Towards effective monitoring of tropical phenology: maximizing returns and reducing uncertainty in long‐term studies

Phenology is a key component of ecosystem function and is increasingly included in assessments of ecological change. We consider how existing, and emerging, tropical phenology monitoring programs can be made most effective by investigating major sources of noise in data collection at a long‐term study site. Researchers at Lopé NP, Gabon, have recorded monthly crown observations of leaf, flower and fruit phenology for 88 plant species since 1984. For a subset of these data, we first identified dominant regular phenological cycles, using Fourier analysis, and then tested the impact of observation uncertainty on cycle detectability, using expert knowledge and generalized linear mixed modeling (827 individual plants of 61 species). We show that experienced field observers can provide important information on major sources of noise in data collection and that observation length, phenophase visibility and duration are all positive predictors of cycle detectability. We find that when a phenological event lasts >4 wk, an additional 10 yr of data increases cycle detectability by 114 percent and that cycle detectability is 92 percent higher for the most visible events compared to the least. We also find that cycle detectability is four times as high for flowers compared to ripe fruits after 10 yr. To maximize returns in the short‐term, resources for long‐term monitoring of phenology should be targeted toward highly visible phenophases and events that last longer than the observation interval. In addition, programs that monitor flowering phenology are likely to accurately detect regular cycles more quickly than those monitoring fruits, thus providing a baseline for future assessments of change.     

Evolutionary heritage shapes tree distributions along an Amazon‐to‐Andes elevation gradient

Understanding how evolutionary constraints shape the elevational distributions of tree lineages provides valuable insight into the future of tropical montane forests under global change. With narrow elevational ranges, high taxonomic turnover, frequent habitat specialization, and exceptional levels of endemism, tropical montane forests and trees are predicted to be highly sensitive to environmental change. Using plot census data from a gradient traversing > 3,000 m in elevation on the Amazonian flank of the Peruvian Andes, we employ phylogenetic approaches to assess the influence of evolutionary heritage on distribution trends of trees at the genus‐level. We find that closely related lineages tend to occur at similar mean elevations, with sister genera pairs occurring a mean 254 m in elevation closer to each other than the mean elevational difference between non‐sister genera pairs. We also demonstrate phylogenetic clustering both above and below 1,750 m a.s.l, corresponding roughly to the cloud‐base ecotone. Belying these general trends, some lineages occur across many different elevations. However, these highly plastic lineages are not phylogenetically clustered. Overall, our findings suggest that tropical montane forests are home to unique tree lineage diversity, constrained by their evolutionary heritage and vulnerable to substantial losses under environmental changes, such as rising temperatures or an upward shift of the cloud‐base.     

Inter‐annual monitoring improves diversity estimation of tropical butterfly assemblages

Monitoring programs for diverse tropical butterfly assemblages are scarce, and temporal diversity patterns in these assemblages are poorly understood. We adopted an additive partitioning approach to determine how temporal butterfly species richness was structured at the levels of days, months, and years in five tropical/subtropical sites across three continents covering up to 9 years of monitoring. We found that observed butterfly richness was not uniformly distributed across temporal extents. Butterfly species composition differed across months and years, potentially accounting for the fact that temporal butterfly species richness contributed a high proportion to total species richness. We further examined how species richness of common and uncommon species (> and <0.5% of total abundance, respectively) were structured across temporal extents. The results showed that the common species relative contribution to total species richness was higher at lower‐temporal levels, whereas uncommon species contributed more at higher‐temporal resolutions. This suggests that long‐term sampling will be more effective in capturing patterns of rare species and the total species pool while lower‐temporal level sampling (e.g., daily or weekly) may be more useful in examining common species demographic patterns. We therefore encourage careful consideration of temporal replication at different extents in developing butterfly monitoring schemes. Long‐term monitoring is essential for improvement in the resolution of species estimation and diversity patterns for tropical ecosystems. Abstract in Chinese is available with online material.     

Current issues in tropical phenology: a synthesis

We retrace the development of tropical phenology research, compare temperate phenology study to that in the tropics and highlight the advances currently being made in this flourishing discipline. The synthesis draws attention to how fundamentally different tropical phenology data can be to temperate data. Tropical plants lack a phase of winter dormancy and may grow and reproduce continually. Seasonal patterns in environmental parameters, such as rainfall, irradiance or temperature, do not necessarily coincide temporally, as they do in temperate climes. We review recent research on the drivers of phenophase cycles in individual trees, species and communities and highlight how significant innovations in biometric tools and approaches are being driven by the need to deal with circular data, the complexity of defining tropical seasons and the myriad growth and reproductive strategies used by tropical plants. We discuss how important the use of leaf phenology (or remotely‐sensed proxies of leaf phenophases) has become in tracking biome responses to climate change at the continental level and how important the phenophase of forests can be in determining local weather conditions. We also highlight how powerful analyses of plant responses are hampered at many tropical sites by a lack of contextual data on local environmental conditions. We conclude by arguing that there is a clear global benefit in increasing long term tropical phenology data collection and improving empirical collection of local climate measures, contemporary to the phenology data. Directing more resources to research in this sector will be widely beneficial.     

Small changes in timing of breeding among subarctic passerines over a 32‐year period

Many bird populations in temperate regions have advanced their timing of breeding in response to a warming climate in recent decades. However, long‐term trends in temperature differ geographically and between seasons, and so do responses of local breeding populations. Data on breeding bird phenology from subarctic and arctic passerine populations are scarce, and relatively little data has been recorded in open‐nesting species. We investigated the timing of breeding and its relationship to spring temperature of 14 mainly open‐nesting passerine species in subarctic Swedish Lapland over a period of 32 years (1984–2015). We estimated timing of breeding from the progress of post‐juvenile moult in mist‐netted birds, a new method exploring the fact that the progress of post‐juvenile moult correlates with age. Although there was a numerical tendency for earlier breeding in most species (on average ?0.09 days/year), changes were statistically significant in only three species (by ?0.16 to ?0.23 days/year). These figures are relatively low compared with what has been found in other long‐term studies but are similar to a few other studies in subarctic areas. Generally, annual hatching dates were negatively correlated with mean temperature in May. This correlation was stronger in long‐distance than in short‐distance migrants. Although annual temperatures at high northern latitudes have increased over recent decades, there was no long‐term increase in mean temperature in May over the study period at this subarctic site. This is probably the main reason why there were only small long‐term changes in hatching dates.     

Testing Chronosequences through Dynamic Approaches: Time and Site Effects on Tropical Dry Forest Succession

Chronosequences, commonly used to assess succession, have been questioned because of their failure to project successional trajectories. Here, we develop a simple analytical approach combining both chronosequence and dynamic data to test the power of age of abandonment and site factors to explain and predict succession. The approach proceeds by first fitting statistical models relating age to attribute values (the chronosequence model) and their observed changes (the dynamic model) to test explanatory power. Predictive power is then tested by bootstrapping the chronosequence model to derive confidence intervals for expected changes and comparing them with the dynamic model. Finally, residuals from both models are tested against site factors. The procedure was applied to six attributes (basal area, plant density, mean plant height, species richness, evenness, and composition) of the woody community (plants >1 cm dbh within 0.1‐ha plots) in nine abandoned cattle pastures (0–12 yr) and three old growth tropical dry forests monitored over 6 yr. Age explained 60–97 percent of the variance in community attributes and only 32–57 percent in observed changes. It significantly overestimated basal area and mean height, while species richness and composition were highly predicted. Besides age, management history also explained successional dynamics. Our results suggest age is not necessarily a reliable predictor of short‐term successional dynamics, and explanatory power is not indicative of predictive power. Because of this low reliability, caution is needed when applying chronosequences to evaluate ecosystem services' recovery. The analytical approach developed here contributes to a better exploration of those possible limitations.     

Latitude and protection affect decadal trends in reef trophic structure over a continental scale

The relative roles of top‐down (consumer‐driven) and bottom‐up (resource‐driven) forcing in exploited marine ecosystems have been much debated. Examples from a variety of marine systems of exploitation‐induced, top‐down trophic forcing have led to a general view that human‐induced predator perturbations can disrupt entire marine food webs, yet other studies that have found no such evidence provide a counterpoint. Though evidence continues to emerge, an unresolved debate exists regarding both the relative roles of top‐down versus bottom‐up forcing and the capacity of human exploitation to instigate top‐down, community‐level effects. Using time‐series data for 104 reef communities spanning tropical to temperate Australia from 1992 to 2013, we aimed to quantify relationships among long‐term trophic group population density trends, latitude, and exploitation status over a continental‐scale biogeographic range. Specifically, we amalgamated two long‐term monitoring databases of marine community dynamics to test for significant positive or negative trends in density of each of three key trophic levels (predators, herbivores, and algae) across the entire time series at each of the 104 locations. We found that trophic control tended toward bottom‐up driven in tropical systems and top‐down driven in temperate systems. Further, alternating long‐term population trends across multiple trophic levels (a method of identifying trophic cascades), presumably due to top‐down trophic forcing, occurred in roughly fifteen percent of locations where the prerequisite significant predator trends occurred. Such alternating trophic trends were significantly more likely to occur at locations with increasing predator densities over time. Within these locations, we found a marked latitudinal gradient in the prevalence of long‐term, alternating trophic group trends, from rare in the tropics (<5% of cases) to relatively common in temperate areas (~45%). Lastly, the strongest trends in predator and algal density occurred in older no‐take marine reserves; however, exploitation status did not affect the likelihood of alternating long‐term trophic group trends occurring. Our data suggest that the type and degree of trophic forcing in this system are likely related to one or more covariates of latitude, and that ecosystem resiliency to top‐down control does not universally vary in this system based on exploitation level.     

Disentangling the long‐term effects of disturbance on soil biogeochemistry in a wet tropical forest ecosystem

Climate change is increasing the intensity of severe tropical storms and cyclones (also referred to as hurricanes or typhoons), with major implications for tropical forest structure and function. These changes in disturbance regime are likely to play an important role in regulating ecosystem carbon (C) and nutrient dynamics in tropical and subtropical forests. Canopy opening and debris deposition resulting from severe storms have complex and interacting effects on ecosystem biogeochemistry. Disentangling these complex effects will be critical to better understand the long‐term implications of climate change on ecosystem C and nutrient dynamics. In this study, we used a well‐replicated, long‐term (10 years) canopy and debris manipulation experiment in a wet tropical forest to determine the separate and combined effects of canopy opening and debris deposition on soil C and nutrients throughout the soil profile (1 m). Debris deposition alone resulted in higher soil C and N concentrations, both at the surface (0–10 cm) and at depth (50–80 cm). Concentrations of NaOH‐organic P also increased significantly in the debris deposition only treatment (20–90 cm depth), as did NaOH‐total P (20–50 cm depth). Canopy opening, both with and without debris deposition, significantly increased NaOH‐inorganic P concentrations from 70 to 90 cm depth. Soil iron concentrations were a strong predictor of both C and P patterns throughout the soil profile. Our results demonstrate that both surface‐ and subsoils have the potential to significantly increase C and nutrient storage a decade after the sudden deposition of disturbance‐related organic debris. Our results also show that these effects may be partially offset by rapid decomposition and decreases in litterfall associated with canopy opening. The significant effects of debris deposition on soil C and nutrient concentrations at depth (>50 cm), suggest that deep soils are more dynamic than previously believed, and can serve as sinks of C and nutrients derived from disturbance‐induced pulses of organic matter inputs.     

Long‐term climate impacts on breeding bird phenology in Pennsylvania,USA

Climate change is influencing bird phenology worldwide, but we still lack information on how many species are responding over long temporal periods. We assessed how climate affected passerine reproductive timing and productivity at a constant effort mist‐netting station in western Pennsylvania using a model comparison approach. Several lines of evidence point to the sensitivity of 21 breeding passerines to climate change over five decades. The trends for temperature and precipitation over 53 years were slightly positive due to intraseasonal variation, with the greatest temperature increases and precipitation declines in early spring. Regardless of broodedness, migration distance, or breeding season, 13 species hatched young earlier over time with most advancing >3 days per decade. Warm springs were associated with earlier captures of juveniles for 14 species, ranging from 1‐ to 3‐day advancement for every 1 °C increase. This timing was less likely to be influenced by spring precipitation; nevertheless, higher rainfall was usually associated with later appearance of juveniles and breeding condition in females. Temperature and precipitation were positively related to productivity for seven and eleven species, respectively, with negative relations evident for six and eight species. We found that birds fledged young earlier with increasing spring temperatures, potentially benefiting some multibrooded species. Indeed, some extended the duration of breeding in these warm years. Yet, a few species fledged fewer juveniles in warmer and wetter seasons, indicating that expected future increases could be detrimental to locally breeding populations. Although there were no clear relationships between life history traits and breeding phenology, species‐specific responses to climate found in our study provide novel insights into phenological flexibility in songbirds. Our research underscores the value of long‐term monitoring studies and the importance of continuing constant effort sampling in the face of climate change.     

When and where to move: Dynamic occupancy models explain the range dynamics of a food nomadic bird under climate and land cover change

Globally, long‐term research is critical to monitor the responses of tropical species to climate and land cover change at the range scale. Citizen science surveys can reveal the long‐term persistence of poorly known nomadic tropical birds occupying fragmented forest patches. We applied dynamic occupancy models to 13 years (2002–2014) of citizen science‐driven presence/absence data on Cape parrot (Poicephalus robustus), a food nomadic bird endemic to South Africa. We modeled its underlying range dynamics as a function of resource distribution, and change in climate and land cover through the estimation of colonization and extinction patterns. The range occupancy of Cape parrot changed little over time (ψ = 0.75–0.83) because extinction was balanced by recolonization. Yet, there was considerable regional variability in occupancy and detection probability increased over the years. Colonizations increased with warmer temperature and area of orchards, thus explaining their range shifts southeastwards in recent years. Although colonizations were higher in the presence of nests and yellowwood trees (Afrocarpus and Podocarpus spp.), the extinctions in small forest patches (≤227 ha) and during low precipitation (≤41 mm) are attributed to resource constraints and unsuitable climatic conditions. Loss of indigenous forest cover and artificial lake/water bodies increased extinction probabilities of Cape parrot. The land use matrix (fruit farms, gardens, and cultivations) surrounding forest patches provides alternative food sources, thereby facilitating spatiotemporal colonization and extinction in the human‐modified matrix. Our models show that Cape parrots are vulnerable to extreme climatic conditions such as drought which is predicted to increase under climate change. Therefore, management of optimum sized high‐quality forest patches is essential for long‐term survival of Cape parrot populations. Our novel application of dynamic occupancy models to long‐term citizen science monitoring data unfolds the complex relationships between the environmental dynamics and range fluctuations of this food nomadic species.