An introduction to the Special Issue on Global Change and Plant Reproduction

Anthropogenic global change (AGC) is the umbrella phrase that describes the numerous environmental impacts humans are having on the global environment, with consequences for much of life, including reproduction by plants. The series of changes encompassing AGC are termed drivers of global change and can be considered in two general categories (Table 1; Vitousek, 1992, 1994; Sala et al., 2000; Sage, 2020). The first category are drivers that directly alter the chemical composition and energy status of the fluid envelopes surrounding the earth, namely Earth’s atmosphere, fresh-water bodies and oceans. Drivers of this nature include rising concentrations of atmospheric CO2, methane and nitrous oxide and the associated enhancement of energy in the oceans and atmosphere through their heat trapping ability as greenhouse gases (Stocker et al., 2001; Forster et al., 2024). The enhancement of atmospheric CO2 also directly affects organisms through stimulation of photosynthesis and reduction of transpiration in plants, and as a signalling molecule for many plants, animals and fungi (Sage, 2002, 2020). The second general category of drivers are those whose impacts are regional in nature but so pervasive they scale to alter the global environment (Vitousek, 1994). Such drivers include land use change, altered soil and water biogeochemistry, the spread of exotic species, pesticide pollution, and overexploitation of natural species (Table 1; Jaureguiberry et al., 2022). While climate change and other forms of global change have occurred over geological time and influenced patterns of biotic evolution, AGC is considered unique relative to past change in that i) numerous drivers such as widespread pesticide use have no natural precedent; ii) multiple drivers are intensifying simultaneously, with interactive effects and feedbacks creating novel and often synergistic outcomes; and iii) the current rate of global change is generally far greater than anything observed through geological time (Rockström et al., 2009; Steffen et al., 2011; Sage, 2020). The combination of novel agents and rapid changes of multiple interacting drivers exceed natural norms and thus can overwhelm an individual’s ability to acclimate, the evolutionary potential of populations, and the resilience of ecosystems and biomes (Bell and Collins, 2008; Brook et al., 2008; Franks et al., 2014; Jaureguiberry et al., 2022). In plants, the reproductive phases are widely considered the most vulnerable stages of the life cycle, and thus may be particularly vulnerable to the combined effects of AGC (Harper, 1977; Baskin and Baskin, 2014; Parmesan and Hanley, 2015). For example, substantial declines in insect pollinators and animal dispersers have already been noted, during what is widely considered to be early stages of climate change (Settele et al., 2016; Thomann et al., 2013; Pérez-Méndez et al., 2016; Wagner, 2020). However, not all plants will suffer from AGC, and some species will do well in an altered world, either because they are resilient to AGC drivers or because their combination of traits are favored by AGC (Brooks et al., 2004; Sage, 2020). Already, AGC drivers have enabled certain species to break out of their ecological constraints and become invasive species, some of which further exacerbate other global change drivers such as climate and land cover change (Vitousek et al., 1997; Stachowicz et al., 2002). Ten anthropogenic global change drivers impacting the biosphere and their consequences for plant reproduction. Adapted from Sage, (2020) based on (Vitousek, 1994; Postel et al., 1996; Sala et al., 2000; Steffans et al., 2004 and; Pérez-Méndez et al., 2016). Ten anthropogenic global change drivers impacting the biosphere and their consequences for plant reproduction. Adapted from Sage, (2020) based on (Vitousek, 1994; Postel et al., 1996; Sala et al., 2000; Steffans et al., 2004 and; Pérez-Méndez et al., 2016). If reproduction is indeed the most sensitive aspect of plant biology to AGC, then it follows that a comprehensive understanding of AGC consequences would emphasize the study of AGC impacts on aspects of plant reproduction. With this in mind, the editors at Annals of Botany commissioned this special issue on Plant Reproduction in a Changing Global Environment. This issue follows numerous Annals of Botany special issues with an AGC theme, notably, Plants and Climate Change (2015, volume 116: 6); Developing Sustainable Bioenergy Crops for Future Climates (2019, 124:4) and Macroalgae in a Changing World (2024, 133:1). Of the AGC drivers, climate change has received most of the recent attention from both the academic community and the public and is viewed by many as the existential crisis of our time (see for example https://climate.mit.edu/ask-mit/why-do-some-people-call-climate-change-existential-threat). From the perspective of the world’s biota, this view is one-sided, because even if we stop climate change, the diversity of the world’s flora, fauna and fungi could still collapse from the action of the other global change drivers (Sage, 2020; Jaureeguiberry et al., 2022; Antonelli et al., 2023). Our goal with this special issue is to extend beyond climate change to include how the multiple AGC drivers affect plant reproduction in its entirety, from the initiation of floral buds to the establishment of seedlings (Fig. 1). As Fig. 1 shows, successful reproduction requires transitioning through at least nine distinct developmental phases, and within each phase, there are multiple attributes potentially affected by AGC. Each attribute represents a potential point of reproductive failure, and thus could be essential for a comprehensive understanding of plant responses to AGC and attempts to predict the future health of species, ecosystems and the biosphere. The ability to predict winners and losers in an altered world will often come down to how individual attributes of the reproductive system are affected by AGC, as discussed by papers in this special issue. A schematic showing phases of the seed plant life cycle, with reproductive phases highlighted by a grey background, and vegetative phases by light blue. Based on descriptions in Harper, (1977). Key parameters associated with each life cycle stage are listed beside the stages. All can be affected by anthropogenic global change. Through the eight reviews and 18 original reports in this special issue, responses of many reproductive traits to one or more AGC drivers are presented, allowing readers to develop a broader appreciation of how plant reproduction may be influenced by global change, and what are some of the priorities for future investigation. Most of the topics emphasize climate change effects on the flowering to fertilization phases of plant reproduction, addressing for example flowering phenology (Collins et al., 2024; Zeng et al., 2024; Zhou et al., 2024), pollinator foraging (Rose-Person et al., 2024), floral traits and nectar production (Basnett et al., 2024), and pollen tube growth in conifers (Hsu and Kim, 2024). Collins et al. for example, observed earlier flowering induced by experimental warming dramatically enhances reproductive fitness of arctic tundra plants, while Zhou et al. observed that earlier precipitation in a temperate steppe lengthened reproductive duration, which their analysis suggests would alter species composition within communities. In recognition that anthropogenic climate change has been progressing for at least a few decades, Pareja-Bonilla et al., (2024) report here that dramatic changes are already being observed in the flowering phenology within Mediterranean shrub communities, while Zeng et al., (2024) show that short-day plants are advancing flowering time more than long-day plants in response to recent warming. Brunet et al., (2024) review flowering to seed set in the context of climate change effects on moisture regimes. Drought is predicted to increase in frequency and intensity in future climates due to a combination of altered precipitation regimes, greater rates of evaporation in warmer climates, and increased human appropriation of fresh-water resources (Caretta et al., 2022). As Brunet et al. discuss, drought can hinder most facets of flowering, including flower size and nectar volume, as well as less obvious traits such as production of floral volatiles, an important olfactory queue for insects. Consistently, in their study on bee-pollinator preferences in the drylands of southern California, Rose-Perron et al., (2024) note in this issue that bees prefer non-droughted flowers over droughted flowers, possibly because the non-droughted flowers are larger, showier and produce more nectar than in droughted-plants. Patterns between drought and species reproductive responses are often inconsistent, however, increasing in general the level of uncertainty surrounding how reproduction will be affected by anthropogenic climate change (Brunet et al., 2024). Stokes and Geitmann, (2024) review heat sterility of pollen and discuss in depth the methodology needed to further our understanding of the heat sterility phenomenon, an inadequately understood threshold effect that could be a major wildcard in the reproductive response of plants to climate change, particularly when coupled with other stressors such as drought. Many species show a marked reduction in pollen viability as flowers warm above the mid-30 °C range; however, the studies supporting this result are largely from crop species, with research on heat sterility in the natural flora being uncommon (Sage et al., 2015). Brunet et al., (2024) also note that reduced pollen viability in response to drought has mostly been shown in crop species, such that AGC effects on pollen failure, a leading cause of reproductive sterility, has to be considered a black box when it comes to wild plants. The methodological review provided by Stokes and Geitmann should accelerate the pace of research into this inadequately understood topic. The Hsu and Kim, (2024) study on pollen growth in conifers nicely complements Stokes and Geitmann by showing the thermal optimum of pollen germination and pollen tube growth varies between conifer species with low elevation pines having higher thermal optima than high-elevation spruces. Climate change is producing a number of surprising outcomes. Unexpected responses to AGC are of great concern to global change biologists, because they hinder our ability to predict AGC effects and develop compensatory strategies (Srivastava et al., 2021). For example, a simple prediction is climate warming will increase the number of hot summer days, while reducing the extreme cold of mid-winter. Surprisingly, climate warming can also increase the incidence of lethal cold exposure, in a phenomenon known as the false spring, when warmer springs trigger precocious blooms before the threat of killing frost has passed (Savage et al., 2024). In their paper in this issue, Savage et al., (2024) investigate cold tolerance of floral tissues from 25 woody species that flower in spring in Minnesota, USA. They note damage from false springs will most likely affect species that currently flower later in the spring, because inflorescences of early flowering species are able to tolerate the cold of a false spring unlike many of the species flowering later in spring. Thus, in contrast to expectations for global warming, increased frequency of false springs should favor more cold-adapted species, and might delay migration of warm-adapted species to higher latitudes. In effect, false springs could lock a landscape into a more temperate vegetation type than the warmer climate regime established by AGC might indicate. Elevation has been an important proxy for understanding climate change, because climate varies substantially over short distances with increasing elevation while other important parameters such as photoperiod remain unchanged. Notably, the Rocky Mountain Biological Laboratory (RMBL) in Gothic, Colorado USA, has been a major center for climate change research on montane and alpine vegetation and two papers in the special issue present research from RMBL. Rodelius and Iler, (2024) document complex reproductive responses to variation in both biotic (pollen limitation) and abiotic factors (drought) affected by climate change in two herbaceous species (Hydrophyllum fendleri and Delphinium nuttallianum) growing in the montane landscape surrounding RMBL. Complex and often inconsistent species response are commonly reported in studies of interacting AGC drivers, such that developing clear predictions to inform policy makers and the wider public are challenging. Wu et al., (2024) studied how warming affects flower size, color, nectar production and scent properties in Ipomopsis aggregata, a widespread and well-studied hummingbird-pollinated species from the western USA, and its close related species, I. tuberfolia, which is pollinated by hawkmoths. Similar to the Rodelius and Iler study, they identified complex and often subtle responses to climate warming that were species specific. However, they did observe a warming enhancement of nectar production in I. aggregata which could increase hummingbird visitation in this species. Elsewhere, Basnett et al., (2024) observed that Himalayan rhododendrons from warm study sites of lower elevation had longer corolla tubes and larger nectar volumes than plants from higher, cooler climates. The longer tubes and larger nectar volumes were associated with a shift from bee to bird pollination. This in tandem with the Wu et al. results suggests bird pollination may be favored by climate warming, so long as other stressors such as drought are not enhanced. In the Italian Alps, Villa et al., (2024) used elevation differences to assess pollination and reproductive success in response to climate variation, noting that pollinator replacement which they observed with increasing elevation indicates there will be continued pollination services with climate change; however, the quality of pollen and seed production declined in warmer locations at lower elevation, suggesting the ability of plants to produce propagules will decline with warming. Gélvez-Zúñiga et al., (2024) studied floral abundance, longevity, and florivory along an elevational gradient in a tropical diversity hotspot within the Espinhaço Mountains of Minas Gerais, Brazil. Their results show that the number of flowers in higher elevation communities were less than in lower elevation locations, such that proportionally more of the higher elevation flowers were attacked by florivores. To fully understand AGC effects on florivory, they note it is necessary to consider population and community wide patterns in addition to impacts on individuals and single species. At the global scale, Novaes et al., (2024) conducted a meta-analysis to consider whether characteristic patterns of reproductive traits occur in response to elevational variation across the Earth, allowing for a global perspective of flowering responses to climate change along elevational gradients. While flowering and pollination exhibit specific patterns of vulnerability to AGC, at the opposite end of the reproductive process—seedling establishment—there are also important responses that will influence community composition and function. Three papers in the special issue address climate change effects on seed germination and establishment. In each, the interactive role of multiple factors associated with AGC are examined. Vásquez-Ramírez and (2024) and germination in alpine and communities in response to warming, and drought in They observed the consequences from effects of multiple leading to clear differences between the and et al., (2024) studied between warming and soil moisture on establishment of elevation conifer species from the of the in the western USA. of each species tolerance to warming if soil moisture due in to the ability to during hot However, if soil moisture warming associated with increased leading et al. to the of conifers at elevation will decline drought and heat both increase with climate change. Vásquez-Ramírez and (2024) and et al., (2024) also the role of whose earlier in warmer at elevation could lethal drought during summer heat et al., (2024) between drought and on in increased drought and are associated with AGC and are to to hinder as AGC However, et al. observed reduced drought of because it reduced water use and to long to extend the during the first summer of establishment. et al. did not consider effects of atmospheric CO2, but it has been shown to a that growth and establishment and may already to establishment of woody vegetation in et al., and Sage, 2022). The results of et al. and et al. the of a between CO2, and drought on woody with substantial consequences for regional vegetation As with elevation change, can as for how global change may affect plants in the they are warmer and of other global change drivers such as higher atmospheric CO2, by exotic species, and et al., a et al., (2024) document in flowering time and in to with higher frequency of plants of and thus in of on by the combined effects of AGC may AGC in the however, greater on could hinder long evolutionary by reducing needed to diversity within and thus hinder the spread of novel traits that individuals to increasing of global change (Bell and Collins, For many species, however, climate change population and their ecological of the of the and other species in the are their due to numerous global change such as invasive species land use change and et al., 2023). In their analysis in this issue, et al., (2024) note that of plants is particularly vulnerable to increased drought associated with climate change, which is likely to its The study of et al., (2024) to a aspect of AGC that is often attention surrounding AGC has considered with that the is a example, and 2023). before species however, population can a ecological role to the point that it due to its to the and of its et al., In many its the is this as are numerous other in ecosystems of the et al., et al., 2024). before the threat of widespread possibly within the of most readers of this special issue et al., 2013; and 2023). of this will reproductive of plants, which a diversity of and which the and diversity within an is whether the distinct in plants will to AGC, as one might predict if they into have distinct or resources et al., 2016). responses of the to the environment is one to and thus the to however, it could increase vulnerability of species to AGC if the relative of the the response of floral traits to water can not between and in a species, but the response of the can between plants from or in Brunet et al., in this et al. in this issue, growth rates in over the past by of in to climate of growth between the In recent when AGC and greater water use had greater drought than as they to the summer drought while were more to the current summer results how a in attempts to understand responses to AGC in plants with and of their reproductive If AGC and associated favor more than as in I. this could to change with consequences for the of the species A number of the papers in the special issue address the broader aspects of AGC beyond climate change. and (2024) the special issue with a of how global change has and will affect floral et al., (2024) a global meta-analysis of land use change effects on pollination and Their results an reduction in pollination as well as and fitness of in et al., (2024) how of climate change, pollinator and affect plants in and out as a phenomenon being by climate change, with of particularly and the world in recent example, and 2016; et al., 2021). Climate warming directly by and increasing however, is considered a global change than a climate change AGC drivers by to with greater frequency and For example, invasive species, and higher CO2 to increase on while increased increase to the landscape for and consequences of increased include in vegetation in due to altered reproductive and Vitousek, and 2011; et al., et al., 2022). In one of Earth’s the increased frequency and intensity due to AGC are reducing the cover of black one of the species of the et al., 2021). This reduction is due in to of before have time to and et al., 2024). papers in the special issue address the impacts of AGC on and plant reproduction. The first meta-analysis of effects on pollination and reproduction by et al., (2024) show how the effects of single in increasing pollination and reproduction of mostly and herbaceous et al., (2024) consider seed production of black along the of are less and lethal than in the of the As intensity in the of a due to AGC, seed from on the become more important to the ability of black to et al., 2024). Notably, as has been identified by the of one of our this special issue, increased frequency of can alter the vegetation composition of through on reproductive of the conifer species et al., 2024). In western increased by climate warming is establishment of conifers that for and seed species an that is by with of down allowing for conifer a of their during an and often to their in a landscape seed from As a by are predicted to spread at the of species with greater so long as the is not greater than the time of the pines et al., 2024). In locations accelerate with AGC such that of all species are before they a from to or could occur (Brooks et al., 2004; et al., et al., 2023). To the papers addressing AGC effects on plant reproduction a to the of issues the world’s plants in this of change. The and original reports readers with an appreciation of issues and the of the in our understanding of the impacts of AGC on plant reproduction. the pervasive and global nature of AGC, in our understanding of AGC such that potential is for and in the response of the to AGC (Srivastava et al., 2021). attention to global change effects on plant reproduction, we readers to consider more AGC effects beyond climate change, and how it impacts all aspects of plant reproduction. of in reproduction of reproduction in the viability of the species at as well as that of the organisms that on

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