Recipient Organization
UNIVERSITY OF CALIFORNIA, RIVERSIDE
(N/A)
RIVERSIDE,CA 92521
Performing Department
Evolution, Ecology & Organismal Biology
Non Technical Summary
Mutually beneficial interactions between species are critical to the stability and functioning of ecological communities and the provision of ecosystem services, such as pollination. In the mutualistic interaction between flowering plants and pollinators, plants receive pollen transfer services and pollinators receive nectar and pollen nutritional resources. To facilitate efficient pollination and resource extraction, plant-pollinator mutualisms require not only the timing of flowering and pollinator foraging but also the traits of each partner to match. However, changing environmental conditions, such as warming temperatures, may cause mismatches in the timing of these key phenological events and the traits of flowers and pollinators, potentially reducing the reproductive success of both partners and ultimately leading to the disruption of the mutualism. This project tests the hypothesis that environmental change will generate phenological mismatches between plants and pollinators and alter traits, thereby threatening an ecologically and economically critical mutualism. Specifically, this research will:(1) experimentally test, for the first time, how simultaneous warming affects plant and pollinator phenology; and (2) determine how warming affects plant and pollinator morphological, physiological, and behavioral traits that shape their interactions.Using foraging arenas in temperature-controlled greenhouses, native wildflowers and solitary bees will be exposed to elevated temperatures before flowering and emergence, respectively, to test how the phenology and phenotype of these interdependent species respond to four different levels of concurrent warming over multiple generations. The effects of simultaneous warming will be quantified for (i) the timing of plant and pollinator life history events, such as the start, peak, and end of flowering and bee nesting activity; and (ii) traits of plants and bees, such as nectar volume and foraging specialization. This project will yield ecological insight into how plant-pollinator interactions are affected when partner species shift in time, revealing to what extent plant and bee phenology respond differently to the same environmental conditions. This research will enable prediction of how pollination will be affected by future environmental change, allowing us to determine how likely environmental change is to disrupt species interactions and the provision of ecosystem services.
Animal Health Component
10%
Research Effort Categories
Basic
90%
Applied
10%
Developmental
0%
Goals / Objectives
Few studies have examined the emergent effects of climate change on mutualistic species interactions, which often require phenological synchrony to generate key ecological services such as pollination, seed dispersal, and nitrogen fixation (Kiers et al. 2010). Hence, although climate change-induced shifts in the phenologies of individual species are well-documented, the likelihood of interacting species experiencing differential shifts is little-understood (de la Torre Cerro and Holloway 2020). However, several characteristics have been posited to be related to the risk of partner species becoming phenologically mismatched as a result of climate change. Mutualisms that involve symbiotic, continuously interacting, symmetrically specialized partners are predicted to be least susceptible to mismatches, in part because such partners have likely been shaped by selection to respond to the same abiotic cues in the same ways(Rafferty et al. 2015). Moreover, for mutualisms to persist over evolutionary time scales, the traits of partner species must enable interactions that confer mutual fitness benefits. If, for instance, anthropogenetic nitrogen deposition reduces nitrogen limitation, plants may cease to form nodules, disrupting the mutualism between legumes and nitrogen-fixing rhizobia(Regus et al. 2017). More subtle changes in partner behavioral traits and resource allocation can also alter the costs and benefits of mutualisms, as when pollinators switch to nectar-robbing or when mycorrhizae shift resources away from the host and toward storage. Whether changes in traits represent plastic or genetic changes or both (and plasticity itself may be selected for), traits can dictate the incidence and net benefits of mutualistic species interactions, and thereby influence ecosystem services (Kiers et al. 2010).The first goal of this proposal is to study interactions among wildflowers and solitary bees to determine how the phenologies of these interdependent species respond to experimental warming in common garden conditions. Phenologicalsynchrony between mutualists is critical to fitness and population persistence, as illustrated by symmetrically specialized, obligate plant-pollinator interactions, such as those between yuccas and yucca moths and figs and fig wasps, where asynchrony equals reproductive failure (Rafferty et al. 2015). Likewise, generalized mutualists act as agents of natural selection (e.g., Aigner 2005); thus, changes in interaction strengths and partner switching will alter selection pressures, even if climate change-driven phenological shifts do not eliminate overlap among species (Gienapp et al. 2014). Whether populations will be able to adapt rapidly enough to keep pace with climate change is an open question (Quintero and Wiens 2013). In antagonistic interactions, such as those between plants and insect herbivores, asynchrony may be the baseline, and increased asynchrony would be expected to benefit the plant but detrimentally affect the fitness of the insect herbivore(Singer and Parmesan 2010). In contrast, given the mutualistic nature of plant-pollinator interactions, it is expected that both sets of species would be under selection to maintain phenological synchrony. However, optimal overlap may differ for each focal species in duration and timing relative to the abiotic environment and the phenologies of other community members. As a result, it is not straightforward to predict the outcome of phenological shifts when species are placed in the context of their interactions with other species.The second goal of this proposal is to measure a suite of plant and pollinator morphological, physiological, and behavioral traits to determine the responses of both partners to warming. In addition to altering phenology, climate change will directly affect plant and pollinator physiology and behavior. As a result, many traits that shape interactions are likely to be altered in both plants and pollinators. In concert with changes in phenological overlap, plant physiological responses to warming could modify floral resource availability and reproductive output of pollinating insects as well as plants. Similarly, pollinator responses could affect patterns of pollen flow and pollination success of flowering plants along with pollinator fecundity. Plant and pollinator traits that are likely to be affected by warming and are important for their interactions include many floral traits involved in pollinator attraction and reward, as well as pollinator traits involved in flower handling and foraging efficiency. Floral display size, flower longevity, floral odor, and nectar and pollen quantity and quality are among the traits known to affect pollinator visitation and to respond to warming. On the pollinator side, body size and mass and foraging behavior are non-phenological traits that shape interactions with plants and are affected by warming temperatures. When warmed, solitary bee larvae and pupae tend to have lower mass and develop into smaller adults. Changes to bee foraging activity patterns and body size will affect plant pollen flow and fitness(reviewed by Scaven and Rafferty 2013). We will quantify these traits in wildflowers and bees simultaneously subjected to different temperature regimes to generate a comprehensive view of how warming will reshape this mutualistic interaction. Although these trait alterations are likely to accompany phenological shifts, the various responses (phenological, morphological, physiological, behavioral) have generally been studied separately. The proposed work will integrate these responses by providing quantitative data on traits and documenting whether they are altered in conjunction with altered phenology.Traits can be altered as a by-product of phenological responses because, for example, those responses can expose organisms to new combinations of abiotic conditions, such as temperature and photoperiod(Memmott et al. 2007).Physiological stress that is expressed in the form of altered traits will likely alter interactions, providing another mechanism by which warming could disrupt plant-pollinator interactions and change the costs and benefits of the mutualism.The proposed experiment will be the first to test how concurrent warming affects plant and bee interactions under controlled settings. We will leverage a novel experimental approach, simultaneously exposing plants and dormant bees to the same temperature regimes before flowering and emergence, respectively, to test how warming affects a key mutualistic interaction. We will measure the effects of warming on the timing of life history events and traits, which will inform our understanding of whether warmer spring temperatures will disrupt plant-pollinator interactions. In doing so, this project will yield ecological insight into how plant-pollinator interactions are affected when partner species shift in time, revealing to what extent plant and bee phenology respond differently to the same environmental conditions. The proposed work will also provide insight into the evolutionary processes shaping plant and pollinator responses to climate change by quantifying the phenotypic effects of different temperature treatments.ObjectivesTheoverallresearch objective of this project is to test the hypothesis that climate change will generate phenological mismatches between plants and pollinators and alter traits, thereby disrupting an ecologically and economically critical mutualism. To test this hypothesis, I propose two objectives:to test how simultaneous warming affects plant and pollinator phenology, specifically the timing of flowering and emergence of solitary bees; andto determine how warming affects plant and pollinator morphological, physiological, and behavioral traits that shape their interactions, such as nectar and pollen production and bee body size.
Project Methods
Objective 1MethodsWe will expose plants and bees to elevated temperatures prior to flowering and emergence, an approach that will test how the same degree of warming affects the phenologies of both taxa. Within foraging arenas, we will create experimental communities with potted wildflowers known to be visited by the focal bee species,Osmia lignaria(Megachilidae; blue orchard bee), a solitary bee native to the U.S. that is used as a commercial pollinator, is experimentally tractable, and has been well-studied in terms of its physiology and life cycle(Kemp and Bosch 2005, Bosch et al. 2010, Sgolastra et al. 2011).Osmia lignariais active in the spring and overwinters inside narrow holes or hollow reeds as an adult inside its cocoon (rather than as a pupa). We will obtain dormant adult bees from a regional supplier in the fall before the experiment begins. Prior to placement in foraging arenas, the bees will be maintained in diapause in an environmental chamber at 4 °C (wintering) for 150 days.Osmia lignariaemergence phenology is sensitive to the timing of spring warming (Slominski and Burkle 2019). ForO. lignariathat have been wintering at 4 °C for 150 days, it generally takes 5 and 7 days for males and females, respectively, to emerge after being exposed to warmer temperatures (incubation at 20 °C; males emerge 1-3 days before females). This 5- and 7-day pre-emergence period can be shortened with increasing incubation temperatures (Bosch and Kemp 2001, 2003), suggesting warmer springs can accelerate emergence. After emergence, adult females mate and begin nesting 1-2 days later (Bosch and Kemp 2001). Although individual nesting females typically live for 20 days (Bosch and Kemp 2001), the entire nesting period can last 4-6 weeks(Kemp et al. 2004), and during this time females forage for floral resources, laying 7-12 eggs (2-4 females and 5-8 males), which they provision with pollen and nectar, in 2-4 nests (Bosch and Kemp 2001). ThoughO. lignariacollects pollen from multiple plant families (is polylectic), pollen from each of the proposed experimental plant species constitutes an important floral resource in its nest provisions in California(Boyle et al. 2020).To study plant phenological responses, we will use the annual wildflowersPhacelia campanularia(Boraginaceae),Collinsia heterophylla(Plantaginaceae), andNemophila menziesii(Boraginaceae), all of which will be grown in greenhouses from seeds collected from natural populations in Southern California, maximizing the chance that our experimental plants originate from populations that are adapted to the same climate as our experimental bees. All 3 species bloom in the spring, overlapping for all of March and April and arehighly reliant on pollinators for seed productionand are visited byO. lignaria(Wood 2010, Boyle et al. 2020), likely an effective pollinator.The warming treatments will begin once plants and bees are placed together in mesh foraging arenas (1.75 m H?1 m W?1.75 m L3 m3) to create experimental communities. Inside each arena, we will place 45plants (15 of each species) at the developmental stage that corresponds to approximately 5 days pre-flowering onset under ambient temperature (the amount of time needed for maleO. lignariato emerge post-diapause at 20 °C).Under this setup, if both plants and bees respond similarly to warming, they should flower and emerge synchronously. The proposed number and diversity of plants, upon flowering, should provide adequate nectar and pollen for the 10O. lignaria(6 males, 4 females, the recommended sex ratio) that will be placed (in diapause) inside a parental nesting blockin each arena.Each arena will also contain mud and water for nest cell construction and 2 empty offspring nesting blocks (with observation windows) in which female bees will lay eggs and provision brood within removable straws. These methods are based on protocols forO. lignarianesting (Bosch and Kemp 2001).We will expose plants and bees to 4 temperature treatments: ambient, +2 °C, +4 °C, +6 °C. These treatments are within the range of projected scenarios of warming from 16 global climate models that are part of the sixth phase of the Coupled Model Intercomparison Project (CMIP6), which by 2100 predict warming of 1.2-7.2 °C per 100 years depending on the Shared Socioeconomic Pathway(Fan et al. 2020). Each treatment will be replicated in 10 arenas, and each set of 10 arenas will be placed into different greenhouse rooms with controlled temperature settings. Thus, we will use 4 greenhouse rooms to achieve the temperature treatments, and we will place data loggers (temperature, humidity, and light) within each arena.In total, the parental generations will comprise: 45 plants and 10 bees per arena?10 arenas per treatment?4 treatments = 1800 plants and 400 bees.Objective 2MethodsTo measure the effects of warming on plant traits, we will use an additional 9 control plants (3 of each species, for a total of 9 plants per arena?10 arenas per treatment?4 treatments = 360 control plants) placed in pots inside each arena but separated from the bees by a divider, such that they experience the same environmental conditions as the plants from which bees forage.From a subset of flowers from each control plant throughout the flowering period, we will collect nectar and pollen to quantify reward quantity and quality. Nectar volume per flower will be measured via microcapillary tubes, and sugar content will be quantified with a handheld refractometer(Corbet 2003). Pollen will be collected, massed, and tested for viability (Rodriguez-Riano and Dafni 2000).We will measure floral traits and rewards for individual flowers throughout the flowering period of each plant, sampling 3 flowers per plant per arena per time point.In quantifying traits in bees, we will focus on body size and behavior. To obtain body mass, we will weigh each dormant bee at the same time that we individually mark them in the cold room to avoid repeated handling. Once the nesting period has ended and all adult bees have died, we will monitor the offspring nesting blocks for pupae. Once all larvae have pupated, we will weigh each nesting straw and divide the total weight by the number of pupae to gain an estimate of pupa mass. After pupae have metamorphosized into adults in their cocoons, we will weigh and sex each individual at the time they are marked for future iterations of the experiment. Sex can be gauged by cocoon size and position in the nesting straw: cocoons containing females are ~2 mm longer and are located near the back of the straw, whereas those containing males are shorter and are near the nest entrance (Bosch and Kemp 2001).The bee behavioral traits we will quantify are foraging specialization and handling time. Specialization on certain flowers can take 3 forms: floral constancy, fixed preferences, and labile preferences(Waser 1986). Floral constancy is the behavior of restricting visits to a subset of species in bloom, ignoring flowers of other species that offer comparable or greater rewards, resulting in specialization at the individual level (Waser 1986, Chittka et al. 1999). Although constancy is often associated with social bees,O. lignariais known to exhibit floral constancy in various contexts(Cripps and Rust 1989,Amaya-Márquez et al. 2008). Fixed preferences, common in oligolectic bees, reflect static affinities, whereas labile preferences reflect optimal foraging (Waser 1986). Because we will collect data on floral abundances and rewards, we can distinguish between these types of specialization. We will collect foraging data by documenting the flower visits of individual focal bees in 10-min observation periods (1 10-min period per day per arena; ~6.5 hr per day and ~4.5 hr per arena over 4 wk; multiple observers will collect data concurrently).