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THE QUARTERLY REVIEW of Biology Volume 91, No. 4 December 2016 THE QUARTERLY REVIEW of Biology PATTERNS AND PROCESSES IN NOCTURNAL AND CREPUSCULAR POLLINATION SERVICES Renee M. Borges* Centre for Ecological Sciences, Indian Institute of Science Bangalore 560 012 India e-mail: [email protected] Hema Somanathan Indian Institute of Science Education and Research Thiruvananthapuram Kerala 695016 India e-mail: [email protected] Almut Kelber Vision Group, Department of Biology, Lund University 22362 Lund, Sweden e-mail: [email protected] *Corresponding author. keywords aridity, crepuscular pollination, dawn, dusk, nocturnal pollination network, water stress abstract Night, dawn, and dusk have abiotic features that differ from the day. Illumination, wind speeds, turbulence, and temperatures are lower while humidity may be higher at night. Nocturnal pollination oc- curred in 30% of angiosperm families across 68% of orders, 97% of families with C3, two-thirds of fam- The Quarterly Review of Biology, December 2016, Vol. 91, No. 4 Copyright © 2016 by The University of Chicago Press. All rights reserved. 0033-5770/2016/9104-0001$15.00 389 390 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 ilies with crassulacean acid metabolism (CAM), and 71% dicot families with C4 photosynthesis. Despite its widespread occurence, nocturnal pollination occurs in more families with xerophytic adaptations than helophytes or mesophytes, suggesting that nocturnal flowering is primarily an adaptation to water stress since flowering is a water-intensive process. We propose the arid or water stress hypothesis for nocturnal flowering suggesting that plants facing water stress in a habitat (e.g., deserts) or a habitat stratum (e.g., upper canopy for epiphytes) gain a selective advantage by nocturnal flowering by reducing water loss through evapotranspiration, leading to larger flowers that provide more nectar or other resources, to sup- port pollinators with higher rewards. Contrary to the wide taxonomic occurrence of nocturnal flowering, few animal taxa serve as nocturnal pollinators. We discuss the sensory and physiological abilities that enable pollinator movement, navigation, and detection of flowers within the nocturnal temporal niche and present a unified framework for investigation of nocturnal flowering and pollination. Introduction Nocturnal Pollination OLLINATION is a process in which Patterns in the Angiosperms Pa stationary plant exchanges gametes Since there has not been a review of noc- with other plants or with itself through the turnal/crepuscular pollination systems af- action of abiotic agents such as the wind or ter Baker (1961), there is a lot of ground biotic agents that range in size from minute to cover. We followed the classification of gall midges to large primates. Most plants angiosperms prepared by the Angiosperm are metabolically active during the day when Phylogeny Group (APG III; Bremer et al. the important reactions of photosynthesis 2009) and the linear sequence of plant occur. The wind is strongest during the day, families in Haston et al. (2009). We did an and it appears that the majority of pollinat- exhaustive search of Google Scholar using ing animal taxa are also active during the a combination of keywords that included day. If this is the case, then most pollina- plant families, and such keywords as noctur- tion should occur during the day and noc- nal pollination, night, evening, crepuscular, turnal pollination should be the exception. matinal, as well as keywords for known noc- What, then, are the factors that facilitate turnal/crepuscular pollinators such as bats, the origin and maintenance of nocturnal beetles, moths, and nocturnal mammals. For pollination? plant traits that were not considered in the The purpose of this review is severalfold. papers we reviewed, we also consulted Watson First, it will document nocturnal pollination and Dallwitz (1992; http://delta-intkey.com). patterns in the angiosperms. Second, it will We have taken the caveats mentioned in this present features of the physical environ- online resource seriously and have made in- ment that characterize the night (includ- dependent checks in the primary literature ing dawn and dusk). Third, it will elaborate wherever possible. We also consulted Ste- on factors that make nocturnal pollination vens (2001; http://www.mobot.org/mobot an advantage to plants. Fourth, it will docu- /research/apweb) for plant traits and for ment the animal taxa involved in nocturnal determining the family affiliation of all gen- pollination and review the special features era with nocturnal/crepuscular pollination that enable the activity of nocturnal polli- especially since several genera have been re- nators given the physical conditions of the assigned to families based on recent phyloge- night. Finally, it will lay out new hypotheses netic information. to fuel future investigations into this fasci- We score pollination to be truly nocturnal nating field. Considering the vast scope of and/or crepuscular (active during dawn or this subject, this review is intended as the dusk) if there is evidence that pollinators beginning of a synthesis toward a better un- are attracted to the flowers during noctur- derstanding of how and why nocturnally nal and/or crepuscular hours, and if there flowering plants and their nocturnal polli- is reasonable evidence of pollen transfer. nators occupy such a special temporal niche. We do not include some systems, for exam- December 2016 NOCTURNAL AND CREPUSCULAR POLLINATION 391 ple, brood site pollination by thrips where only the Acorales and the Petrosaviales did it is clear that the thrips are attracted to not have any families with nocturnal pollina- the flowers in large numbers during the tion, although the other orders had represen- day and they continue to be present in the tation of this trait. In the other “clades,” there flowers during the night. Similarly, we in- is no evidence for nocturnal pollination in clude thermogenic pollination systems as the following orders: Ceratophyllales, Troch- being nocturnal only if there is evidence odendrales, Buxales, Gunnerales, Dilleniales, that the attraction to the heat-producing Vitales, Fagales, Picramniales, and Garryales. flowers is during the crepuscular/noctur- In the following orders, pollination systems nal hours; for example, while Aristolochi- are unknown in some or all families, so the aceae and Rafflesiaceae are thermogenic presence of nocturnal pollination cannot be families (Thien et al. 2009), there is no determined: Berberidopsidales, Huerteales, evidence that the flies are attracted to the Bruniales, and Paracryphiales. Across orders, flowers during the night itself. Similarly, Magnoliales, Pandanales, Arecales, Zingibe- Hydnoraceae includes thermogenic trap rales, Myrtales, Gentianales, and Escalloniales blossoms, but the odor that attracts beetles (represented by only one family) had the is produced during the day and no noctur- highest percentage (at least 60%) of families nal visitors have yet been observed (Bolin with nocturnal pollination (Table 1). It must et al. 2009). Also, in Nelumbonaceae, there be remembered that our scoring of nocturnal is no evidence of nocturnal attraction by pollination is at the family level; some orders beetles, which are the major pollinators, and clades have many more families than oth- although the flowers are thermogenic (Li ers, and this factor must be considered when and Huang 2009). This is in contrast to the evaluating the phylogenetic occurrence of thermogenic Araceae, e.g., Amorphophallus, nocturnal pollination. which begin to emit odor at dusk (Punekar Using Phylomatic (Webb and Donoghue and Kumaran 2010). 2005; http://www.phylodiversity.net/phylo Of the 413 families recognized in the matic), we constructed a phylogeny for the APG III classification, 113 families had spe- 413 APG III angiosperm families and lo- cies with nocturnal pollination, 37 families cated the nocturnal/crepuscular families have unknown pollination mechanisms, and on the obtained phylogenetic tree, which 263 families have no evidence of nocturnal was visualized using the program FigTree pollination (Table 1, see Appendixes 1 and (http://tree.bio.ed.ac.uk/software/figtree/; 2 available at http://www.journals.uchicago Figure 1). The value of good phylogenies is .edu/loi/qrb). Therefore 113/376, or ap- essential to any analysis on functional traits proximately one-third of angiosperm fam- (Hinchliff et al. 2015). As the figure shows, ilies, whose pollination sys tems are known, nocturnal pollination occurs throughout have species with nocturnal pollination. This the tree of angiosperms and does not appear is likely to be a conservative estimate since to be restricted to any particular groups, most studies on pollination are conducted whether early or more recent. With its wide on day-flowering species. At a higher taxo- distribution, nocturnal pollination does not nomic level, at least 42/61 = 69% of orders appear to be restricted to particular types (with designated families) have species with of flowers. Is it possible then to understand nocturnal pollination (Table 1; excludes all what types of processes may have given rise orders marked with a “?”). This indicates the to nocturnal pollination? We therefore ex- wide taxonomic occurrence of nocturnal amine the abiotic environment that is char- pollination, presumably in some cases, due acteristic of the night since pollinators that to convergent evolution. use this temporal niche must have abilities Examining these trends phylogenetically, to function
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