How plant phenomena can save species

Phenology is an integrative environmental science that has achieved a prominent position in current global-change research, due to its capacity to monitor, understand and predict the timing of recurrent biological events related to climate, such as bird migration, frog calling, and leafing, flowering and fruiting of plant populations (Rosenzweig et al., 2008). Phenological studies also provide key knowledge that can be incorporated into predictive models forecasting climate change scenarios (IPCC, 2014; Rosemartin et al., 2014).

Climate is the main factor controlling and regulating phenological events in plants, and global warming has affected species distributions and the timing of leaf change and reproduction (Chuine and Beaubien, 2001; Menzel et al., 2006), with likely effects on biogeochemical processes and physical properties of the atmosphere (van der Sleen et al., 2015). Across the tropics, subtle changes in temperature have been regarded as a less important phenological trigger, whereas seasonal variation in rainfall has been usually considered as an environmental cue for phenology (Borchert, 1998; Morellato et al., 2000, 2013). However, plant phenology responses to invariant cues, such as photoperiod, may be important in defining the timing, periodicity and particularly the synchrony of plant reproduction, especially in tropical environments where climatic seasonality is low (Borchert et al., 2005; Rivera and Borchert, 2001). Long-term phenological time series from the Northern Hemisphere have shown a strong link between the earlier onset of leafing and flowering and elevated temperatures due to climate change (Menzel et al., 2006; Schwartz et al., 2006). However, information on the effects of climate change in tropical regions is still sparse, particularly in the Southern Hemisphere, and long-term data sets are rare (Chambers et al., 2013; Morellato et al., 2013).

The management and conservation of natural systems can be critically enhanced with a greater understanding of the triggers regulating and controlling plant cycles and differences across species, populations and communities (Miller-Rushing and Weltzin, 2009; Polgar and Primack, 2011). In this regard, recent improvements in vegetation monitoring techniques such as repeated digital photographs, and the growing field of satellite-derived phenology (Alberton et al., 2014; Morisette et al., 2009; Richardson et al., 2013) have paved the way to inferences about temporal shifts at multiple scales that can be applied worldwide.

Despite the well-known connection between phenology and climate change (IPCC, 2014), its relevance and implications for resource conservation and management remain poorly understood. These implications include the synchronicity between flowering and pollinator activity or fruiting and seed disperser activity, the connectivity and gene flow through pollen and seed movements across fragmented landscapes, and the forecasting of climate-change effects on species distributions and ecosystem processes. In fact, plant phenology links different hierarchical levels and functional groups within a community, including decomposers, detritivores, herbivores, predators, pollinators, and seed dispersers. Consequently, efforts to conserve these temporal links will safeguard the functionalities and long-term maintenance of ecosystem services. In this context, we explore how phenology — as a multidisciplinary science encompassing biometeorology, ecology, and evolutionary biology (Wolkovich et al., 2014) — can be harnessed as a key research endeavour in applied ecology and conservation biology, with special emphasis on the tropics.

Our framework is centred on the potential shifts in plant phenology driven by global environmental change and their impact on the high diversity of species and plant–animal interactions found in the tropics (Fig. 1). One key issue would be to incorporate phenology into community-level coexistence theory tied to the species niche concept. As such, broadening the ecological niche to a more explicit temporal space would allow investigators to test hypotheses and make predictions regarding plant responses to environmental and competitive changes at different scales (e.g. Schellhorn et al., 2015; Wolkovich and Cleland, 2011; Wolkovich et al., 2014). We highlight issues where phenology can provide a major contribution to conservation science. We begin addressing how phenology can help conservation efforts in relation to plant–animal interactions from the perspective of resource availability in plant populations and communities, and bottom-up trophic organization. We point out the relevance of ecological networks to understand the effects of temporal changes and mismatches between resources and consumers on the maintenance of mutualistic interactions (Fig. 1). We examine how phenological mismatches affect communities, ecosystem services, and ecosystem recovery dynamics over time. Furthermore, we discuss how knowledge of plant phenology can help evaluate and mitigate the effects of land use change on ecological interactions, including habitat fragmentation, edge effects, and fire. We also consider the thorny problem of exotic and invasive species and the key role of phenology in managing biological invasions and restoring natural ecosystem integrity. We indicate the use of phenology as a functional trait that, combined with traditional leaf morphology and other traits, would be a more accurate indicator of plant functions related to responses to climate and other environmental cues, such as wildfires (Carvalho and Batalha, 2013) or biological invasions (Wolkovich and Cleland, 2011).

To our knowledge, this is the first appraisal specifically addressing the implications of phenological knowledge to conservation biology. We propose, therefore, a set of avenues that would allow a stronger and more effective contribution of organismal phenology to conservation science. We point out the value of novel monitoring strategies improving spatial and temporal coverage of phenological monitoring, from satellites to drones and digital cameras. We highlight the key role of retrieving historical information from herbaria and observational studies to fill the gaps of long-term time series (e.g. Hart et al., 2014; Primack et al., 2004; Primack, 2014) and shed light on the potential effects of climate change and the consequences of directional phenological shifts in tropical systems. In this sense, the concept of “phenospecies” (i.e. sympatric species that share the same phenological triggers and strategies (Proença et al., 2012), may help reconstruct longer temporal series which can be investigated for biases in reproductive schedules over time. Along this line, advances in dendrochronology may also open new directions for tropical forest conservation from the point of view of past chronological reconstruction, carbon stock accumulation, and ecosystem processes (Schöngart et al., 2011). We propose integrating phenology and species evolutionary history into predictive models, to distinguish between species groups that are either resilient or sensitive to projected climate changes scenarios (Staggemeier et al., 2015; Willis et al., 2008). Finally, we draw attention to the value of citizen science to build phenology databases for conservation (Rosemartin et al., 2014; Theobald et al., 2015) and its unexplored potential in the tropics.

Fig. 1. (A)

The abiotic and biotic effects of human activities on plant life cycles. Abiotic influences as a result of human activities include climate change, modifications of geochemical cycles, and frequency of fires. Biotic influences as a result of human activities include habitat loss and fragmentation, hunting, and species invasion. These factors collectively influence plant phenology, including leafing, flowering and fruiting, and seed germination and establishment.

Fig. 1.  (B)

The effects of climate change on leaf production and insect activity. Climate change has resulted in later leaf production, which creates an increased overlap between leafing and insect activity. This increases the likelihood of herbivory damage to plants and ultimately decreases plans' abilities to survive and reproduce viable offspring.

Fig.1. (C)

Climate change has created longer, more intense dry seasons; which ultimately contributes to later plant reproduction, lower fruit yield, and lower germination rates. Delays in flowering might limit the the amount of time pollinators have to disperse pollen, which will reduce plants' abilities to produce viable offspring.

 

METHODS

The present appraisal focuses on phenology from an ecological and evolutionary point of view, its relevance for climate change research and its implications and applications in conservation science, with special attention to the tropics. Our intended audience are conservation practitioners and researchers on phenology and related fields, and we strived to attain a broad but concise perspective of phenology within conservation practices. This appraisal is derived from a two-day workshop on phenology and conservation held by the Phenology Laboratory (UNESP, Brazil) in December 2014. We discussed a wide range of links between phenology to conservation science, and selected key topics with relevant contributions for the conservation and management of natural systems: phenology and conservation of biotic interactions; phenology, climate and land use change; phenology, evolutionary history and species distributions; data sets and monitoring systems; a set of practical and innovative research approaches; and new avenues for future research. The synopsis was also based on recently published (Hagen et al., 2012; Morellato et al., 2013, Chambers et al., 2013) and ongoing reviews (Buisson et al., 2015; Mendoza et al., 2014; Morellato et al., 2014) conducted by members and collaborators of the UNESP Phenology Lab, and the authors' own experience in phenology and conservation science. The criteria for the systematic literature search are available in Chambers et al. (2013) and Morellato et al. (2013). We updated these surveys by searching the top conservation science journals using the terms “phenolog*” and “conservation” over the last 10 years. Our goal was to identify relevant research and applications for conservationists and managers, rather than perform an exhaustive review of the topic.

PHENOLOGY AND THE CONSERVATION OF BIOTIC INTERACTIONS

Leafing and herbivory

Studies of leafing phenology have twofold implications for conservation. First, leaf phenology is directly linked to ecosystem processes (Polgar and Primack, 2011). Leaf flushing and senescence are related to plant growth, and as such are crucial for understanding plant–water relations and primary productivity in terrestrial ecosystems, as well as gas exchange rates, biogeochemical cycling, and the dynamics of carbon sequestration (Morisette et al., 2009; Polgar and Primack, 2011). Investigating the timing and drivers of leaf production and senescence is important to define the length of growing seasons and seasonal patterns of photosynthesis at local to global scales (Morisette et al., 2009). Leaf phenology thus provides key information for ecosystem process models that forecast responses to land-use change, atmospheric chemistry, and climate (Morisette et al., 2009). Thus, shifts at both the onset and end of growing seasons due to climate change may have consequences on ecosystems processes such as net primary production. For instance, increases in temperature and drought frequency may lead to premature leaf senescence in deciduous forests, affecting the efficiency of nutrient resorption and the length of growing seasons, impacting carbon uptake and ecosystem nutrient cycling (Estiarte & Peñuelas 2015), and therefore management practices (e.g. Eriksson et al., 2015).

Second, the timing of leaf production has consequences for interactions between plants and herbivores (Fig. 1B), which in the tropics comprise mainly phytophagous insects (Novotny et al., 2006). The conservation of insect populations can be severely affected by changes in the timing of leaf production (Kocsis and Hufnagel, 2011), particularly in the context of declining invertebrate faunas, estimated at a global scale to have exceeded 45% between 1970 and 2010 (Dirzo et al., 2014). In turn, shifts in herbivorous insect phenology due to climate change, land-use change, or use of insecticides can threaten plant population viability, leading to increases in herbivore damage (van Asch and Visser, 2007).

Plants can adopt several phenological strategies to avoid insect damage, such as synchronizing the timing of leafing peaks to the season with the lowest insect densities, or producing large, synchronous pulses of leaves to satiate herbivores (Aide, 1988; Lamarre et al., 2014). Future climatic scenarios may induce higher overlap between insects and plants activity (Fig. 1B), such as prolonged dry seasons delaying leaf production in plants that are stimulated by the first rains, increasing herbivore damage (Aide, 1993). Conversely, changes in abiotic factors can also reduce leafing synchrony, which would fail to satiate insect herbivores. Such extreme changes can lead to pest outbreaks and massive losses in plant production (van Asch and Visser, 2007). Phenological mismatches between agricultural pest insects and their natural enemies due to climate change could also decrease the effectiveness of biocontrol measures (Thomson et al., 2010).

Potential trophic mismatches may also arise between vertebrates and plant growing seasons, for instance as documented for caribou in Greenland where a reduction in the spatial variation in plant phenology caused by climate warming decreased offspring production (Post et al., 2008), with implications for managers and conservationists. A detailed knowledge of phenological dynamics of folivorous animals and their host/target plants can therefore be instrumental in the conservation and management of both herbivores and plant populations, and when designing pest control programmes in natural and agricultural ecosystems (Baumgartner and Hartmann, 2000; Eriksson et al., 2015).

Flowering and pollinators

The clearly delimited flowering seasonality during springtime, typical of temperate and boreal ecosystems, is generally absent in the tropics. Instead, open flowers are available throughout the year, albeit with varying abundances, inducing periods of peaks and troughs depending on community characteristics, and leading to diverse and complex phenological patterns (Morellato et al., 2013; Morellato et al., 2000).

Most of the world's plants rely on animal pollination for successful reproduction, especially in the tropics, where the proportion of animal-pollinated species has been estimated at 94% (Ollerton et al., 2011). Floral resources, provided primarily as food rewards for pollination services, can also include substances used for nest construction or aromatic compounds to attract females. The reliable and continuous availability of floral resources in the tropics has enabled strong and diverse adaptations in flower visitors, maintaining rich assemblages of highly specialized floral foragers, such as bees and hummingbirds. Resource extraction by flower visitors is limited to a subset of plants, being constrained by morphology, phenology, and the behaviour of visitors (Rosas-Guerrero et al., 2014). Therefore, spatial and temporal variation in floral resource diversity, abundance and distribution are major structuring factors in pollinator communities (Burkle and Alarcon, 2011; Carstensen et al., 2014; Olesen et al., 2008).

Pollinators offer essential pollination services and play a key role in the maintenance of agricultural systems worldwide (Garibaldi et al., 2013), and the interdependency of plant and pollinator populations affects community stability and the productivity of native and agricultural systems (Vázquez et al., 2009). Flowering phenology is therefore highly relevant for the organization and structure of plant communities, the conservation of mutualists and their interactions, and maintenance of essential ecosystem services (CaraDonna et al., 2014; Cruz-Neto et al., 2011; Garibaldi et al., 2013).

Fruiting and frugivory

Frugivorous animals critically rely on fruits, and fundamental aspects of their ecology—including diet, population size, social behaviour, reproduction, and movements — depend on fruit abundance and seasonality (Hanya and Chapman, 2013), which in turn affect seed dispersal and germination effectiveness (Schupp et al., 2010).Neotropical plant species not only bear a high percentage of fruits dispersed by animals, but most tropical vertebrates are frugivores to at least some extent (Hawes and Peres, 2014). Therefore, frugivores can be constrained by low fruit production or changes in fruit supply over time (Fig. 1c) according to their nutritional content, morphology and colour (Camargo et al., 2013; Develey and Peres, 2000; Herrera, 2009), with consequences for their conservation and management (Kannan and James, 1999). Significant and unexpected crashes in fruit availability can have dramatic effects on vertebrate frugivores. For example, episodic community-wide fruit shortages following an El Niño event greatly elevated mortality of frugivorous and granivorous vertebrates in Barro Colorado Island, Panama (Wright et al., 1999).

Plant conservation is also constrained by growing defaunation scenarios in tropical ecosystems,with cascading consequences for seed dispersal and seedling establishment (Galetti and Dirzo, 2013). This is especially critical for large-seeded plant species, given their reliance on large-bodied seed dispersers that are usually the preferred targets of game hunters (Dirzo et al., 2014; Jerozolimski and Peres, 2003). For instance, defaunation of large-gaped frugivorous birds has been singled out as the main cause of rapid evolutionary change in palm seed size (Galetti et al., 2013). Though poorly studied, the same evolutionary pressure could affect plant phenology (e.g. favouring a greater overlap between fruiting and the activity of non-hunted frugivores), with farreaching consequences. Conservation of tropical communities requires an understanding of the interconnection between seasonal fluctuations in climate and the availability of resources for primary consumers (e.g. (Wright and Calderon, 2006;Wright et al., 1999), including potential changes induced by both natural (Haugaasen and Peres, 2007) and anthropogenic disturbances (Barlow and Peres, 2006; Haugaasen and Peres, 2007).

Mismatches in mutualistic networks

The impact of global change on plant phenology is not expected to be uniform across all species, and effects at the species level may lead to consequences at the community level, potentially changing the timing of flowering or fruiting peaks and the duration of reproductive seasons (Donnelly et al., 2011; Hanya and Chapman, 2013; Hoye et al., 2013). Furthermore, phenological change in some plant species can potentially affect other plants through competition and/or facilitation for pollinators and seed dispersers, resulting in complex community-wide responses (Burkle and Alarcon, 2011). Understanding the higherorder effects of phenological shifts on biotic interactions requires a community level approach, possibly achieved by the application of ecological networks.

Phenology is an important structuring force in plant–animal interactions and influences the topological position of species within mutualistic networks, affecting the organization of interactions and competitive relationships depending on the length and interspecific overlap of reproductive seasons (Encinas-Viso et al., 2012; Olesen et al., 2008, see Fig. 1). The length of reproductive seasons is a defining factor in the number of interaction partners a species can have. Some studies indicate that phenology plays a key role in the stability and diversity of mutualistic communities (Thébault and Fontaine, 2010) and is of key importance for the management and conservation of plant–pollination interactions and mutualistic networks (Memmott et al., 2007).

In this context, one potential threat from climate change is the temporal uncoupling of mutualistic species interactions (Hegland et al., 2009; Hoye et al., 2013; Memmott et al., 2007). Mismatches between organism and resources, such as plants and their animal symbionts, may arise if climate change affects the onset, peak, and/or duration of flowering and fruiting differentially (Fig. 1C), compared to the activity and life cycles of consumers (Donnelly et al., 2011). Such mismatch can have stark consequences, including recruitment failure in plants and resource scarcity, if not famines and population crashes, in consumers (Berg et al., 2010; Memmott et al., 2007; Wright and Calderon, 2006; Wright et al., 1999). Environmental changes that cause some level of mismatch between plants and pollinators can reduce pollination services (Petanidou et al., 2014) and, consequently, seed production (Satake et al., 2013), affecting the dynamics of plant and animal populations (Fig. 1C). The significance of temporal mismatches in the functioning of ecological communities is inextricably linked to the ability of pollinators and other mutualistic partners to switch their resource use according to the timing of availability. Recent studies indicate great variability in the identity of plant–pollinator interactions (Burkle and Alarcon, 2011; Carstensen et al., 2014; Dupont et al., 2009), which could mediate compositional changes driven by phenological mismatches (Kaiser-Bunbury et al., 2010). Changes in the taxonomic composition of visitors due to mismatching between plants and pollinators caused by earlier flowering can affect pollination success and seed set (Rafferty and Ives, 2012). Ultimately, both the ability of animal partners to forage on changing host plants as well as the maintenance of viable services for host plants from these mutualistic partners will influence the severity of potential effects of phenological mismatches and the conservation of mutualistic networks (Burkle et al., 2013; Memmott et al., 2007). However, evidence for climate-driven mismatches is at best difficult to obtain and still lacking for most systems (Miller-Rushing andWeltzin, 2009).

PHENOLOGY, CLIMATE, AND LAND USE CHANGE

Fragmentation and edge effects

One of the main outcomes of land-use change is habitat loss, which is arguably the main driver of declines in plant and animal diversity (Laurance, 2008). Habitat loss and the resulting fragmentation and edge effects produce fine-scale variation in light, temperature and humidity conditions, inducing phenological changes, with consequences to plant–animal interactions and ecological services reverberating throughout the ecosystem (Hagen et al., 2012). Different studies have reported an increase in flowering and fruiting activity in native habitats with increased sunlight, such as edges and gaps (Athayde and Morellato, 2014; Burgess et al., 2006; Camargo et al., 2011). However, in fragmented areas and those subjected to edge effects, this higher production in reproductive plant parts does not always favour the reproductive success and recruitment of native species from the original plant community (Athayde and Morellato, 2014; Christianini and Oliveira, 2013; Quesada et al., 2004). This is probably a consequence of the previously discussed temporal mismatches induced by new environmental conditions, with loss of pollinators and seed dispersers (Hagen et al., 2012). For conservation purposes, phenological studies investigating plant responses to particular environmental conditions, such as natural or anthropogenic edges and forest gaps, would help manage fragmented reserves (deMelo et al., 2006) and model vegetation responsiveness and susceptibility to similar environmental shifts expected in future global change scenarios (Breed et al., 2012; Hagen et al., 2012; Morellato et al., 2013).

Fire, phenology and conservation

Fire is a natural element of many tropical ecosystems around the world, and often determines vegetation physiognomy and species diversity (Bond and Keeley, 2005; Carvalho and Batalha, 2013). Fire disturbance can be either natural or anthropogenic, and the few studies evaluating the effects of fire on phenology have shown that, depending on the plant community, fire can stimulate flowering and fruiting (Pausas et al., 2004) and germination (e.g.Williams et al., 2005), elevate fruit production (Paritsis et al., 2006), and/or accelerate the phenological cycle by shifting the starting date of flowering/fruiting (Paritsis et al., 2006), but may also depress the availability of large-seeded fruits (Barlow and Peres, 2006). However, fires can also reduce flowering and fruiting by destroying buds, flowers and fruits, affecting species that reproduce during the fire season (Alvarado et al., 2014; Hoffmann, 1998) and/or favour invasive species (D'Antonio, 2000). Therefore, fire-induced changes in plant phenology comprise a key issue for vegetation management and conservation.

Phenology can be adopted as a functional trait to characterize plant community responses to fire (Carvalho and Batalha, 2013), and predict the dynamics of vegetation recovery or guide management practices and restoration strategies in fire-prone landscapes (Andersen et al., 2005). This has been the case of Ibity New Protected Area (NPA) in Madagascar. Phenology observations showed that high fire frequency reduce flower and fruit production of tapia woodlands (Alvarado et al., 2014), indicating the limited potential for natural regeneration of the vegetation (Alvarado et al., 2015). Phenological information has been used to improve the management actions for the Ibity NPA, and is considered as an important issue for the successful implementation of an integrated conservation strategy, targeting restoration of plant communities and reintroduction of threatened plant species.

Phenological patterns and exotic, invasive and native species interactions

The study of how native, exotic and invasive species (see Richardson et al., 2000 for definitions) interact could benefit from acknowledging plant phenology as a key trait influencing their interactions (Wolkovich and Cleland, 2011). Invasive species are managed because they modify the composition and functioning of native ecosystems, driving native species declines or local extinctions (Vilà et al., 2011). Closely related native and exotic species may hybridize if they have matching phenologies, inducing the loss of genetic diversity and disrupting locally adapted populations, such as rare and threatened species (Huxel, 1999; Vilà et al., 2000). Theymay further compete for pollinators and seed dispersers, altering fruit quantity, quality, seed dispersal and thus community structure and ecosystem functioning (Morales and Traveset, 2009; Vilà et al., 2000). Exotic species can also leaf out, bloom or produce fruits when natives are not producing alternative resources (thus filling a vacant niche), or can flower or germinate earlier than natives thus benefiting from a priority effect (Wolkovich and Cleland, 2011). Both cases (vacant niche and priority effect) affect native species conservation because management can be applied when exotics are vulnerable (e.g. fire, grazing, herbicide, Marushia et al., 2010; Wolkovich and Cleland, 2011) and natives are not. Exotics can also leaf or fruit for longer periods of time than natives, sustaining a wider niche, or exhibit greater flowering plasticity, both of which would confer advantages over natives, providing more adaptability to environmental changes with implications for management and conservation (Wolkovich and Cleland, 2011).

Native species can act as invasive if disturbances promote biomass growth; e.g. native liana hyperabundance resulting fromincreased temperature and CO2 availability associated with global atmospheric change (Phillips et al., 2002; Schnitzer et al., 2014). The phenology of liana-supporting trees may therefore be modified by light competition, affecting leaf, flower and fruit production (Avalos et al., 2007). Conversely, native lianas can play an essential role in providing flower resources to pollinators during periods of scarcity of flowering trees (Morellato and Leitão-Filho, 1996). Forest conservation and management in areas with high liana abundance must take into account these potential phenological effects and associated trade-offs.

EVOLUTIONARY HISTORY, SPECIES DISTRIBUTIONS AND PHENOLOGICAL VARIABILITY

Deciphering the role of evolutionary history on phenological patterns is important to identify species that are sensitive or resilient to climate change scenarios. Moreover, building more realistic species distribution models based on historical information (from herbaria and/or ground-based phenology) can help to identify changes in plant responses over timeand predict their future outcomes. This is especially relevant in systems where available phenological data are restricted to local scales and short time periods as tropical environments in the Southern Hemisphere (Chambers et al., 2013; Morellato et al., 2013).

Evolutionary history, phenology and conservation

Evolutionary history can affect phenology (Staggemeier et al., 2010, 2015), likely because the physiological pathways triggering reproduction are inherited at an evolutionary timescale (reviewed in Weinig et al., 2014). If evolutionary history matters, closely related species are expected to reproduce under the sameenvironmental conditions; alternatively, if climate is the primary cue, species would reproduce in the most favourable period of time, regardless of their evolutionary relationships (Kochmer and Handel, 1986). Current molecular techniques allow us to explicitly examine the evolutionary patterns of species traits and test whether phenology has a strong phylogenetic signal (Staggemeier et al., 2010, 2015). Plants with conservative phenologies are more susceptible to changes in the climatic conditions triggering their reproduction (Willis et al., 2008). Hence, incorporating phenology into predictive models of evolutionary responses to climate change is crucial to identify fragile clades that are more susceptible to global change. Managers and conservationists can then target vulnerable species that do notmodify their phenology according to climate, and design effective conservation strategies in light of climatic change scenarios (Miller-Rushing and Weltzin, 2009; Willis et al., 2008), especially in complex tropical ecosystems (Staggemeier et al., 2015). Conservation plans can prioritize the protection andmaintenance of sensitive species by selecting sites that maximize their persistence.

The timing of reproduction critically defines plant reproductive success, and determines species dynamics, affecting dispersal and colonization rates and the geographic distribution of plants (Chuine and Beaubien, 2001). However, the relationships between phenology and species range attributes are underexplored in the literature (Chuine and Beaubien, 2001). For example, integrating phenological traits into ecological niche models would result in more representative and reliable projections of the ecology and dynamics of plants and biomes. We advocate combining occupancy records and phenological data archived in historical collections such as herbaria (Lavoie and Lachance, 2006) to investigate reproductive phenology at large geographic scales (Zalamea et al., 2011) and in species distribution modelling, to build predictions for future ecosystem alterations and formulate effective conservation strategies (Chapman et al., 2014).

Variation within populations: why preserve individual variability

Phenological patterns may differ between individuals of the same species, diverging from the average pattern exhibited by the population or community. Intraspecific variation in plant phenology can be related to the micro-environmental conditions where individuals are established, as well as genetic provenance (Herrera, 2009; Satake et al., 2013). This is highly relevant in the case of flowering, as it comprises the first mechanism of reproductive isolation; flowering synchrony is critical to the reproductive success of the predominantly out-crossing species in tropical ecosystems (Burgess et al., 2006).

Therefore, assessing the influence of local factors on individual phenology within populations becomes very relevant under current scenarios of global climate change (Diez et al., 2012). Population management and conservation are constrained by the available gene pool and plasticity, which enable species persistence by adaptation and successful reproduction under new environmental conditions. Environmental change reduces the local variability of coexisting conspecifics and hinders their adaptation to new scenarios, as shown for fruit/seed size in arborescent palms (Galetti et al., 2013). Fragmented and spatially isolated habitat patches can remain connected and ecologically functional if their populations maintain ecological interactions and gene flow among individuals across the landscape (D'Eon et al., 2002; Fahrig et al., 2011). Topographical diversity associated with phenological variability in populations of Centaurea scabiosa minimise the phenological mismatches with pollinator related to recent climate change (Hindle et al., 2015). Thus, understanding the processes that influence individual phenology and interactions within populations is critical, not only to ensure the viability of these plant populations, but also for the conservation of communities and ecosystems.

PHENOLOGY DATABASES, NEW MONITORING TOOLS AND CONSERVATION PRACTICES

Long-term phenological databases

Phenological monitoring typically falls outside the spectrum of mainstream conservation strategies, although basic phenological data extracted from traditional direct observations of plant populations have provided critical information for conservation planning, at all biodiversity levels defined by the Convention on Biological Diversity (CBD; www.cbd.int/convention/text/)): genes, species and ecosystems. For instance, datasets resulting fromphenological studies can be organized as a seed collection calendar, supporting restoration efforts or ex situ genetic conservation (e.g. Packard et al., 2005). Also, those data sets make an invaluable contribution for initiatives such as the Kew's Millennium Seed Bank, aiming to harbour the germplasm of up to 25% of the world's plant diversity (Ali and Trivedi, 2011). Besides creating a seed collection calendar, the relationship between fruiting phenology and seed germination, dormancy (Garwood, 1983; Salazar et al., 2011; Yang et al., 2013), and storage behaviour (Pritchard et al., 2004) in seasonal habitats can be additional criteria for choosing species, methods for breaking dormancy, and seed preservation. Therefore, seeds dispersed at the onset of the rainy season tend to be non-dormant and desiccation-sensitive, while those dispersed during the dry season tend to be dormant and desiccation-tolerant (Salazar et al., 2011; Yang et al., 2013).

From a conservation perspective, phenological research is the basis of several studies, such as the effects of generalized fruiting failure on periodic frugivore famines (e.g. due to El Niño events, Wright et al., 1999), or the importance of the timing of fruiting peaks for breeding seasons of frugivorous birds (Develey and Peres, 2000). Also, defining keystone plants for vertebrate fauna during lean times of the year relies on previous knowledge of the phenological patterns of non-redundant resources, compared to alternative resources across the entire plant community (Peres, 2000).

Herbaria are a remarkable database and significant source of long-term phenological data that have been used to reconstruct past historical patterns of plant phenology (Hart et al., 2014; Lavoie and Lachance, 2006; Primack et al., 2004). Phenological time series from herbarium can be a reliable predictive tool in the context of scarce historical information from ground observation, especially in the tropics (Chambers et al., 2013; Morellato et al., 2013). Therefore, herbarium records can play a key contribution to conservation, providing data on reproductive patterns of single species to whole assemblages across entire regions where no phenological information is available (Bolmgren and Lonnberg, 2005; Boulter et al., 2006; Rawal et al., 2015; Tannus and Assis, 2004). Considering the growing number of digitalized collections from herbaria all around the world, including some major tropical herbaria, phenological information is available at no cost for managers and conservationists at sites such as the REFLORA, the website for the Brazilian Herbaria collections and species lists (http://reflora.jbrj.gov.br/jabot/PrincipalUC/PrincipalUC.do; jsessionid=52939BFB2B6A0EE6DAE92077C796583F). In addition, one may infer geographic patterns and build phylogeographic models that can offer key insights on the future distribution of endangered and rare species. We can further use herbarium records to identify “phenospecies” (Proença et al., 2012), which can be investigated for shifts in reproductive schedules over time (Borchert, 1998; Primack, 2014; Rivera and Borchert, 2001).

Dendrochronology has been also an effective way to reconstruct longer series of leaf phenology for understudied systems, as the growth rings and cambial activity of tree species are linked to climate (Schweingruber, 1996). Although little information is available on tree-ring analysis for tropical trees (Worbes, 2002), new methods and tools have increased the reconstruction accuracy of the periodicity of growth ring formation (Roig, 2000) and, as a consequence, the prediction of growth seasons and carbon stocks of ecosystems. Dendrochronology and phenology have been applied to understand how climatic variables influence growth and cambial activity of tree species (Brienen et al., 2010), and develop growth models that inform the management and conservation of different tree species (Lisi et al., 2008; Schöngart, 2008), including some of the most important non-timber forest products in tropical forests, such as the Brazil-nut tree (Schöngart et al., 2015), which is threatened by systematic over exploitation of mature seeds (Peres et al., 2003). Long-term observations of the cambial phenology may facilitate the interpretation of cell differentiation phases, the length of the growing season and how their growth respond to environmental changes (Rossi et al., 2012). This factor can be critical in cell production and carbon uptake by forests (Rossi et al., 2013).

Phenological monitoring and new tools

Phenological monitoring techniques continues to grow in tandem with the increasing importance of systematic phenological data to explain ecological patterns, predict the effects of climate change, and address applied environmental and conservation issues (Miller-Rushing and Weltzin, 2009). This has led to the development of alternative observation methods (Morisette et al., 2009), such as phenological networks (Betancourt et al., 2005; Fuccillo et al., 2014), remote sensing based phenology from regional to global scales (Reed et al., 2013), and more recently, deployment of in situ digital cameras for continuous monitoring of multiple simultaneous sites, referred to as near-surface remote phenology (e.g., Richardson et al., 2009, 2013). Sampling species-rich plant communities can be expensive and labour-intensive in tropical phenology studies, limiting the establishment of comprehensive direct phenological observation systems, and increasing the relevance of alternative techniques such digital repeated photographs (Alberton et al., 2014).

Near-surface remote phenology using digital cameras (“phenocams”) allows the daily detection of leafing events according to changes in the red, green and blue (RGB) channels (Crimmins and Crimmins, 2008; Morisette et al., 2009), and have become reliable tools in monitoring leafing changes even in highly diverse vegetation in the seasonal tropics (Alberton et al., 2014).

Orbital remote sensing provides daily to monthly observations of surface radiation, which can be associated to changes in biophysical (e.g. leaf area index) and biochemical (e.g. chlorophyll and water content) vegetation parameters, thereby tracking phenology across space and time (Reed et al., 2013). Remote sensing approaches have proved useful in detecting seasonal vegetation changes over a large range of spatial and temporal scales, and have been incorporated into conservation practices (Nagendra et al., 2013). In the National Park network of Spain, radiometric information derived from the NOAA/AVHRR sensor series was used to assess changes in phenological activity between 1982 and 2006, detecting a decrease in seasonality and the advancing of leaf peak activity (Alcaraz- Segura et al., 2009). In North America, the United States Geological Survey (USGS) is at the forefront on collaborative studies in phenology, combining remote sensing imagery with field-collected datasets obtained by the USA National Phenology Network (USA-NPN, Graham et al., 2011; Willis, 2015). The typical high temporal frequency of these sensors, although not appropriate for local scale or individuals monitoring, provides valuable phenological information for ecologists and land managers, and support decisions on the allocation of further resources for more detailed spatial assessments (Nagendra et al., 2013; Willis, 2015).

Recent developments in remote sensing, such as hyperspectral, hyperspatial, and 3-D remote sensing (LiDAR and InSAR) bring the promise of identifying individual species and directly estimating leaf and canopy traits, which will enable a better coupling with traditional phenology (Reed et al., 2013). More recently, rapid advances in unmanned aerial systems (UAS) have allowed the deployment of these technologies with high temporal repeatability, providing an unparalleled platform for high-resolution phenological data acquisition (Anderson and Gaston, 2013). The ability of UAS in providing centimetre spatial resolution data at low cost, and the range of sensors that can be integrated to these systems also have wide applications in conservation science (Colomina and Molina, 2014). Paneque-Gálvez et al. (2014) discuss how small drones can support continuous monitoring and aid management and environmental conservation actions, and be easily included in community-based monitoring programmes due to its low-cost and ease of operation.

The use of UAS increases monitoring capacity when quantifying land use change, enabling comprehensive ecosystem surveys and monitoring of animal populations at low cost and reduced manpower (Koh and Wich, 2012). Furthermore, the use of specific software and algorithms to extract three-dimensional data from low-cost, UAV-based aerial photography, allows the repeated monitoring of several measures related to vegetation structure and complexity, which can help conservationists to address temporal and spatial vegetation dynamics in the landscape and evaluate vegetation recovery for conservation goals (Zahawi et al., 2015).

CONCLUSIONS: PROMISING AVENUES FOR FUTURE RESEARCH LINKING PHENOLOGY AND CONSERVATION

Plant reproduction triggers remain poorly understood across the tropics, especially in highly a seasonal ecosystems (Morellato et al., 2013). Recent advances in digital technologies to retrieve historical phenological information from herbaria, satellite images and field cameras will be essential to improve our capability to define proximate triggers, and forecast the effects of climate change. That is the promise of the e-phenology Phenology Project (http://www.recod.ic.unicamp.br/ ephenology/client/index.html), the first tropical initiative to build a network of digital cameras monitoring several vegetation systems in Brazil, while integrating UAVs and remote sensing into phenology monitoring, combined with the traditional on-the-ground direct observations (Alberton et al., 2014; Morellato et al., 2014).

As previously discussed, few studies have confirmed the occurrence of phenological mismatches due to climate or land-use change, and to our knowledge, none of these studies has been conducted in tropical systems, partly because suitable data sets are scarce. Phenology can help identify resource discontinuities along the chronosequence of plant resource availability for consumers that may affect growth and reproduction of target organisms (Schellhorn et al., 2015), and the resulting mismatches in time and space. The understanding and support of ecosystem services provided by biodiversity should take into account the temporal dimension in resource abundance and dynamics across the landscape (Schellhorn et al., 2015).

We therefore propose a series of measures and research topics that can increase the contribution of phenology research to conservation science (Box 1). We have described how phenological studies can support conservation management protocols in actively triggering or accelerating the resilience of degraded ecosystems, potentially making a large contribution to the general research framework on global climate and land-use change. Phenological parameters provide essential measures that can be easily recorded and directly applied to an evolving conservation paradigm centred on preserving ecological processes, rather than a single-minded focus on endangered species or forest structure (Bennett et al., 2009). Recently, phenology was included among the Essential Biodiversity Variables (EBV), defined as “a measurement required for study, reporting, and management of biodiversity change” (GCOS, 2010; Pereira et al., 2013). The idea is achieving a global monitoring system that would provide critical data capturing chief elements of biodiversity change, thereby improving conservation management. Phenology as an EBV reaches the criteria of scalability, temporal sensitivity, feasibility, and relevance (Pereira et al., 2013). Remote sensing phenology is highlighted along with the few phenology global networks (Pereira et al., 2013). We also advocate developing other data platforms, especially citizen-science initiatives (Theobald et al., 2015), a denser network of local direct observations, and herbarium data (Lavoie and Lachance, 2006; Proença et al., 2012). Those data sources will provide invaluable information to validate remote sensing global patterns and improve biodiversity management and conservation.

The advancements in information science technologies to digitalize herbaria records and retrieve the historical phenological information from herbaria, satellite images and field cameras, will be essential to improve our capability to define proximate triggers and forecast the effects of climate change. The very essence of the importance of recovering historic phenological information, and its wide application for conservation, are illustrated by the work of Primack (2014) on the Thoreau records. As technology evolves and Land Surface Phenology becomes more likely, the ubiquity of ground-based phenology and remote sensing approaches will play an increasingly important role for phenology and conservation. This will help answer questions about the timing and drivers of phenological events under climate and land-cover change scenarios, especially in highly diverse and heterogeneous tropical system.

A final approach concerns the relevance of plant phenology as a tool for conservation education and citizen science as a whole (Fuccillo et al., 2014). Unfortunately, tropical countries have no proposed data acquisition networks or citizen science initiatives that are analogous to important phenological programmes in North America (USA — NPN https://www.usanpn.org/ and Cornell Bird Laboratory http://www.birds. cornell.edu/page.aspx?pid=1664); Canada — PlantWatch https://www.naturewatch.ca/plantwatch/) and Europe (United Kingdom — https://www.naturescalendar.org,uk) (Gonsamo et al., 2013) or the new Australian network (ClimateWatch — Australia's National Phenology Network, https://www.climatewatch.org.au). The whole of Latin America, Africa and South-East Asia lacks similar initiatives, butwe consider this a worthwhile goal to pursue in the near future. Those networks will become increasingly valuable for conservation managers (Rosemartin et al., 2014) wherever they can obtain cost-effective phenological information, boosting our capacity to preserve natural resources and ecosystem services.

Conflict of interest

The authors declare no conflicts of interest.

Acknowledgements

Our research was supported by Sao Paulo Research Foundation (FAPESP) grants FAPESP-Microsoft Research # 2013/50155-0 and #2010/52113-5; FAPESP-VALE-FAPEMIG # 2010/51307-0); additional funds were provided by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) through grants CNPq/LBA 458038/2013-0 and CNPq PELD Cipó. LPCM holds a research productivity fellowship from CNPq. The following authors received fellowships from FAPESP: BA (grant # 2014/00215-0); STA (grant # 2014/12728-1); BDB (grant # 2014/07700-0); MGGC (grant # 2010/01762-3); LFC (grant # 2014/ 13354-8); DWC (grants # 2011/22635-2, # 2014/01594-4); IM (grant # 2012/21601-0); NMWBR (grant # 2012/12429-9); VGS (grant # 2014/13899-4), and ASS (grant # 2015/17534-3). The authors DFEE, PTL, NCS, ASS and BCV received a fellowship from CAPES (Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior) through the Programa de Pós-graduação em Biologia Vegetal — UNESP, Rio Claro and the Programa de Pós-graduação em Ecologia e Biodiversidade — UNESP, Rio Claro. EB was supported by grants from French Embassy/ UNESP Rio Claro, Chairs 2012 and 2014, STA (grant # 035/016/13- PROPe/CDC) and MGGC (Recém-doutor #292) received support from PROPe/CDC/UNESP; and CAP is supported by CAPES grant PVE 004/ 2012.

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