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Elsa Youngsteadt, Margarita M López-Uribe, Clyde E Sorenson, Ecology in the Sixth Mass Extinction: Detecting and Understanding Rare Biotic Interactions, Annals of the Entomological Society of America, Volume 112, Issue 3, May 2019, Pages 119–121, https://doi.org/10.1093/aesa/saz007
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The Earth is experiencing a wave of anthropogenic biodiversity loss, such that current rates of extinction are 100–1,000 times the background rate observed between prior mass extinctions in the fossil record (Barnosky et al. 2011, Pimm et al. 2014). These losses place Earth’s biota in the early stages of an extinction event comparable to those precipitated only five times before in the past 540 million years (Barnosky et al. 2011, Ceballos et al. 2015). Among plants—the foundation of terrestrial food webs—an estimated 20% of all species are currently threatened with extinction (Brummitt et al. 2015). Among invertebrates, conservation status has been reviewed for only about 1% of described species, and of those, some 40% are threatened (Dirzo et al. 2014). Regional surveys regularly detect striking losses in insect biomass and population size over recent decades (e.g., Fox 2013, Hallmann et al. 2017, Lister and Garcia 2018).
Loss of species richness, population size, and biomass are striking, but they do not capture the full impact of biotic change. Each species participates in a web of interactions, such as predation, parasitism, and mutualism, that underpin ecosystem functions (Tylianakis et al. 2008). These interactions are expected to disappear before the species themselves (McConkey and Drake 2006, Valiente-Banuet et al. 2015), precipitating changes in ecosystem function and extinction of other species that depend on the interactions (Säterberg et al. 2013, Risch et al. 2018). In this context, the study of rare biotic interactions is becoming more widespread and more urgent; however, challenges abound in detecting such interactions and interpreting their ecological relevance. These challenges were the focus of a Plant-Insect Ecosystems Section Symposium convened at the 2017 annual meeting of the Entomological Society of America in Denver, CO. Among the symposium’s 16 presenters, 6 contributed papers to this collection, providing a cross section of the dimensions of rarity with which ecologists must grapple.
Rarity is not always associated with decline and extinction risk. A rare species may have a small population size, low population density, small geographical range, restricted habitat type, or all of the above (Kunin 1997, Harnik et al. 2012). Rare interactions, in turn, may involve one or more rare species or may include common species participating in interaction types that rarely evolve, are rarely observed, or are fleeting in time. By embracing all facets of rarity in the symposium and collection, we hope to supply fresh perspective on the study of species interactions in an era when many of them are indeed threatened with extinction.
Some interpretations suggest that abundant species are most important in maintaining ecosystem function (Aarssen 1997, Kleijn et al. 2015). Evidence is growing, however, that rare species maintain key functional diversity and may have disproportionate effects on foodweb structure (Zavaleta and Hulvey 2004, Bracken and Low 2012, Mouillot et al. 2013). Papers in this collection add to the basic and applied motives to overcome the challenges inherent in studying interactions that are rare. Lhomme and Hines (2018), in their comprehensive review of the ecology and evolution of cuckoo bumble bees, make the case that these rarely encountered social parasites have much to contribute to the study of coevolution. Realizing this potential will involve logistical challenges, as well as some urgency; some cuckoo bumble bee species are threatened by population declines in their formerly common hosts.
Espíndola and Pliscoff (2018) make unique use of another rare interaction to query the extent to which environmental conditions shape interaction strength over a large geographical area. They work with a specialized pollination system involving nectarless flowers pollinated by bees that extract floral oils for nest construction and provisioning. Roughly, 1% of angiosperm species and 2% of bee species participate in the exchange of floral oil for pollination service, and this form of mutualism was only documented in the latter half of the 20th century (Buchmann 1987). Because of its unusual specialization, this interaction provided a straightforward study system in which to integrate field sampling, species distribution modeling, and geospatial analyses to determine whether plants were more frequently visited when growing in sites most climatically suitable for their pollinators.
From an applied angle, Howard and Hall (2018) make a strong argument in favor of incorporating information about biotic interactions into conservation plans for threatened and endangered insects. Reviewing case studies of two species—the U.S. federally endangered American burying beetle and the rare prairie mole cricket—they outline the ways in which biotic interactions (including predation, interspecific competition, microbial mutualisms, and mating behaviors) all have the potential to illuminate causes and consequences of rarity, as well as recovery from it.
Howard and Hall’s case studies also highlight some of the ways in which technology can overcome challenges involved in studying rare interactions, with insights derived from video surveillance, automatic locomotion monitors, and acoustic analyses. In a related advance, Edwards et al. (2018) use time-lapse videography to observe many sites simultaneously, thereby obtaining near-complete records of floral visitors over the entire bloom period of individual plants of ten species. Analysis of the resulting video demonstrated distinct differentiation in visitor communities of same-species flowers just a few hundred meters apart, providing a remarkably thorough example of the potential for pollinators to generate fine-grained selection mosaics experienced by plants. This team’s approach is applicable to many kinds of interactions among macroscopic organisms, enhancing opportunities to observe rare or fleeting interactions.
Youngsteadt and Sorenson (2018) and Hamon et al. (2018) accept the premise that detailed knowledge of biotic interactions is essential to developing successful conservation plans, and set out to document the previously unknown pollinator interactions of two rare plants. Youngsteadt and Sorenson (2018) worked with a U.S. federally endangered shrub with a dioecious mating system—an unusual arrangement known in about 4% of temperate angiosperm species (Bawa 1980). Using a combination of time-lapse videography (Edwards et al. 2015, Edwards et al. 2018) and direct observation, they documented a highly generalized pollinator community. Despite frequent visits, however, pollen was rarely delivered to female plants due to the spatial arrangement of the sexes in the studied populations—suggesting a path for conservation interventions to increase pollination and seed set. Hamon et al. (2018) focused on the fire ecology of a carnivorous plant, the Venus flytrap, asking how the history of controlled burns at a site affected floral morphology and pollen limitation of seed set. Neither the pollinator community nor the extent of pollen limitation correlated with time since fire, but plants at some sites were pollen-limited, suggesting that the pollination ecology of this species also warrants further attention in a conservation context. These case studies confirm that—as Howard and Hall (2018) argue—going to the trouble of documenting biotic interactions of rare species does often provide relevant conservation insights.
Although the diversity of life on Earth is declining, the majority of species have the potential to persist if the worst stresses upon them are mitigated. This collection provides evidence that biotic interactions are an essential part of this picture. Advances in—and strategic use of—surveillance technology and analytical techniques are improving the feasibility of detecting and interpreting rare interactions. Papers in this collection make the case that the resulting insights are not only relevant to the conservation of individual species but also take a broader perspective by showing how certain interactions—despite their rarity—provide model systems for addressing basic evolutionary and ecological questions. We look forward to future work that embraces these perspectives to promote the persistence of a rich web of biotic interactions on Earth and to understand the evolutionary and ecological significance of even the rarest links in that web.
Acknowledgments
We thank Larry Hurd, Editor-in-Chief, for the invitation to prepare this special collection and for handling our own submissions to the section. Lisa Junker and Josh Lancette also provided invaluable guidance throughout the process. It was a pleasure to work with all of the authors who contributed to this collection, as well as the anonymous referees who reviewed and strengthened their work.