Phenological diversity in tropical forests

One of the most intriguing and complex characteristics of reproductive phenology in tropical forests is high diversity within and among forests. To understand such diversity, Newstrom et al. provided a systematic framework for the classification of tropical flowering phenology. They adopted frequency and regularity as criteria with priority, and classified plants in La Selva, Costa Rica, where most plants reproduced more than once a year irregularly. Many other studies have demonstrated annual cycles corresponding to rainfall patterns at the community level in Neotropical forests, including La Selva. On the other hand, supraannual flowering synchronized among various plant species, called general flowering, is known from aseasonal lowland dipterocarp forests in Southeast Asia. Within both forests, a wide spectrum of flowering patterns is found. This range of patterns suggests the great potential of tropical phenological studies to explore the selective pressures on phenology. Various abiotic and biotic factors can be selective agents. The shared pollinators hypothesis suggests that plant species sharing pollinators segregate flowering temporarily to minimize interspecific overlap in flowering times and thus minimize ineffective pollination or competition for pollinators, indicating strong phylogenetic constraints in timing and variation of flowering. Comparison of phenology within and among forests may help our understanding of phenological diversity. Attempts are now being made to develop a common language to communicate concepts and render interpretations of data more compatible among investigators and to create a network to promote comparative studies. Received: September 8, 2000 / Accepted: January 30, 2001     

The phenology of growth and reproduction in plants

The study of phenological aspects of plants involves the observation, recording and interpretation of the timing of their life history events. This review considers the phenology of leafing, flowering and fruit production in a range of species and communities. The selective forces (both abiotic and biotic) that influence the timing of these events are discussed. Within the limits imposed by phylogenetic constraints, the phenological patterns (timing, frequency, duration, degree of synchrony, etc.) of each phase are probably the result of a compromise between a variety of selective pressures, such as seasonal climatic changes, resource availability, and the presence of pollinators, predators and seed dispersers. Many studies on flowering times stress the role of interactions between plant species which share pollinators or predators. The timing of fruiting plays a key role in controlling the abundance and variety of obligate frugivores in many tropical communities. The importance of long-term recording is stressed, particularly in species which fruit irregularly. An understanding of the phenology of plants is crucial to the understanding of community function and diversity.     

Seasonal dietary niche contraction in coexisting Neotropical frugivorous bats (Stenodermatinae)

Tropical dry forests are characterized by punctuated seasonal precipitation patterns that drive primary production and the availability of fruits, seeds, flowers, and insects throughout the year. In environments in which the quantity and quality of food resources varies seasonally, consumers should adjust their foraging behavior to maximize energy intake while minimizing overlap with competitors during periods of low food availability. Here, we investigated how the diets of frugivorous bats in tropical dry forests of NW Mexico varied in response to seasonal availability and how this affected dietary overlap of morphologically similar species. We performed stable isotope analyses to understand temporal and interspecific patterns of overall isotopic niche breadth, trophic position, and niche overlap in the diet of six frugivorous species of closely related New World leaf-nosed bats (family Phyllostomidae, subfamily Stenodermatinae). We estimated seasonal changes in resource abundance in two complementary ways: (a) vegetative phenology based on long-term remote sensing data and (b) observational data on food availability from previously published insect and plant fruiting surveys. In all species, there was a consistent pattern of reduced isotopic niche breadth during periods of low food availability. However, patterns of niche overlap varied between morphologically similar species. Overall, results from our study and others suggest that seasonal food availability likely determines overall dietary niche breadth in Phyllostomidae and that despite morphological specialization, it is likely that other mechanisms, such as opportunistic foraging and spatiotemporal niche segregation, may play a role in maintaining coexistence rather than simply dietary displacement.     

Host-mediated effects on the reproductive phenological asynchrony of a generalist mistletoe in China

一种泛性桑寄生植物繁殖物候异步性的寄主介导效应 寄主介导效应被认为会导致半寄生性的桑寄生植物的繁殖物候异步性，并由此为与桑寄生植物互惠共生的传粉者和种子散布者提供更长时间的食物资源供应，但目前关于此方面的研究还缺乏相关的实证数据。本研究以广泛分布于中国西南西双版纳地区的一种泛性桑寄生科植物五蕊寄生(Dendrophthoe pentandra)为材料，每周监测其开花、结果物候，检测了其开花和结果物候是否呈季节性格局，量化了五蕊寄生繁殖物候的异步程度，并检测了影响该植物始花期早晚的因素。最后，本研究还检验了五蕊寄生繁殖物候的异步性随寄主种类数量变化的效应。研究结果表明：(i)在连续两年的物候观测中五蕊寄 生的花期和果期都呈单峰分布格局；(ii)始花期显著受到植物大小和光照强度的影响，即冠幅越大和受光程度越高的植物个体有更早的始花期和更长的花期和果期；(iii)不同的寄主种类对五蕊寄生的繁殖物候有显著的影响，但与假设相反的是，随着寄主种类数量的增加，五蕊寄生繁殖物候的异步性没有显著提高。这项研究表明，在解释泛性桑寄生植物的繁殖物候异步性及寄主种类的数量对其影响的生态学意义还需进行更深入的探究。     

Flower and Fruit Availability along a Forest Restoration Gradient

Frugivores and pollinators are two functional groups of animals that help ensure gene flow of plants among sites in landscapes under restoration and to accelerate restoration processes. Resource availability is postulated to be a key factor to structure animal communities using restoration sites, but it remains poorly studied. We expected that diverse forests with many plant growth forms that have less‐seasonal phenological patterns will provide more resources for animals than forests with fewer plant growth forms and strongly seasonal phenological patterns. We studied forests where original plantings included high tree species diversity. We studied resource provision (richness and abundance of flowers and fruits) of all plant growth forms, in three restoration sites of different ages compared to a reference forest, investigating whether plant phenology changes with restoration process. We recorded phenological data for reproductive plant individuals (351 species) with monthly sampling over 2 years, and found that flower and fruit production have been recovered after one decade of restoration, indicating resource provision for fauna. Our data suggest that a wide range of plant growth forms provides resource complementarities to those of planted tree species. Different flower phenologies between trees and non‐trees seem to be more evident in a forest with high non‐tree species diversity. We recommend examples of ideal species for planting, both at the time of initial planting and post‐planting during enrichment. These management actions can minimize shortage and periods of resource scarcity for frugivorous and nectarivorous fauna, increasing probability of restoring ecological processes and sustainability in restoration sites.     

Reproductive phenology of a northeast Brazilian mangrove community: Environmental and biotic constraints

Brazil has the third largest area of mangrove in the world, which is widely threatened by anthropogenic pressures. We carried out the first long-term phenological study investigating whether environment and competition for pollinators shape the reproduction of a western mangrove community in Brazil, and provide new information for mangrove conservation. We monitored monthly the flowering and fruiting of Avicennia schaueriana, Conocarpus erectus, Laguncularia racemosa and Rhizophora mangle, the only species composing this mangrove community. We applied circular statistics to detect seasonal trends, null models to test for aggregated, staggered or random flowering patterns, performed correlations between phenophases and climate, and calculated intra-specific phenological synchrony. Each species presented a different flowering pattern, from brief annual to continuous and from regular to irregular, resulting in a bimodal pattern at community level. Fruiting was annual or continuous and seasonally unimodal at community level. Precipitation showed the strongest correlation with reproduction for all species, except L. racemosa. Flowering was randomly distributed among species sharing pollinators and each species presented high intra-specific synchrony. The studied mangrove showed a diversity of flowering patterns despite the low number of species. Annual to sub-annual sequential flowering were prevalent, sustaining the pollinators of species all the year long, while the wind-pollinated species flowered continuously. We provide strong evidence that daylength, rainfall and temperature are driving the flowering and fruiting rhythm of these mangrove species.     

Effects of microtopography and hydrology on phenology of an invasive herb

Phenological traits may influence invasion success via effects on invasiveness of the colonizing species and invasibility of the receiving ecosystems. Many species exhibit substantial fine-scaled spatial variation in phenology and interannual differences in phenological timing in response to environmental variation. Yet describing and understanding this variation is limited by the availability of appropriate spatial and temporal datasets. Remote sensing provides such datasets, but has primarily been used to monitor broad-scale phenological patterns at coarse resolutions, necessarily missing fine spatial detail and intraspecies variation. We used hyperspectral remote sensing to characterize the spatial and temporal phenological variation of the invasive species Lepidium latifolium (perennial pepperweed) at two sites in California's San Francisco Bay/Sacramento–San Joaquin River Delta. Considerable phenological variation was detected: L. latifolium was simultaneously present in vegetative, early flowering, peak flowering, fruiting, and senescent stages in late June; the relative dominance and distribution of these stages varied interannually. Environmental determinants of phenology were investigated with variables derived from the hyperspectral image data, from a high resolution LiDAR (light detection and ranging) digital elevation model (DEM), and from local precipitation and streamflow data. Lepidium latifolium phenology was found to track water availability, and may also be influenced by intraspecific competition and edaphic stress. Lepidium latifolium has a unique phenology (summer flowering) relative to the communities it invades, which may allow invasion of an empty niche. Furthermore, many habitats are invaded by L. latifolium, which occurs in locally appropriate phenologies under the different environmental conditions. The environmental responsiveness of L. latifolium phenology may mediate the wide breadth of invasible habitats.     

Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms

Abstract Biotic pollination is thought to correlate with increased interspecific competition for pollination among plants and a higher speciation rate. In this study we compared patterns of flowering phenology and species richness between abiotically (wind) and biotically pollinated plants, using phylogenetically independent contrasts. We compiled phenological data from eight local seasonal floras, in which we found geographically overlapping sister clades. Of 65 documented origins of wind pollination, we were able to use up to 17 independent contrasts. In contrast to previous studies we found no difference in global species richness between wind- and biotically pollinated sister clades. Regarding phenology, we found wider phenological spread in biotically pollinated clades, earlier flowering onset in wind-pollinated trees, but no difference in duration of flowering between pollination modes. These results corroborate previous views that niche space is more constrained for wind-pollinated species, and that niche partitioning is less important between wind-pollinated plants compared to plants pollinated by animals.     

Marine influence controls plant phenological dynamics in Mediterranean Mexico

Aims To assess the role of moisture in phenological timing in the mediterranean coastal flora of Baja California, and specifically to assess the role of coastal fog and ocean-derived moisture in plant phenology. Moisture seems to be the primary driver of flowering times and durations at the arid end of the mediterranean-climate region, where rainfall is often sporadic (temperature and day length can be expected to play a much lesser role as they are not growth limiting). We aimed to understand: What factors drive climatic variation between sites? Are there general flowering patterns allowing us to identify phenological categories? Do flowering patterns vary in relation to site-specific weather? and most importantly, does maritime influence on weather affect flowering dynamics in coastal mediterranean ecosystems?Methods The southernmost extent of the California Floristic Province (in Baja California, Mexico) is a biological diversity hotspot of high endemism and conservation value, with two steep moisture gradients: rainfall (N–S) and coastal fogs (W–E), providing an ideal study system. We installed five weather stations across the moisture gradients, recording data hourly. We monitored flowering phenology in the square kilometer surrounding each weather station from 2010 to 2013. About 86 plant taxa were monitored across the five sites, every 6–8 weeks. Averaged climatic data is presented with general trends in flowering, and specific flowering syndromes were observed. Data for flowering intensity across the sites was analyzed using a principal components analysis.Important findings Data analysis demonstrates a general seasonal pattern in flowering times, but distinct differences in local weather and phenology between the five study sites. Three flowering syndromes are revealed in the flora: (i) water responders or spring bloomers, (ii) day-length responders or fall-blooming taxa and (iii) aseasonal bloomers with no seasonal affinity. The two moisture gradients are the strongest drivers of flowering times. Inland sites showed higher phenological variation than coastal sites where seasonality is dampened by ocean-derived moisture, which extends and buffers perennial plant phenology and is a probable driver of local endemism. Phenological controls vary globally with climate and geography; moisture is the primary driver of phenology in mediterranean climates and fog is an important climatic variable in coastal Mexico.     

Pollination Ecology of a Pioneer Species: Musa itinerans (Musaceae) in Xishuangbanna,South Yunnan,China

Pollination ecology of Musa itinerans Cheesman (Musaceae), a pioneer species in the tropical rain forest, was explored in Xishuangbanna, South Yunnan, China. This research involved flowering phenology, nectar production, visitation patterns of pollinators and bagging experiments. It was found that (1) flowering of M. itinerans occurred a whole year round with a peak at the early dry season (Nov.) and the daily flowering pattern had two obvious peaks in the early morning and in the late evening, respectively; (2) nectar production occurred at two obvious peaks, during the day and in the night-time (from 8 am to 12 pm, and from 8 pm to 12 am, respectively), which allowed the two different foragers to visit at specific times; and (3) long-tongue fruit bats ( Macroglossus sobrinus ) and sunbirds ( Arachnothera longirostris ) were both effective pollinators of Musa itinerans.     

Flowering phenologies of hummingbird plants from the temperate forest of southern South America: is there evidence of competitive displacement?

Plant species sharing pollinators may compete through pollination. This type of competition may lead to overdispersed flowering phenologies. However, phenological segregation is difficult to detect in seasonal climates. We compared patterns of phenological overlap in assemblages of ornithophilous plants from three localities of the temperate forest of southern South America with those generated by four different null models. These species were all visited and presumably pollinated by a single species, the hummingbird Sephanoides sephaniodes, which makes this situation ideal to evaluate the role of pollination‐mediated competition. For one site, we compiled data on flowering phenologies for three different years. Three models considered the flowering period of the whole assemblage of ornithophilous plants as the phenological window within which flowering phenologies were randomized, but made no further assumptions on how species should be distributed within that temporal frame. The fourth model assigned differential probabilities to different time intervals based on the flowering onset of non‐ornithophilous plant species. Observed mean pairwise overlaps for all localities and years were well within the interval defined by the 2.5 and 97.5% percentiles of the randomized distribution of expected mean pairwise overlaps according to models 1–3. However, model 4 showed a consistent trend towards overdispersion of ornihophilous phenologies, which show a shift towards mid‐ to late‐summer flowering. Thus, to the extent that the distribution of flowering of non‐ornithophilous species reflects the constraints imposed by a highly seasonal climate, our results provide support to the proposal that pollinator sharing may cause evolutionary displacement or ecological sorting of flowering phenologies. Other factors, such as phylogenetic inertia, could also contribute to explain extant phenological patterns in the highly endemic ornithophilous flora of the temperate forest of southern South America.     

Ornithophilous and Chiropterophilous Pollination in Musa itinerans (Musaceae), a Pioneer Species in Tropical Rain Forests of Yunnan, Southwestern China1

The role of bats and sunbirds in the pollination ecology of Musa itinerans Cheesman (Musaceae) was studied in the tropical seasonal rain forests of Xishuangbanna, southern Yunnan, China. It was found that both long–tongued fruit bats (Macroglossus sobrinus) and sunbirds (Arachnothera longirostris) were effective pollinators of M. itinerans. Nectar production had two peaks, one during the day and one during night (0800–1200 h and 2000–2400 h), which allowed the two different foragers to visit at specific times. The visitation patterns of the two foragers coincided with both flowering time and nectar production. By measuring the differences in fruit weight and seed production among different bagging experiments, we found that birds and bats were equally effective as pollinators of this species.     

Annual cycles are the most common reproductive strategy in African tropical tree communities

We present the first cross‐continental comparison of the flowering and fruiting phenology of tropical forests across Africa. Flowering events of 5446 trees from 196 species across 12 sites and fruiting events of 4595 trees from 191 species across 11 sites were monitored over periods of 6 to 29 years and analyzed to describe phenology at the continental level. To study phenology, we used Fourier analysis to identify the dominant cycles of flowering and fruiting for each individual tree and we identified the time of year African trees bloom and bear fruit and their relationship to local seasonality. Reproductive strategies were diverse, and no single regular cycle was found in >50% of individuals across all 12 sites. Additionally, we found annual flowering and fruiting cycles to be the most common. Sub‐annual cycles were the next most common for flowering, whereas supra‐annual patterns were the next most common for fruiting. We also identify variation in different subsets of species, with species exhibiting mainly annual cycles most common in West and West Central African tropical forests, while more species at sites in East Central and East African forests showed cycles ranging from sub‐annual to supra‐annual. Despite many trees showing strong seasonality, at most sites some flowering and fruiting occurred all year round. Environmental factors with annual cycles are likely to be important drivers of seasonal periodicity in trees across Africa, but proximate triggers are unlikely to be constant across the continent.     

西双版纳先锋植物野芭蕉的传粉生态学研究

Pollination ecology of Musa itinerans Cheesman (Musaceae), apioneer species in the tropical rain forest, was explored in Xishuangbanna, South Yunnan, China. This research involved flowering phenology, nectar production, visitation patterns of pollinators and bagging experiments. It was found that (1) flowering of M. itinerans occurred a whole year round with a peak at the early dry season (Nov.) and the daily flowering pattern had two obvious peaks in the early morning and in the late evening, respectively; (2) nectar production occurred at two obvious peaks, during the day and in the night-time (from 8 am to 12 pm, and from 8 pm to 12 am, respectively), which allowed the two different foragers to visit at specific times; and (3) long-tongue fruit bats (Macroglossus sobrinus) and sunbirds (Arachnothera longirostris) were both effective pollinators of Musa itinerans.     

Inter and intraspecific variation on reproductive phenology of the Brazilian Atlantic forest Rubiaceae: ecology and phylogenetic constraints

The reproductive phenology of seven species of Rubiaceae from the Brazilian Atlantic rain forest was compared to evaluate the occurrence of phylogenetic constraints on flowering and fruiting phenologies. Since phenological patterns can be affected by phylogenetic constraints, we expected that reproductive phenology would be similar among plants within a family or genus, occurring during the same time (or season) of the year. Observations on flowering and fruiting phenology were carried out monthly, from December 1996 to January 1998, at Núcleo Picinguaba, Parque Estadual da Serra do Mar, Ubatuba, S?o Paulo State, Brazil. Nine phenological variables were calculated to characterize, quantify and compare the reproductive phenology of the Rubiaceae species. The flowering patterns were different among the seven species studied, and the Kruskal-Wallis test indicated significant differences in flowering duration first flowering, peak flowering and flowering synchrony. The peaks and patterns of fruiting intensity were different among the Rubiaceae species studied and they differed significantly from conspecifics in the phenological variables fruiting duration, fruiting peak date, and fruiting synchrony (Kruskal-Wallis test). Therefore, we found no evidence supporting the phylogenetic hypotheses, and climate does not seem to constrain flowering and fruiting patterns of the Rubiaceae species in the understory of the Atlantic forest.     

Changes in snowmelt date and summer precipitation affect the flowering phenology of Erythronium grandiflorum (glacier lily; Liliaceae)

? Premise of the study: Climate change has affected species worldwide, including alterations in phenology, migration patterns, distribution, and survival. Because Erythronium grandiflorum is an early-season bloomer, alterations in its phenology may have serious implications for many North American Rocky Mountain communities, including changes in resource availability for pollinators and herbivores. ? Methods: We investigated whether changes in the snowmelt date, summer temperature, and summer precipitation have altered the timing and abundance of flowering in E. grandiflorum by collecting long-term data on floral abundance from 1975-2008 in a series of 2 × 2 m plots at the Rocky Mountain Biological Laboratory (RMBL) in Gothic, Colorado in the United States. ? Key results: Snowmelt date and mean summer temperature were negatively correlated. Over the 30-yr study, the snowmelt date advanced by 4.14 d/decade, and mean summer temperature increased by 0.38°C/decade. Summer precipitation was variable, showing no change. The first, peak, and last flowering dates of E. grandiflorum advanced an average of 3.2 d/decade. Furthermore, earlier snowmelt and greater summer precipitation in the previous year led to earlier flowering in E. grandiflorum. There was no change in flowering abundance in this species, indicating it may be controlled by a complex set of abiotic and biotic variables. ? Conclusions: Our study indicates that snowmelt is arriving earlier at the RMBL, which has caused earlier flowering in E. grandiflorum. Because alterations in phenology can disrupt important ecological interactions, information on potential phenological shifts in species that interact with E. grandiflorum is essential in determining the net effect of climate-driven alterations in phenology.     

Phenological patterns among plant life-forms in a subtropical forest in southern Brazil

Phenological patterns in tropical plants usually are associated with the clear seasonality of rainfall associated with very different wet and dry seasons. In southern Brazil, in a subtropical forest with no pronounced dry season (average annual precipitation = 1389 mm, minimum monthly average c. 75 mm), plant phenology was studied to test for patterns (periodicity), to examine how phenological patterns vary among life-forms, and to test whether phenological cycles are associated with climatic variables. Thirty-seven plant species in four life-forms (trees, shrubs, lianas and epiphytes) were studied for 2 yr (1996-98) in an Araucaria forest remnant in southern Brazil, in the state of Paraná. Correlation and multiple regression methods established relationships between phenology and climate in terms of daylength, temperature and rainfall. In this Araucaria forest, plants showed seasonality in most life-forms and phenological phases. Leaf-fall, with its peak during the drier months (April to July), was the most seasonal. Flushing and flowering occurred during the wetter months (September to December), while fruiting occurred all year long. Phenologies varied among life-forms, and were strongly associated with daylength or temperature of preceding months, suggesting that plants receive their phenological cues well in advance of their phenological response. Phenologies in this Araucaria forest appear to be associated with the most predictable and highly correlated of the climatic variables, daylength and temperature and least so with rainfall, which is unpredictable.     

Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae)

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.     

Impact of climate change on plant phenology in Mediterranean ecosystems

Plant phenology is strongly controlled by climate and has consequently become one of the most reliable bioindicators of ongoing climate change. We used a dataset of more than 200 000 records for six phenological events of 29 perennial plant species monitored from 1943 to 2003 for a comprehensive assessment of plant phenological responses to climate change in the Mediterranean region. Temperature, precipitation and North Atlantic Oscillation (NAO) were studied together during a complete annual cycle before phenological events to determine their relative importance and potential seasonal carry‐over effects. Warm and dry springs under a positive phase of NAO advance flowering, leaf unfolding and fruiting dates and lengthen the growing season. Spatial variability of dates (range among sites) was also reduced during warm and dry years, especially for spring events. Climate during previous weeks to phenophases occurrence had the greatest impact on plants, although all events were also affected by climate conditions several months before. Immediate along with delayed climate effects suggest dual triggers in plant phenology. Climatic models accounted for more than 80% of variability in flowering and leaf unfolding dates, and in length of the growing season, but for lower proportions in fruiting and leaf falling. Most part of year‐to‐year changes in dates was accounted for temperature, while precipitation and NAO accounted for <10% of dates' variability. In the case of flowering, insect‐pollinated species were better modelled by climate than wind‐pollinated species. Differences in temporal responses of plant phenology to recent climate change are due to differences in the sensitivity to climate among events and species. Spring events are changing more than autumn events as they are more sensitive to climate and are also undergoing the greatest alterations of climate relative to other seasons. In conclusion, climate change has shifted plant phenology in the Mediterranean region.     

Variable flowering phenology and pollinator use in a community suggest future phenological mismatch

Recent anthropogenic climate change is strongly associated with average shifts toward earlier seasonal timing of activity (phenology) in temperate-zone species. Shifts in phenology have the potential to alter ecological interactions, to the detriment of one or more interacting species. Recent models predict that detrimental phenological mismatch may increasingly occur between plants and their pollinators. One way to test this prediction is to examine data from ecological communities that experience large annual weather fluctuations. Taking this approach, we analyzed interactions over a four-year period among 132 plant species and 665 pollinating insect species within a Mediterranean community. For each plant species we recorded onset and duration of flowering and number of pollinator species. Flowering onset varied among years, and a year of earlier flowering of a species tended to be a year of fewer species pollinating its flowers. This relationship was attributable principally to early-flowering species, suggesting that shifts toward earlier phenology driven by climate change may reduce pollination services due to phenological mismatch. Earlier flowering onset of a species also was associated with prolonged flowering duration, but it is not certain that this will counterbalance any negative effects of lower pollinator species richness on plant reproductive success. Among plants with different life histories, annuals were more severely affected by flowering–pollinator mismatches than perennials. Specialized plant species (those attracting a smaller number of pollinator species) did not experience disproportionate interannual fluctuations in phenology. Thus they do not appear to be faced with disproportionate fluctuations in pollinator species richness, contrary to the expectation that specialists are at greatest risk of losing mutualistic interactions because of climate change.