, biodiversity assessment, or similar applications requiring distributional information.
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Orchids are the largest family of flowering plants, encompassing several times as many species as birds or mammals. Because of their diversity, charisma, and threats from overcollection and habitat loss, they are a key group in conservation. Nevertheless, preservation of this group is plagued by taxonomic problems, particularly in Europe, where new taxa are actively being described. We used a checklist of orchids to compare the taxonomic treatment of this family between Europe and neighboring areas to search for geographical patterns. Numbers of invalid, infraspecific, and hybrid names are significantly higher in Europe than in surrounding areas. Recognition of numerous and poorly circumscribed orchid taxa is a serious obstacle to their conservation because rare, poorly defined species may be prioritized for conservation over taxonomically "good" species. This phenomenon may be the result of the popularity of orchids in Europe. We believe that more taxonomic effort should be made in other areas of the world (e.g., the tropics) and on less charismatic groups.
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Field observations on growth form and laboratory observations on structure were made of the root systems of Piper auritum L. (Piperaceae), a small weedy tree colonizing disturbed sites in humid lowland areas of the neotropics. Adventitious roots (prop roots, stilt roots) of P. auritum are dimorphic, with differences in form, structure, and orientation between above-ground and subterranean portions. Above ground the root is wide (mean diameter 1.78 cm), unbranched, and has numerous protoxylem poles (x = 42) around a broad pith (mean diameter 0.72 cm). Upon penetration of the soil the root forms several branch roots, some of which grow vertically and provide anchorage and absorption, while others grow horizontally and produce new shoots (root suckers). Both subterranean types differ from the above-ground root and from each other. Horizontal roots are narrowest (1.01 cm diameter) with the fewest protoxylem poles (9) around the narrowest pith (0.04 cm diameter). Vertical subterranean roots have intermediate values (root diameter 1.06 cm; 22 protoxylem poles; pith diameter 0.44 cm). Vessels are on average wider in the xylem of the horizontal root portions (36 to 84 μm radius) than in either above-ground or vertical subterranean parts of the roots (24 to 60 μm and 36 to 72 μm in radius, respectively), and a greater percentage of total conduction is performed by wider vessel size classes in horizontal sections. Fast-growing vegetative shoots produced from the horizontal portions of the roots result in large stands of P. auritum and allow the species to persist in successional areas no longer favorable for germination of its light-dependent seeds.
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The tropical forest pioneer trees Cecropia obtusifolia and Piper auritum germinate and become established in large light gaps of the forest canopy in the rain forest of south-eastern Mexico. Germination of the seeds of both species is under photocontrol and is triggered when the red: far-red ratio (R: FR) of the incident light increases due to a reduction of the green canopy density. Exposure to simulated light canopies retarded and reduced germination. The light environment inside the forest inhibits germination totally. Experiments with alternate R and FR light treatments indicate the need for long periods of exposure to R light for germination, and demonstrate a strong reversibility of the R light stimulation by FR light in both species. This property of the seeds may be related to the detection of light gap size and its differentiation from the normal sunflecks of the forest.
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Secondary fallow vegetation in parts of the Papua New Guinea lowlands is dominated by the shrub Piper aduncum L. that originates from South America. Here we report on its seed bank, growth rate and biomass accumulation. P. aduncum accounted for 69 % (408 m−2) of the seed bank in the forest and 53 % (1559 m−2) of the seed bank under fallow. About 90 % of the tree seed bank at the fallow site was dominated by P. aduncum whereas this was 78 % in the forest soil. Two-year-old P. aduncum had grown to 4.5 m height and had accumulated 48 Mg dry matter (DM) per ha of above ground biomass. The rate of biomass accumulation increased from 10 Mg DM ha−1 y−1 in the first year to 40 Mg DM ha−1 y−1 in the second year when 76 % of the biomass consisted of mainstems. The highest growth rate of 134 kg DM ha−1 d−1 occurred when P. aduncum was 17-mo-old. Aggressive invasion and monospecific stands of P. aduncum are explained by its dominance in the seed bank, fast growth, and high rates of biomass accumulation. P. aduncum is a major competitor to indigenous tree species and presents a threat to Papua New Guinea's rich biodiversity.
Article
Aim We explored the effects of prevalence, latitudinal range and spatial autocorrelation of species distribution patterns on the accuracy of bioclimate envelope models of butterflies.Location  Finland, northern Europe.Methods  The data of a national butterfly atlas survey (NAFI) carried out in 1991–2003 with a resolution of 10 × 10 km were used in the analyses. Generalized additive models (GAM) were constructed, for each of 98 species, to estimate the probability of occurrence as a function of climate variables. Model performance was measured using the area under the curve (AUC) of a receiver operating characteristic (ROC) plot. Observed differences in modelling accuracy among species were related to the species’ geographical attributes using multivariate GAM.Results  Accuracies of the climate–butterfly models varied from low to very high (AUC values 0.59–0.99), with a mean of 0.79. The modelling performance was related negatively to the latitudinal range and prevalence, and positively to the spatial autocorrelation of the species distribution. These three factors accounted for 75.2% of the variation in the modelling accuracy. Species at the margin of their range or with low prevalence were better predicted than widespread species, and species with clumped distributions better than scattered dispersed species.Main conclusions  The results from this study indicate that species’ geographical attributes highly influence the behaviour and uncertainty of species–climate models, which should be taken into account in biogeographical modelling studies and assessments of climate change impacts.
Article
Since the biologically extirpating eruption of Krakatau (Sunda Strait) in 1883, Rakata (Krakatau's remnant) and two closely adjacent islands, Sertung and Panjang, have been colonized by over 200 species of vascular plants. They now carry species-poor mixed tropical forest, including some twenty-three species of Ficus. Data on the sequence of colonization over the last century by twenty-four Ficus species, twenty-three species of volant frugivores, and by agaonid fig-wasps, presumably from the large islands of Java and Sumatra, each some 44 km distant, are summarized. The potential of the volant frugivores as dispersers of fig seeds is assessed, the pollination problems involved in the colonization of islands by figs are reviewed and patterns of colonization by fig species and by their bird and bat dispersers are identified and discussed. In 1930 a new island, Anak Krakatau, emerged from Krakatau's submerged caldera. This active volcano suffered a self-sterilizing eruption in 1952/1953 and has been colonized, under considerable constraint from its own volcanic activity, probably largely from the (selected) species pool present on Rakata, Sertung and Panjang, 2–4 km away. Its vegetation is at an earlier successional stage (grassland and Casuarina woodland) than that of the three older islands, and in 1992 the Casuarina woodland was in an early stage of transition to mixed forest. The colonization of Anak Krakatau by Ficus species, agaonid wasps and volant frugivores over a critical decade (1982–92) is reviewed, including preliminary assessments of the effects of pollinator limitation on four pioneer fig species and indications of a possible effect of the presence of avian raptors, particularly the peregrine falcon, on fig colonization and forest diversification.
Article
Aim The role of biotic interactions in influencing species distributions at macro-scales remains poorly understood. Here we test whether predictions of distributions for four boreal owl species at two macro-scales (10 × 10 km and 40 × 40 km grid resolutions) are improved by incorporating interactions with woodpeckers into climate envelope models. Location Finland, northern Europe. Methods Distribution data for four owl and six woodpecker species, along with data for six land cover and three climatic variables, were collated from 2861 10 × 10 km grid cells. Generalized additive models were calibrated using a 50% random sample of the species data from western Finland, and by repeating this procedure 20 times for each of the four owl species. Models were fitted using three sets of explanatory variables: (1) climate only; (2) climate and land cover; and (3) climate, land cover and two woodpecker interaction variables. Models were evaluated using three approaches: (1) examination of explained deviance; (2) four-fold cross-validation using the model calibration data; and (3) comparison of predicted and observed values for independent grid cells in eastern Finland. The model accuracy for approaches (2) and (3) was measured using the area under the curve of a receiver operating characteristic plot. Results At 10-km resolution, inclusion of the distribution of woodpeckers as a predictor variable significantly improved the explanatory power, cross-validation statistics and the predictive accuracy of the models. Inclusion of land cover led to similar improvements at 10-km resolution, although these improvements were less apparent at 40-km resolution for both land cover and biotic interactions. Main conclusions Predictions of species distributions at macro-scales may be significantly improved by incorporating biotic interactions and land cover variables into models. Our results are important for models used to predict the impacts of climate change, and emphasize the need for comprehensive evaluation of the reliability of species–climate impact models.
Article
To relate differences in phenological strategies of a group of closely related plants to biotic (pollinators, dispersers) and abiotic (water, light) factors, we studied leafing, flowering, and fruiting phenology of 12 species of Piper (Piperaceae) in a neotropical lowland forest in Panama for 28 months. We asked how Piper may partition time and vertebrate frugivores to minimize possible competition for dispersal agents. Based on habitat preferences and physiological characteristics we discriminate between forest Piper species (eight species) and gap Piper species (four species). Forest Piper species flowered synchronously mostly at the end of the dry season. Gap Piper species had broader or multiple flowering peaks distributed throughout the year with a trend towards the wet season. Both groups of Piper species showed continuous fruit production. Fruiting peaks of forest Piper species were short and staggered. Gap Piper species had extended fruiting seasons with multiple or broad peaks. Both groups of Piper species also differed in their time of ripening and disperser spectrum. Forest Piper species ripened in late afternoon and had a narrow spectrum consisting mainly of two species of frugivorous bats: Carollia perspicillata and C. castanea (Phyllostomidae). Fruits of gap Piper species, in contrast, ripened early in the morning and were eaten by a broader range of diurnal and nocturnal visitors, including bats, birds, and ants. We conclude that the differences in flowering phenology of forest and gap Piper species are primarily caused by abiotic factors, particularly the availability of water and light, whereas differences in fruiting patterns are mostly influenced by biotic factors. The staggered fruiting pattern of forest Piper species may reflect competition for a limited spectrum of dispersers. The long and overlapping fruiting periods of gap Piper species are associated with a larger spectrum of dispersers and may be a strategy to overcome the difficulty of seed dispersal into spatially unpredictable germination sites with suitable light conditions.