Exploitation of different food resources during periods of resource scarcity, as well differences in foraging heights, may allow these closely related primates to live in sympatry. Tutin and Fenandez compared the diets of sympatric chimpanzees and gorillas at Lope, Gabon and found a high degree of dietary overlap, particularly for fruits. Importantly, they found that the diets of these two primates diverged most during periods of fruit scarcity, and that gorillas incorporated more leaves, stems and bark into their diets, while chimpanzees maintained high levels of frugivory even during times when fruit was scarce. Dietary divergence during periods of resource scarcity potentially allows primates to mitigate the effects of feeding competition, and the authors interpreted dietary divergence as evidence of niche separation in these two sympatric primates. In our study, we provide further evidence that dietary divergence is an important mechanism in which closely-related, sympatric primate species may mitigate feeding competition.Figs have been classified as an important food for primates throughout the tropics, and are often fallback foods, blueberries in containers growing due to their relatively constant availability and increased representation in the diet when other fruit is scarce, but in some sites figs have been identified as “preferred” or over-selected.

Differences between sites have been attributed to differences in the quality of non-fig fruits, with figs being fallback foods in sites where there are other high-quality fruits, and figs being preferred foods in sites where high-quality non-fig fruits are lacking. In our study, both gibbons and leaf monkeys showed a marked decrease in fig consumption when fruit availability increased. In addition, the proportion of figs included in gibbon and leaf monkey diets was similar . We analyzed figs from two perspectives: 1) as a genus in the selectivity analyses which did not take into account temporal variation of food availability, and 2) as a food class when investigating the proportion of stems included in the diet, which did take into account changes in food availability over time. In the selectivity analyses, the genus Ficus was an important and preferred food because gibbons select figs more than would be expected based on the stem density of figs. Use of the food class “figs” decreased with an increase in overall fruit availability. In this context, figs were a fallback food because they were eaten in periods of low fruit availability, and consumption was inversely correlated with preferred food availability. Thus, as a food class, figs conformed to the definition of a fallback food, but in the selectivity analyses that excluded temporal variation in food availability, gibbons preferred figs. This difference occurred because figs were more consistently available than most genera and gibbons disproportionately feed on genera that are consistently available over time. Previous research from our study site found that the number of gibbon feeding observations on figs was negatively correlated with availability of ripe fruit, and thus figs were a fallback food for gibbons.

We present the results of over five additional years of new feeding observations and find a consistent result that the proportion of figs in gibbon diets decrease as fruit availability increased. Our study therefore substantiates the earlier finding that figs are an important food class for gibbons during periods of low fruit availability, and highlights that this pattern is stable over long periods.Characterizing primate diets has important conservation implications. For example, preferred and fallback foods may be important factors influencing primate population density. Gibbon population density at Gunung Palung National Park is highly correlated with the abundance of their main fallback food, while leaf monkey population density is highly correlated with the abundance of their preferred foods. This trend may not be consistent across regions, as colobine biomass was correlated with proportion of trees that are legumes , which are generally preferred foods, in Asia but not in Africa –although differences in sampling intensity, study duration and study design may also contribute to these differences. This potential for regional variation in preferred and fallback foods, as well as the implications for primate ecology, highlights the needs for intensive sampling of a broad range of diets of various primate species and populations. In addition, anthropogenic climate change is and will continue to impact plant reproductive phenology. In the face of a changing climate, especially in hyper-variable dipterocarp forests where masting is correlated with El Niño events, long-term data sets can provide reference points for primate feeding ecology, which may be useful to assess how climate change affects primate species and their food resources.

Feeding ecology studies can provide insights into the range of resources used by primates, and may allow for predictions about how habitat disturbance, such as selective logging of primate food trees, will influence their ecology and likelihood of persistence. Feeding ecology studies can also be used to inform conservation actions for specific populations and meta populations. For example, an in-depth knowledge of primate feeding ecology can be used in habitat restoration projects, when the goal is to minimize periods of resource scarcity for primates in restored habitats.Plant phenology, the periodic timing of plant life cycle events, is innately linked to exogenous climatic variables that affect plant development, such as temperature, photoperiod, and nutrient and water availability, as well as other abiotic and biotic factors . Additionally, endogenous genome-encoded factors such as dynamic internal photosynthate source-sink pathways, intricate phytohormone signaling networks, and other developmental regulatory processes mediate the transition between phenological stages . The timing of specific developmental stages, such as flowering, can determine a plant’s geographic distribution range as well as determine crop yield and productivity . Alterations in plant phenology can also have a cascading effect on the fitness of organisms that depend on those specific plants for nutrient acquisition, such as pollinator species . Citrus is a significant economic crop and provides several health benefits because of the myriad of nutrients, antioxidants, vitamins, minerals, and dietary fiber found in fresh and juiced citrus fruits . Citrus varieties are grown across the globe, and because of this, citrus phenology is well characterized to guide management strategies of different varieties for specific climatic conditions. Phenological modeling of citrus has focused primarily on buds, flowers, and fruit and is used to predict bloom time across different growing regions . This has implications for protecting flowers from floral pests and pathogens by allowing growers to time spray applications in an informed manner . Citrus flowers are a significant source of nectar related to honey production, particularly in California’s Central Valley. As such, bloom timing models are also important for the beekeeping industry . In addition, bloom time and duration models can be extrapolated to predict fruit set , and these performance models can provide yield predictions. Soil and rhizosphere microbiomes can drive changes in flowering time in the herbaceous perennial plant Boechera stricta, a wild relative of Arabidopsis , and affect other aboveground plant traits in the annual plant system Brassica rapa . However, questions about microbiome shifts associated with transitions between phenological stages have not been addressed in perennial trees, particularly domesticated evergreens like citrus . Citrus phenology models primarily take into account temperature and number of degree days above a certain threshold temperature but, to the best of our knowledge, have not incorporated studies on the microbial communities associated with transitions across phenological stages. The citrus microbiome is an emerging prototype for understanding microbial contributions to plant health in a perennial arboreal crop system . Due to its well-defined phenology, planting blueberries in containers citrus is an ideal system to investigate the interplay between host phenology and microbial community composition. Several seminal studies in annual and short-lived perennial plants have characterized changes in rhizosphere and root microbiome composition across plant developmental cycles, suggesting that host phenology drives these alterations . However, Dombrowski et al. suggests that initially microbiota are sequentially acquired resulting in community changes as the host ages but eventually the microbiome matures and stabilizes, functioning independently from host development . Another recent study supports the idea that time is a stronger predictor of microbiome composition than plant developmental stage . This prompts discussion on whether these community shifts are a consequence of tissue age and a microbiome maturation process or if these changes are driven by plant phenology.

In addition to producing and maturing leaves and roots throughout the year, long-lived evergreen perennial plant systems retain mature leaves for 1 to 3 years , which allows for selection of leaf tissues of similar age and developmental cohort across phenophases. Because of these features, we utilized this system to help decouple tissue age from host phenological effects and tested the hypothesis that host phenology acts as a driver of community compositional shifts within the above ground and below ground microbiomes of citrus. Indeed, we determined that the significant shifts in both diversity and composition of the microbial community structure were driven primarily by host phenological stages and not exogenous environmental factors such as rainfall, hours of irrigation, or temperature. Foliar communities were more affected by host phenology than root microbiomes, which were comparably more stable. Interestingly, major alterations in foliar microbial community composition correlated with the shifts in source to-sink pathways of carbohydrate transit, namely, during the transition from floral bud development to full flowering to fruit set. More specifically, subsets of these taxa displayed temporal turnover patterns indicating that specific taxa were enriched as trees shifted to reproductive growth associated with fruit production. We also observed taxa typically associated with pollinator species that were substantially enriched only during flowering, suggesting that these microbes were introduced into the foliar microbiome as microbial immigrants via an insect-mediated dispersal mechanism. In agricultural plant systems, comprehensive microbiome studies allow researchers to place an emphasis on how the microbiome as a whole functions to promote overall plant health by a variety of mechanisms, such as enhancing nutrient uptake or resisting pathogen ingress to promote a sustainable agroecosystem. Uncovering links between plant phenology and shifts in microbiome structure is the first step toward a mechanistic understanding of microbiome resilience over cyclical development in a perennial plant host. In addition, this can further serve as the foundation to understanding how the microbiome responds to changes in host development and, in turn, if microbiome community structure can influence host phenological transitions.We focused our study on seven citrus phenophases that included spring vegetative shoot flush, referred to as “flush” , early floral bud break and development , full flowering , fruit set , exponential fruit growth and development, referred to as “fruit development” , color break , and mature fruit . Citrus phenological stages can overlap on individual trees, and some stages span multiple months; thus, some stages include multiple months of sampling . Initially, we accessed alpha diversity or the diversity within a sample, in this case the number of operational taxonomic units . Overall, bacterial and fungal leaf microbiomes had the most significant shifts in alpha diversity across phenological stages compared to those of the root microbiomes. Specifically, alpha diversity in both the leaf bacteriome and mycobiome remained consistent as trees transitioned from leaf flush to flowering . Following full flowering, there was a significant increase in alpha diversity in the leaf bacteriome and mycobiome at fruit set . Species richnesswithin the leaf bacteriome significantly decreased when trees transitioned from fruit growth and development to color break and mature fruit stages. Despite being relatively stable across the study, root bacteriome alpha diversity peaked during full flowering. Similar to the overall leaf microbiome, the root mycobiome had the highest alpha diversity during fruit set . Our study did not discriminate between rhizoplane and endophytic root microbiota, nor was it possible to select feeder roots of a specific age cohort. Future work that separates these compartments in similarly aged roots may reveal more finely resolved shifts in species richness associated with these root environments.Although climatic variables can be difficult to uncouple from plant development variables, the greatest amount of the variation in the data was attributed to the host phenological stage for all four communities . Interestingly, the community composition of leaf bacteriome and mycobiome was influenced by host phenology more than that of root communities, indicating that changes in host phenology had a larger influence on diversity within foliar microbiomes than in root microbiomes.