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UC Riverside UC Riverside Previously Published Works UC Riverside UC Riverside Previously Published Works Title EFFECTS OF ROAD DUST ON THE POLLINATION AND REPRODUCTION OF WILDFLOWERS Permalink https://escholarship.org/uc/item/6sj927h5 Journal INTERNATIONAL JOURNAL OF PLANT SCIENCES, 178(2) ISSN 1058-5893 Authors Waser, Nickolas M Price, Mary V Casco, Genesis et al. Publication Date 2017-02-01 DOI 10.1086/689282 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Int. J. Plant Sci. 178(2):85–93. 2017. q 2016 by The University of Chicago. All rights reserved. 1058-5893/2017/17802-0001$15.00 DOI: 10.1086/689282 EFFECTS OF ROAD DUST ON THE POLLINATION AND REPRODUCTION OF WILDFLOWERS Nickolas M. Waser,1,*,† Mary V. Price,*,† Genesis Casco,* Maria Diaz,* Asia Liza Morales,* and Jennie Solverson* *Rocky Mountain Biological Laboratory, PO Box 519, Crested Butte, Colorado 81224, USA; and †School of Natural Resources and the Environment, University of Arizona, Tucson, Arizona 85721, USA Editor: Janette Steets Premise of research. Dust particles and pollen grains are similar in size. Dust deposition might therefore influence the pollination and reproduction of flowering plants. Little is known about such effects, however, despite more general interest in ecological effects of dust. Methodology. We used observational and experimental methods to explore whether dust generated by traf- fic on unpaved roads affects the amounts of pollen received and numbers of seeds produced by four species of native wildflowers in the western United States. Pivotal results. Flowers of Nuttall’s larkspur (Delphinium nuttallianum), scarlet gilia (Ipomopsis aggregata), Lewis flax (Linum lewisii), and sulphur paintbrush (Castilleja sulphurea) growing 1–2 m from a road received sub- stantially more dust and less pollen than those growing 40–50 m away. We observed the same pattern when we transplanted individuals of the first two species into pots and placed pots near to compared with far from a road. Experimental “hand dusting” of scarlet gilia and Lewis flax plants also reduced stigma pollen loads to a degree that resembled the average effect of road proximity for those species. On the other hand, numbers of seeds per flower (“seed set”) did not vary consistently for any species as a function of road proximity or hand-dusting treatment. Conclusions. Several mechanisms might contribute to the different effects of dust on pollen loads and seed set. We discuss four possible mechanisms, which we refer to as pollen excess, pollen quality, resource limitation, and compensatory herbivory. These mechanisms suggest avenues for further study of dust, pollination, and plant repro- duction with this and other systems. Keywords: Castilleja sulphurea, Delphinium nuttallianum, hand dusting, Ipomopsis aggregata, Linum lewisii, seed set. Online enhancements: appendix tables. Introduction transportation along unpaved roads (Field et al. 2010). Most dust (including dust from roads) travels over short distances and is de- In German, the word Staub refers both to dust and to the pol- posited locally. However, dust storms regularly cover large areas len of flowering plants.2 This dual definition is unsurprising. Pol- in dry regions such as the western United States (Steltzer et al. len can resemble dust, which is defined as fine, dry, particulate 2009), and some dust even reaches sufficient heights in the at- matter with linear dimensions of microns to tens of microns, a mosphere to be carried over intercontinental distances (VanCuren size range that includes many pollen grains. These physical simi- and Cahill 2002; Prospero and Lamb 2003). Dust production larities between dust and pollen suggest that they might interact is expected to increase with climate change and intensifying hu- in more than a linguistic sense: dust might interfere with pollina- man land use (Field et al. 2010). tion (German Bestäubung) and thereby with plant reproduction. To date, research on ecological effects of dust has mostly fo- Dust arises from natural sources, in particular from the scour- cused on its consequences for ecosystem processes from local to ing of soils in arid regions by wind, as well as from soil-disturbing global scales (Field et al. 2010). Much less is known about effects human activities such as agriculture, livestock husbandry, and at the level of individual organisms. We do not know, for exam- ple, whether dust harms plant reproduction, even though there is ample reason to expect that it might. Consider possible direct 1 Author for correspondence; e-mail: [email protected]. effects related to the sequential phases of angiosperm reproduc- 2 This Germanic introduction is not meant to slight Romance lan- tion: pollination, ovule fertilization, and seed maturation. Most guages—the Latin root of “pollen” is a fine flour or meal, also implying dust. angiosperm species rely on animals (primarily insects) for polli- Manuscript received July 2016; revised manuscript received August 2016; nation (Ollerton et al. 2011), and pollinators might avoid dusty electronically published November 23, 2016. flowers, much as chewing herbivores avoid dusty or sandy forage 85 86 INTERNATIONAL JOURNAL OF PLANT SCIENCES (Ndibalema et al. 2008; LoPresti and Karban 2016). Dust also could interfere with the culmination of the pollination phase and onset of the fertilization phase by inhibiting pollen adhesion or germination on the stigma, the receptive female floral organ, or through mechanical changes in the stigma that reduce subse- quent pollen receipt (e.g., see Waser and Fugate 1986). Finally, dust-induced changes in plant resource status—e.g., via effects on leaf pH, light capture, or gas exchange through stomata— might reduce the number or mass of seeds that a plant can mature or the number of flowers it produces. To such direct effects might be added indirect ones. For example, airborne particulates gen- erated by traffic on unpaved roads can alter soil chemistry (Kaliscz and Powell 2003), soil decomposition via effects on microbial biochemistry (Moorhead et al. 1996), and earliness of spring snow- melt (Walker and Everett 1987; Painter et al. 2007; Steltzer et al. 2009), all of which could influence the physiology of individual plant species and their reproduction. Here we describe the effects of dust from unpaved roads on pollination and reproduction of four species of montane wild- flowers. In studies conducted over four summers, we did the fol- lowing: (1) We characterized dust deposition at the soil surface and on stigmas of flowers as a function of distance from roads. (2) Having found substantial dust deposition near the roads, we used both observational and experimental methods to ask whether dust influences the pollination phase of reproduction, as- sessed as loads of pollen on stigmas. The answer is that lower pollen loads are consistently associated with dust deposition. (3) Using the same flowers from which we had collected stig- mas (with one exception), we then asked whether dust influ- ences overall female reproductive output of plants, assessed as numbers of seeds set per flower (hereafter seed set). Here the answer is that seed set is not consistently associated with dust deposition. We discuss four mechanisms that might possibly Fig. 1 Flower morphology of the study species. Arrows indicate contribute to these seemingly discrepant results, as a means of stigma positions. A, Delphinium nuttallianum, frontal view showing five suggesting avenues for further research. Finally, we consider pigmented petaloid sepals, two whitish petals that contain the nectaries, “ ” general conditions under which dust is likely to have observable and two pigmented guard petals that cover the sex parts. B, Delphinium effects on seed production. nuttallianum, lateral view with right-hand nectar petal and guard petal removed to show positions of the three carpels, styles, and stigmas in fe- male phase. C, Ipomopsis aggregata, lateral view with half of the corolla removed to reveal the pistil. The position of the three-lobed stigma ranges Material and Methods continuously across individuals from inserted within the corolla tube to exserted beyond the tube (Campbell et al. 1994). Illustrated is a common Study System and Sites stigma position at the entrance to the tube. D, Linum lewisii,lateralview with two front petals and one front anther removed to show positions of To explore possible effects of dust on pollen loads and seed pro- the five stigmas. E, Castilleja sulphurea, lateral view of one flower and its duction, we chose four perennial herbaceous wildflowers that are subtending yellow bract, with neighboring bracts and flowers removed. native to the mountains of western Colorado. These are Nuttall’s (pNelson’s) larkspur Delphinium nuttallianum (Pritzel ex Wal- We examined dust effects on one or more of these wildflower pers) (Ranunculaceae), scarlet gilia Ipomopsis aggregata (Pursh) species during four summers (2008, 2013, 2014, and 2015; see V. Grant (Polemoniaceae), Lewis flax Linum lewisii (Pursh) (Lina- table 2 for details of years, species, and sites). We worked mostly ceae), and sulphur paintbrush Castilleja sulphurea (Rydberg) in the East River Valley, either in Gothic or north of Gothic along (Orobanchaceae). All four species are common in meadows USFS Road 317. In 2015 we added sites along USFS Road 811 in around Gothic, Colorado, the site of the Rocky Mountain Bio- Washington Gulch, the parallel valley just to the west of the East logical Laboratory (RMBL; lat. 38758ʹ N, long. 106759ʹ W; eleva- River Valley, and along USFS Road 734 in the Slate River Valley, tion 2900 m), and in the Grand Mesa-Uncompahgre-Gunnison the parallel valley just to the west of Washington Gulch. All of National Forest (US Forest Service [USFS]) near this field station. these roads are unpaved and ca. 6 m wide. During the snow-free All four species are animal pollinated, and they exhibit a range of season (approximately June–September) the roads experience heavy floral phenotypes (fig. 1) and of animal pollinators (table 1). Fur- use by private automobiles and pickup trucks (two axles), motor- thermore, all species, and especially the first two, have been stud- cycles, and larger vehicles (more than two axles).
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