Divergent responses of generalist and specialist pollinators to experimental drought: Outcomes for plant reproduction

Abstract

Drought is an increasingly important consequence of climate change. Drought often causes plants to alter patterns of resource allocation, which in turn can affect how plants interact with other species. How these altered interactions subsequently influence plant reproductive success remains incompletely understood and may depend on the degree of specialization exhibited by antagonists and mutualists. Specialist pollinators, for example, are dependent on floral resources from their obligate hosts and under drought conditions may thus indiscriminately visit these hosts (at least in certain circumstances). Generalist pollinators, in contrast, may only forage on host plants in good condition, given that they can forage on other plant species. We tested this hypothesis and its consequences for plant reproduction in squash (Cucurbita pepo) grown along an experimental moisture gradient ranging from dry (growth and flowering compromised) to wet conditions. Floral visitation increased with plant soil moisture for generalist honey bees but was independent of plant soil moisture for specialist squash bees. Pollen production increased with plant soil moisture, and fluorescent pigments placed on flowers revealed that pollinators primarily moved pollen from male flowers on well‐watered plants to the stigmas of female flowers on well‐watered plants. Seed set increased with increasing plant soil moisture but, notably, was higher in bee‐pollinated plants compared to plants pollinated by hand with an even mix of pollen from plants grown at either end of the experimental moisture gradient. These results suggest that superior pollen rewards, perhaps combined with selective foraging by generalists, enhanced reproductive success in C. pepo when plant soil moisture was high and more generally illustrate that pollinator behavior may contribute to how drought conditions affect plant reproduction.

Temperature and soil moisture manipulation yields evidence of drought‐induced pollen limitation in bee‐pollinated squash

“…Like other Cucurbita , C. pepo attracts a variety of insect pollinators, primarily bees, which include generalists, such as the western honey bee ( Apis mellifera ), and specialists, such as squash bees ( Xenoglossa [formerly Peponapis and Xenoglossa ]; Freitas et al., 2023 ), that require pollen from cucurbits to reproduce (Hurd et al., 1974 ). For the above reasons and because of the economic importance of cultivated squash (Gallai et al., 2009 ; McGrady et al., 2020 ), interactions between Cucurbita and their pollinators are extensively studied (Artz & Nault, 2011 ; Delgado‐Carrillo et al., 2018 ; Hoehn et al., 2008 ; Hurd et al., 1971 ; Hurd et al., 1974 ; Tepedino, 1981 ), including in the context of how climate change affects squash reproduction (Gambel & Holway, 2023 ; Hoover et al., 2012 ).…”

“…Heat stress in plants can lower the frequency (de Manincor et al., 2023 ; Descamps, Jambrek, et al., 2021 ) and duration (de Manincor et al., 2023 ) of bee visits and lead to complicated effects on plant–pollinator networks (Moss & Evans, 2022 ). Similarly, plants subjected to drought conditions can also experience reduced bee visitation (Al‐Ghzawi et al., 2009 ; Burkle & Runyon, 2016 ; Gambel & Holway, 2023 ; Glenny et al., 2018 ; Rering et al., 2020 ). In some cases, however, pollinators may visit flowers more often but for shorter lengths of time because of reductions in floral resources caused by soil‐moisture limitation (Waser & Price, 2016 ).…”

“…Recent attention to how climate change influences plant–pollinator interactions recognizes that warming or drought can disrupt interactions among plants and pollinators with potentially negative consequences for plant reproduction (de Manincor et al., 2023 ; Gambel & Holway, 2023 ; Moss & Evans, 2022 ; Rering et al., 2020 ). To date, research has mostly addressed how variation in temperature (de Manincor et al., 2023 ; Moss & Evans, 2022 ) or soil moisture (Al‐Ghzawi et al., 2009 ; Rering et al., 2020 ; Waser & Price, 2016 ) impact plant reproductive allocation and how pollinator behavior responds to changes in floral resources.…”

“…To date, research has mostly addressed how variation in temperature (de Manincor et al., 2023 ; Moss & Evans, 2022 ) or soil moisture (Al‐Ghzawi et al., 2009 ; Rering et al., 2020 ; Waser & Price, 2016 ) impact plant reproductive allocation and how pollinator behavior responds to changes in floral resources. Direct effects (i.e., plant responses) and indirect effects (i.e., pollinator responses) can interact with one another, however, in ways that may ultimately compromise plant reproduction (Gambel & Holway, 2023 ). Reductions in pollen quantity (number of grains) or quality (viability) caused by warming or soil‐moisture limitation, for example, could result in pollen limitation even in cases when rates of pollinator visitation remain unchanged.…”

“…We tested this final prediction using results from prediction (i) and data from a second experiment that specifically tested how variation in physical conditions affected pollen viability. This study is one of few (Gambel & Holway, 2023 ) that attempts to separate the direct effects of warming and soil‐moisture limitation on plant reproduction from those effects that result from pollinator foraging behavior. Given that warming and soil‐moisture limitation commonly impact reproductive allocation in animal‐pollinated plant species, pollinator‐mediated effects are likely widespread.…”