Pollination for the people

Abstract

At the conclusion of her 2014 book, The Sixth Extinction, Elizabeth Kolbert explains that her aim was not so much to document the devastating impact of human activities on specific endangered species as to highlight the more ominous global patterns of biotic decline as a harbinger of the Anthropocene. Subsequent reports of catastrophic losses of insects1Hallmann C.A. Sorg M. Jongejans E. Siepel H. Hofland N. Schwan H. Stenmans W. Müller A. Sumser H. Hörren T. et al.More than 75 percent decline over 27 years in total flying insect biomass in protected areas.PLoS One. 2017; 12: e0185809Crossref PubMed Scopus (1292) Google Scholar and birds2Rosenberg K.V. Dokter A.M. Blancher P.J. Sauer J.R. Smith A.C. Smith P.A. Stanton J.C. Panjabi A. Helft L. Parr M. Marra P.P. Decline of the North American avifauna.Science. 2019; 366: 120-124Crossref PubMed Scopus (547) Google Scholar at alarmingly broad faunistic scales have compounded the sense of urgency felt by many biologists, especially those who study plant–pollinator interactions. Pollinator conservation awareness was kindled in the mid-1990s by a popular book (The Forgotten Pollinators by Stephen Buchmann and Gary Nabhan) and a seminal review3Kearns C.A. Inouye D.W. Waser N.M. Endangered mutualisms: The conservation of plant–pollinator interactions.Annu. Rev. Ecol. Syst. 1998; 29: 83-112Crossref Scopus (1211) Google Scholar on the vulnerability of plant–pollinator mutualisms as well as their undervalued ecosystem services to humans. Since then, the study of pollination has expanded to a much larger tent, beneath which developmental geneticists study how flowers are constructed, neuro-ethologists measure how pollinators perceive such flowers, community ecologists apply social network tools to explore their complex interactions, and agricultural biologists struggle to sustainably manage these interactions in the abused margins of the world’s croplands. Few pollination biologists have played a more pivotal role in the expansion of the pollination tent than Jeff Ollerton, author of the recent book Pollinators and Pollination: Nature and Society. Ollerton is a joyful provocateur with an inordinate fondness for milkweeds and a passion for challenging dogma with large data sets. He is also a prolific author (130 publications and 11,450 citations) who signs his reviews and is energized by vigorous debate. A cartoon sketch of Ollerton’s career highlights would include global reviews4Ollerton J. Cranmer L. Latitudinal trends in plant–pollinator interactions: are tropical plants more specialised?.Oikos. 2002; 98: 340-350Crossref Scopus (148) Google Scholar of pollination (latitudinal trends, pollinator syndromes, diversification in the dogbane family) along with an iconoclastic paper5Waser N.M. Chittka L. Price M.V. Williams N.M. Ollerton J. Generalization in pollination systems, and why it matters.Ecology. 1996; 77: 1043-1060Crossref Scopus (1353) Google Scholar and an edited volume6Waser N.M. Ollerton J. Plant–Pollinator Interactions: From Specialization to Generalization. University of Chicago Press, Chicago2006Google Scholar on pollinator generalization, produced with co-provocateur, Nick Waser. As a young scientist, Ollerton7Ollerton J. Reconciling ecological processes with phylogenetic patterns: The apparent paradox of plant–pollinator systems.J. Ecol. 1996; 84: 767-769Crossref Scopus (209) Google Scholar observed that evolutionary patterns of floral specialization often conflict with ecological patterns of pollinator generalization for many plant taxa, a paradox that now bears his name. I linger on Ollerton’s credentials because Pollinators and Pollination is a deeply personal book, written as an eyewitness account to a revolution that he helped to instigate, with much affection for (and credit shared with) his many collaborators and students. Ollerton’s text is rich with personal flourishes, from his formative childhood ramblings, through yearly field trips with Northampton University (UK) students to Tenerife, to his more recent forays into gardening and urban renewal closer to home. Interestingly, the author’s voice emerges more as a dialogue with the reader than as an intimate meditation, and his narrative is more forward-looking than retrospective. Ollerton outlines his four primary aims in writing this book: first, to share his fascination with pollination and its importance to nature and humanity; second, to dispel myths and misconceptions about pollinators; third, to convey to lay enthusiasts how they can advance our understanding of pollination; and fourth, to help ensure that species and their interactions are not lost in the ecological maelstrom of the Anthropocene. Ollerton’s personal style notwithstanding, his book is a slalom course of data, with 36 graphs and seven tables that send the reader careening through graphical gates of evidence supporting each of his teaching points. In one revealing passage, Ollerton recalls how his frustration with the repeated (mis)quoting of imprecise statistics on what proportion of flowering plants is pollinated by animals compelled him and two colleagues to answer this question themselves8Ollerton J. Winfree R. Tarrant S. How many flowering plants are pollinated by animals?.Oikos. 2011; 120: 321-326Crossref Scopus (1642) Google Scholar. Just as important as the answer (an estimated 87.5% of angiosperm species) was the opportunity to provide other scientists, policy makers, and journalists with figures grounded more firmly in published data. Given the alarming erosion of public trust in science, Ollerton reiterates the importance of evidence-based policy throughout his book, especially in its penultimate chapter, ‘The Politics of Pollination’. Pollinators and Pollination begins with profiles of pollinator diversity, floral form, and function as an introductory sequence, before progressing to a cluster of ecological and evolutionary chapters close to the author’s own research. Ollerton revisits some of his least favorite “pollination myths” in these core chapters: that flowers with specialized structures always have a single pollinator, that pollination is inherently a cooperative venture, and that bees are the only/most important pollinators. One of the most extensively covered topics in this part of the book is the study of plant–pollinator networks and their ecological properties. The re-imagining of plant–pollinator interactions as food webs caught fire around the time that Waser and Ollerton’s edited volume6Waser N.M. Ollerton J. Plant–Pollinator Interactions: From Specialization to Generalization. University of Chicago Press, Chicago2006Google Scholar was published (2006), featuring key early studies on this subject. I and others reacted skeptically to the network approach, criticizing it for conflating floral visitation with effective pollination and for promoting abstruse terms (e.g. nestedness, centrality) that reveal few novel concepts about pollination. Ollerton, as an advocate, explains how networks re-frame binary plant–pollinator interactions within a broader community context, emphasizing indirect effects that facilitate such pairings. It so happens that ‘influencers’ are as important in plant–pollinator networks as in human social media. Consider a rare orchid species that depends upon a large bee species for pollination, whereas its bee pollinator may be long-lived and generalized in its foraging habits, patronizing abundant plants that bloom for extended periods beyond the orchid’s time frame. The resulting inference that “no pollinator is an island” has intriguing consequences. Not only is our hypothetical orchid–bee relationship not mutually specialized, it is likely subsidized by common thistles and cherry tree blossoms (or their tropical equivalents) in the same community. Even when ‘links’ in plant–pollinator networks don’t strictly reflect pollination events, they help to visualize a bustling floral marketplace, including the ebb and flow of commerce (nectar and pollen usage) and its consequences for public health (inter-floral transfer of pathogens9Figueroa L.L. Blinder M. Grincavitch C. Jelinek A. Mann E.K. Merva L.A. Metz L.E. Zhao A.Y. Irwin R.E. McArt S.H. Adler L.S. Bee pathogen transmission dynamics: deposition, persistence and acquisition on flowers.Proc. Biol. Sci. 2019; 286: 20190603PubMed Google Scholar). My own skepticism about networks waned when I realized that ecological subsidies extend to the nocturnal pollination systems that I have studied in the Sonoran Desert. There, a rare night-blooming cactus pollinated by adult hawkmoths is subsidized on two distinct trophic levels by common, co-blooming Datura plants, which serve as more reliable nectar sources for these moths and as host plants for their hornworm larvae10Raguso R.A. Henzel C. Buchmann S.L. Nabhan G.P. Trumpet flowers of the Sonoran Desert: Floral biology of Peniocereus cacti and sacred Datura.Int. J. Plant Sci. 2003; 164: 877-892Crossref Scopus (93) Google Scholar. The remainder of Ollerton’s book engages subjects more directly impacted by human activities: agriculture, urban environments, gardens, extinction and invasiveness, and the management of restored habitats. These chapters touch upon a common set of themes: habitats need not be pristine to support populations of pollinators, urban green spaces can bolster such populations, and individuals can make a difference by modifying their own gardens or participating in citizen science. Ollerton’s animated account of his students discovering over 50 species of bees within Northampton channels Rob Dunn’s bemused descriptions of the unexpected (micro)biotic frontiers within our own homes in Never Home Alone. Another core element of Ollerton’s latter chapters is his effort to balance the ledger in discussions of “pollinator crises”, reminding readers that global change involves both the local declines and extinctions of some species and the range extensions and invasiveness of others. Ollerton wisely avoids devoting too much space to the perils of honey bee health and commercial management, important but complex subjects that tend to dominate the public sphere and would distract from the biogeographical scope of the author’s thesis. Ollerton’s passage on the rapid naturalization of an introduced bumble bee (Bombus hypnorum) in Northampton squares the circle by describing how quickly wild pollinator populations can change, while showing how citizen scientists can help to track such changes. In closing, Ollerton’s forward-looking, human-inclusive chapters provide readers with ways to think more creatively about how to embrace human-impacted environments as reality, and how to enrich them as reservoirs for pollination and other ecosystem services. A terrifying specter of the Anthropocene is the unanticipated impact (in economic and social costs) of insect vectored disease and crop failure due to the loss of natural pest control by birds, bats, and other rapidly declining predators. Clearly, plant–pollinator mutualisms are just as imperiled by unchecked biotic declines. In Pollinators and Pollination, Jeff Ollerton empowers readers to overcome future shock with the background and tools needed to promote pollination in their local environments, as an ecosystem service and a public good. Flowers and their pollinators have evoked wonder and interest throughout human history and, no doubt, will continue to inspire popular books, art, and other forms of human expression. Among many excellent offerings on the subject, Pollinators and Pollination is unique in providing a thorough overview of some of the most important (and rapidly changing) themes in pollination biology, while showcasing the author’s zest for engagement with his students, colleagues, and fellow citizens.