Phenology has achieved a prominent position in current scenarios of global change research given its role in monitoring and predicting the timing of recurrent life cycle events. However, the implications of phenology to environmental conservation and management remain poorly explored. Here, we present the first explicit appraisal of how phenology -a multidisciplinary science encompassing biometeorology, ecology, and evolutionary biology -can make a key contribution to contemporary conservation biology. We focus on shifts in plant phenology induced by global change, their impacts on species diversity and plantanimal interactions in the tropics, and how conservation efforts could be enhanced in relation to plant resource organization. We identify the effects of phenological changes and mismatches in the maintenance and conservation of mutualistic interactions, and examine how phenological research can contribute to evaluate, manage and mitigate the consequences of land-use change and other natural and anthropogenic disturbances, such as fire, exotic and invasive species. We also identify cutting-edge tools that can improve the spatial and temporal coverage of phenological monitoring, from satellites to drones and digital cameras. We highlight the role of historical information in recovering long-term phenological time series, and track climate-related shifts in tropical systems. Finally, we propose a set of measures to boost the contribution of phenology to conservation science. We advocate the inclusion of phenology into predictive models integrating evolutionary history to identify species groups that are either resilient or sensitive to future climatechange scenarios, and understand how phenological mismatches can affect community dynamics, ecosystem services, and conservation over time. We hereby submit the revised draft of our 'Perspectives' manuscript entitled "Linking plant phenology to conservation biology" to which we now incorporate the rather minor changes suggested by the reviewers. While responding to those very positive comments, we also indicate how we have incorporated the reviewers' remarks. UNIVERSIDADE ESTADUAL PAULISTAWe thank you and the reviewers again for all the suggestions that have improved our The MS is well written, integrates interesting different aspects of plant phenology and provide a guide to include phenology in prospective long-term studies and management plans. Therefore the study is of general interest for a wide audience, particularly for Biological Conservation readers.Next, I suggest some changes to improve the current version of the MS 1. Authors comment the effect of climate and land use change on Section 4. For example, they argue that edge effect "increase of flowering and fruiting activity" (Line #389) or fragmentation affect reproductive success. Yet, these are functional responses of plant populations to different types of disturbances/changes, but they do not necessary entail changes in phenology. Please, review the MS and make sure that you only include ...
Summary1. Many factors shape plant reproductive patterns including climate, competition or attraction of pollinators and seed dispersers, flower and fruit morphologies and phylogenetic relationships. South American Myrtaceae (Myrteae) were chosen to evaluate hypotheses on how abiotic and biotic factors, morphology and phylogeny influence plant reproductive phenology. 2. We examined whether Myrteae reproductive patterns are seasonal and related to climate; whether aggregated or segregated flowering and fruiting occur among species sharing pollinators or seed dispersers; the relationship between phenological and morphological traits, time of reproduction and Myrteae phylogenetic history; and the shared influence of ecological (environmental) and phylogenetic factors on Myrteae reproductive patterns. 3. We observed flowering and fruiting of 34 Myrteae species during 30 months in an Atlantic rain forest (south-eastern Brazil). We employed circular statistics to test for seasonality and multiple regressions to relate climate and phenology. Competition and facilitation hypotheses were tested using null models. We quantified the phylogenetic signal on phenology and morphology of Myrteae species using phylogenetic eigenvector regression (PVR) analyses, and used PVR and partial regressions to quantify the influences of ecology and phylogeny on phenology. 4. Myrteae flowered seasonally, whereas fruiting was not seasonal. Environmental factors (daylength and temperature) and associations with biotic vectors through facilitation hypothesis explained the aggregated blossom. Fruit maturation time affected the species' flowering sequence. Plants with longer fruit maturation times flowered at the end of the appropriate season, explaining the continuous fruit availability despite the seasonal flowering. The random fruiting pattern explained the regular presence of seed dispersers. Myrteae phenology was phylogenetically structured, even when phenophases were not seasonal, i.e., closer related species fruited under more similar environmental conditions, suggesting that the reproductive phenological niche was inherited along the course of evolution. We detected a shared influence of ecology and phylogeny on Myrteae phenological responses, and the ecological component explained better phenological variation than phylogeny. 5. Synthesis. We provided a new perspective on plant phenology based on phylogeny and ecology and demonstrated the importance of considering their shared influence in phenological studies. Our analyses can be employed for the most representative families of highly diverse ecosystems to improve our understanding of evolutionary patterns and general trends in phenology.
The availability of fruits is critical for tropical forests, where the majority of plant species rely upon animal vectors for seed dispersal. However, we do not know how fruit production is temporally distributed over species and families. Two plant families are particularly important in floristic inventories of Atlantic rain forests: Arecaceae, a few species of which are highly abundant; and Myrtaceae, which is abundant and displays outstanding species diversity. In this context, we asked whether hyperdominance occurs in fruit production in the Atlantic rain forest, and whether it occurs in the abundant species of Arecaceae and Myrtaceae. We investigated whether the temporal fruit production patterns differ between Myrtaceae, Arecaceae, and the plant community as a whole. We also applied a functional dispersion index to assess the temporal fruit diversity over a 2‐yr period, with regard to morphological and phenological traits. We found that the phenomenon of hyperdominance occurs in fruit production: five species accounted for more than half of the pulp biomass. Arecaceae fruit biomass peaked at the end of wet season, overlapping with the community peak; whereas Myrtaceae species fruited throughout the year and were an important resource during periods of food scarcity. Myrtaceae filled more of the fruit morphospace over time because their fruits exhibit a large range of morphologies and phenological strategies. Our results demonstrated the importance of combining phenology and fruit morphology in the evaluation of resource availability, which revealed periods of high fruit diversity that could support a range of frugivore sizes and maintain overall ecosystem functionality.
Many recent studies discuss the influence of climatic and geological events in the evolution of Neotropical biota by correlating these events with dated phylogenetic hypotheses. Myrtaceae is one of the most diverse Neotropical groups and it therefore a good proxy of plant diversity in the region. However, biogeographic studies on Neotropical Myrtaceae are still very limited. Myrcia s.l. is an informal group comprising three accepted genera (Calyptranthes, Marlierea and Myrcia) making up the second largest Neotropical group of Myrtaceae, totalling about 700 species distributed in nine subgroups. Exclusively Neotropical, the group occurs along the whole of the Neotropics with diversity centres in the Caribbean, the Guiana Highlands and the central-eastern Brazil. This study aims to identify the time and place of divergence of Myrcia s.l. lineages, to examine the correlation in light of geological and climatic events in the Neotropics, and to explore relationships among Neotropical biogeographic areas. A dated phylogenetic hypothesis was produced using BEAST and calibrated by placing Paleomyrtinaea princetonensis (56Ma) at the root of the tree; biogeographic analysis used the DEC model with dispersal probabilities between areas based on distance and floristic affinities. Myrcia s.l. originated in the Montane Atlantic Forest between the end of Eocene and early Miocene and this region acted as a secondary cradle for several lineages during the evolution of this group. The Caribbean region was important in the diversification of the Calyptranthes clade while the Guayana shield appears as ancestral area for an older subgroup of Myrcia s.l. The Amazon Forest has relatively low diversity of Myrcia s.l. species but appears to have been important in the initial biogeographic history of old lineages. Lowland Atlantic Forest has high species diversity but species rich lineages did not originate in the area. Diversification of most subgroups of Myrcia s.l. occurred throughout the Miocene, as reported for other Neotropical taxa. During the Miocene, geological events may have influenced the evolution of the Caribbean and Amazon forest lineages, but other regions were geological stable and climate changes were the most likely drivers of diversification. The evolution of many lineages in montane areas suggests that Myrcia s.l. may be particularly adapted to such environments.
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