keywordsaridity, crepuscular pollination, dawn, dusk, nocturnal pollination network, water stress
abstractNight, 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-
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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.
IntroductionOLLINATION is a process in which a stationary plant exchanges gametes
with other plants or with itself through the action of abiotic agents such as the wind or biotic agents that range in size from minute gall midges to large primates. Most plants are metabolically active during the day when the important reactions of photosynthesis occur. The wind is strongest during the day, and it appears that the majority of pollinat-ing animal taxa are also active during the day. If this is the case, then most pollina-tion should occur during the day and noc-turnal pollination should be the exception. What, then, are the factors that facilitate the origin and maintenance of nocturnal pollination?
The purpose of this review is severalfold. First, it will document nocturnal pollination patterns in the angiosperms. Second, it will present features of the physical environ-ment that characterize the night (includ-ing dawn and dusk). Third, it will elaborate on factors that make nocturnal pollination an advantage to plants. Fourth, it will docu-ment the animal taxa involved in nocturnal pollination and review the special features that enable the activity of nocturnal polli-nators given the physical conditions of the night. Finally, it will lay out new hypotheses to fuel future investigations into this fasci-nating field. Considering the vast scope of this subject, this review is intended as the beginning of a synthesis toward a better un-derstanding of how and why nocturnally flowering plants and their nocturnal polli-nators occupy such a special temporal niche.
Nocturnal Pollination Patterns in the Angiosperms
Since there has not been a review of noc-turnal/crepuscular pollination systems af-ter Baker (1961), there is a lot of ground to cover. We followed the classification of angiosperms prepared by the Angiosperm Phylogeny Group (APG III; Bremer et al. 2009) and the linear sequence of plant families in Haston et al. (2009). We did an exhaustive search of Google Scholar using a combination of keywords that included plant families, and such keywords as noctur-nal pollination, night, evening, crepuscular, matinal, as well as keywords for known noc-turnal/crepuscular pollinators such as bats, beetles, moths, and nocturnal mammals. For plant traits that were not considered in the papers we reviewed, we also consulted Watson and Dallwitz (1992; http://delta-intkey.com). We have taken the caveats mentioned in this online resource seriously and have made in-dependent checks in the primary literature wherever possible. We also consulted Ste-vens (2001; http://www.mobot.org/mobot /research/apweb) for plant traits and for determining the family affiliation of all gen-era with nocturnal/crepuscular pollination especially since several genera have been re-assigned to families based on recent phyloge-netic information.
We score pollination to be truly nocturnal and/or crepuscular (active during dawn or dusk) if there is evidence that pollinators are attracted to the flowers during noctur-nal and/or crepuscular hours, and if there is reasonable evidence of pollen transfer. We do not include some systems, for exam-
P
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ple, brood site pollination by thrips where it is clear that the thrips are attracted to the flowers in large numbers during the day and they continue to be present in the flowers during the night. Similarly, we in-clude thermogenic pollination systems as being nocturnal only if there is evidence that the attraction to the heat-producing flowers is during the crepuscular/noctur-nal hours; for example, while Aristolochi-aceae and Rafflesiaceae are thermogenic families (Thien et al. 2009), there is no evidence that the flies are attracted to the flowers during the night itself. Similarly, Hydnoraceae includes thermogenic trap blossoms, but the odor that attracts beetles is produced during the day and no noctur-nal visitors have yet been observed (Bolin et al. 2009). Also, in Nelumbonaceae, there is no evidence of nocturnal attraction by beetles, which are the major pollinators, although the flowers are thermogenic (Li and Huang 2009). This is in contrast to the thermogenic Araceae, e.g., Amorphophallus, which begin to emit odor at dusk (Punekar and Kumaran 2010).
Of the 413 families recognized in the APG III classification, 113 families had spe-cies with nocturnal pollination, 37 families have unknown pollination mechanisms, and 263 families have no evidence of nocturnal pollination (Table 1, see Appendixes 1 and 2 available at http://www.journals.uchicago .edu/loi/qrb). Therefore 113/376, or ap-proximately one-third of angiosperm fam-ilies, whose pollination sys tems are known, have species with nocturnal pollination. This is likely to be a conservative estimate since most studies on pollination are conducted on day-flowering species. At a higher taxo-nomic level, at least 42/61 = 69% of orders (with designated families) have species with nocturnal pollination (Table 1; excludes all orders marked with a “?”). This indicates the wide taxonomic occurrence of nocturnal pollination, presumably in some cases, due to convergent evolution.
Examining these trends phylogenetically, Malpighiales had the maximum number of families with nocturnal pollination (i.e., 10 out of 35 families; Table 1). In the monocots,
only the Acorales and the Petrosaviales did not have any families with nocturnal pollina-tion, although the other orders had represen-tation of this trait. In the other “clades,” there is no evidence for nocturnal pollination in the following orders: Ceratophyllales, Troch-odendrales, Buxales, Gunnerales, Dilleniales, Vitales, Fagales, Picramniales, and Garryales. In the following orders, pollination systems are unknown in some or all families, so the presence of nocturnal pollination cannot be determined: Berberidopsidales, Huerteales, Bruniales, and Paracryphiales. Across orders, Magnoliales, Pandanales, Arecales, Zingibe-rales, Myrtales, Gentianales, and Es calloniales (represented by only one family) had the highest percentage (at least 60%) of families with nocturnal pollination (Table 1). It must be remembered that our scoring of nocturnal pollination is at the family level; some orders and clades have many more families than oth-ers, and this factor must be considered when evaluating the phylogenetic occurrence of nocturnal pollination.
Using Phylomatic (Webb and Donoghue 2005; http://www.phylodiversity.net/phylo matic), we constructed a phylogeny for the 413 APG III angiosperm families and lo-cated the nocturnal/crepuscular families on the obtained phylogenetic tree, which was visualized using the program FigTree (http://tree.bio.ed.ac.uk/software/figtree/; Figure 1). The value of good phylogenies is essential to any analysis on functional traits (Hinchliff et al. 2015). As the figure shows, nocturnal pollination occurs throughout the tree of angiosperms and does not appear to be restricted to any particular groups, whether early or more recent. With its wide distribution, nocturnal pollination does not appear to be restricted to particular types of flowers. Is it possible then to understand what types of processes may have given rise to nocturnal pollination? We therefore ex-amine the abiotic environment that is char-acteristic of the night since pollinators that use this temporal niche must have abilities to function within this part of the diel cy-cle, and plants must also have an advantage to open their flowers during nocturnal or crepuscular periods.
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TABLE 1The frequency of nocturnal pollination across the angiosperm tree of life (the orders and families follow
Bremer et al. 2009 and Haston et al. 2009)
Order
Families with nocturnal pollination (percent
of families with nocturnal pollination excluding those with unknown pollination
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The Night (Including Dawn and Dusk) as a Niche Axis
During sunrise and sunset, the physical en-vironment changes in many respects that are important for plants and their pollinators.
The most direct effects of reduced electro-magnetic radiation from the sun are lowered light intensity and changes of temperature. However, these changes themselves strongly influence several other parameters, including
*This excludes Dasypoganales whose position in the Commelinids appears to be unsure; this family has no nocturnal pollina-tion reported.?, Undefined, or Unassigned indicates that the taxonomic position is unclear; families are arranged in the linear sequence of Haston et al. (2009).
TABLE 1 Continued
Order
Families with nocturnal pollination (percent
of families with nocturnal pollination excluding those with unknown pollination
mechanisms)
Families without
nocturnal pollination*
Families with
unknown pollination
mechanisms
Families with thermogenesis
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humidity, speed, and turbulence in air mo-tion—winds—and this again influences the speed, efficiency, and distance over which pollen or floral volatiles can be dispersed by abiotic factors. The changes in these param-eters are not the same in all habitats; they dif-fer between tropical and temperate zones, between mountains and lowland, between open habitats and forests, and between the understory and the canopy of a forest. In ad-dition, moon phase affects light levels. These changes influence the relationship between plants and their pollinators in many differ-
ent ways that will be discussed in later sec-tions but we will, in this section, concentrate on the changes themselves.
light and infrared radiationAs the sun sets, the intensity of electromag-
netic radiation falls continuously until the sun is 18° below the horizon. This is the same for visible light (for animal vision, this means light between 300 and 800 nm) and infrared or heat radiation (wavelengths up to 300 μm). Heat radiation influences temperature, but
Figure 1. Nocturnal/Crepuscular Families (in Bold and Marked with Black Circles Near Their Names) Located on the Apg III Angiosperm Tree of Life
See the online edition for a full-size version of this figure.
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tem perature changes vary to a large degree with landscape, vegetation, and weather con-ditions, and differ vastly between seasons and latitude. These changes are complicated be-cause they depend on changes in air move-ments, and will therefore be discussed with the other changes of the atmospheric bound-ary layer that occur at night.
Between a sunny day and full moon night, the light intensity differs by a factor of about one million, albeit with a similar spectrum (Figure 2A,B). On a moonless night, light intensity provided by stars is dimmer than moonlight by a factor of approximately 100 (Figure 2B), and the spectrum is consider-ably shifted toward long wavelengths (Fig-ure 2A; Johnsen et al. 2006; Johnsen 2012). Twilight is blue-shifted in comparison to di-rect sunlight or moonlight. The changes in light color are less obvious than the intensity change (Figure 2B) but may nevertheless be important for the detection of flower colors and pollinator vision under these conditions. Finally, both the moon and the sun create a pattern of polarized light scattered from the sky, and can be used by insects to navi-gate (Warrant and Dacke 2011), although no such pattern is present in a moonless sky.
In different habitats, and depending on weather conditions, light intensity can change for reasons other than described above. Un-der the more open canopy of a temperate or deciduous forest, intensity is reduced only by a factor of approximately 10, while in some tropical rainforests, the canopy may transmit as little as 0.1% of the light available above, and the wavelength spectrum is largely dom-inated by the green and infrared light that is not absorbed by chlorophyll (Endler 1993). This means that pollinators or flowers in the understory at dawn, dusk, or at night would be under more stringent illumination constraints.
Close to the equator, the dark period of the day lasts approximately 12 hours all year, including morning and evening twi-light periods of little more than one hour each. The further away from the equator, the influence of the seasons on day–night cycles is more pronounced. For example, at 50° latitude, the sun does not sink 18° below the horizon for 40 summer days, at 60° latitude, one-third of the year never gets
that dark, and twilight can last for six hours, while at 70° latitude, the sun does not set for more than two months. Fig ure 2C shows the duration of the midsummer night and the different phases of twilight as a func-tion of latitude. The respective light inten-sities are in Figure 2B. The full moon rises around sunset and sets around sunrise, and during full moon nights, light levels never drop below those at nautical twilight (when the sun is 12° below the horizon). The half moon rises or sets around midnight and reaches only lower light levels, and during the darkest moon phase, the moon is never up during the dark part of the night. The duration of the night therefore dif-fers largely across latitudes while the lunar phases vary similarly at each latitude, factors that should be relevant in a global under-standing of nocturnal pollination.
the atmospheric boundary layer at night: wind and temperature
The atmospheric boundary layer is the lowest part of the atmosphere where wind is influenced by surface friction from veg-etation and topography, and wind speed increases with height over ground. The thickness of the boundary layer depends on wind speeds and temperature, and the structure differs strongly between day and night (e.g., Grant 1997; Nadeau et al. 2011). Although the boundary layer is thick and characterized by convective turbulences due to solar heat radiation during the day, it is more stably stratified, thinner, and solely driven by wind shear at night when the Earth’s surface is colder than the air above. The temperature inversion starts close to the ground shortly before sunset, because the ground cools down, while warm air rises (Figure 3). As stratification depends on temperature, it is more stable in temperate zones where it can even last during day-time, although in the tropics, stratification may be less stable even at night. With a clear sky, the ground cools down more rap-idly, and inversion is more likely to occur than with a cloudy sky. Thus, in humid cli-mates, night temperature does not sink as much as in dry climates, and temperature inversion is less common.
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Generally, wind speeds at night tend to be lower than during the day (Figure 3), and there are two different scenarios: with strongly stable stratification, wind speeds above the inversion capping the boundary layer are larger than surface wind speeds, while with less stable stratification, wind speeds are distributed in a similar way as during the day (Monahan et al. 2011). In forested mountainous areas, at night, winds above and below the canopy are most often decoupled. The lower canopy flow is most often downhill (Sedlák et al. 2010) and wind speeds are usually lower at night under tropi-cal rainforest canopies (McCay 2003).
Temperature inversion has several effects. Most importantly, with the stable stratifica-tion under an inversion layer, pollutants but possibly also odorants released from plants are trapped and accumulate more than usual. Although this effect is well known, the changes in the atmospheric boundary layer during the late afternoon and evening, and again during the morning are not well un-derstood (Nadeau et al. 2011), and few stud-ies on the shape of odor plumes at night are available (e.g., Willis 2008; Girling et al. 2013).
humidityIn addition to temperature and winds, hu-
midity changes systematically between day and night, with generally higher relative hu-midity at night (Figure 3). As a result of large diurnal temperature varia tions, mean rela-tive humidity at night is up to 15% higher than daytime relative humidity over most land areas. This effect is weaker in humid climates and strongest in dry areas such as
deserts (Dai 2006). The diurnal humidity cy-cle varies considerably depending on terrain (e.g., Gebhart et al. 2001; Duane et al. 2008), and in heterogeneous structures such as val-leys, the characteristics of the boundary layer differs from textbook conditions described for homogeneous and flat terrain. For in-stance, in a coastal valley, temperature de-creases over the late afternoon and transport of cold moist air is important for nocturnal dew deposition (Khodayar et al. 2008).
Therefore, temperature, humidity, and latitude interact to influence ambient con-ditions in different ways that can affect flow ering plants and pollinators. Given the par ticular abiotic features of dawn, dusk, and the night, we now examine why and how plants and pollinators may use the noctur-nal niche.
Physiological Constraints in Plants Leading to Nocturnal PollinationDespite the fact that nocturnal pollina-
tion appears to be widespread, are there ecophysiological traits and processes that can help to predict its occurrence? We used BayesTraits V2 (http://www.evolution.rdg.ac .uk/BayesTraits.html) to determine whether plant traits that we examined evolved in-dependently on the phylogenetic tree. We used the Discrete module for examining correlated evolution between pairs of these discrete binary traits such as nocturnal pol-lination and any other traits. We used Mar-kov Chain Monte Carlo (MCMC) methods for calculating Bayes Factors (BF). A step-ping stone sampling method was used to estimate marginal likelihoods of the mod-els following the procedures recommended
Figure 2. Light Conditions During Dusk, Night, and DawnA. The number of photons of different wavelengths before sunset (sun at 11.4° elevation), at sunset, and
during nautical twilight (sun at 10.4° below the horizon), and with a full moon and starlight. Note that dim twilight is dimmer and strongly blue-shifted compared to moonlight, and that starlight is strongly red-shifted. B. The illuminance as a function of solar (upper two curves) and lunar (lower three curves) elevation. Starlight illuminance (gray shaded zone) differs with time of year and region. Vertical lines give limits: 0°: sunset/sunrise; -6°: civil twilight; -12°: nautical twilight; -18° of astronomical twilight, which is when the sun or moon no longer contributes to illuminance. The luminance values are approximations, and indicate the luminance of a white surface positioned horizontally, in an open landscape given the indicated illuminance. C. Duration of the night in different regions, given for 21 June in the Northern Hemisphere, or 21 December in the Southern Hemisphere as a function of latitude.
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in Cooper et al. (2015) who adopted this method since it has been shown to be su-perior at estimating marginal likelihoods compared to other methods. In the step-ping stone method, we sampled 50 step-ping stones from a beta distribution with α = 0.4 and β = 1; each stone was sampled for 20,000 iterations with the first 5000 iter-ations (burn-in) being discarded (Cooper et al. 2015). MCMC runs equalled 1,000,000 iterations with a prior drawn from an expo-nential distribution of mean 10. In the Dis-crete module, we examined models where the traits evolve in a correlated fashion such that the rate of change in one trait depends upon the background state of the other (dependent model), as well as mod-els where the traits evolve independently of each other (independent model). In these cases, BF = 2 (likelihood of depen-dent model – likelihood of independent model). Correlated evolution between pairs of binary states is considered to have oc-curred when the BF value exceeds the crit-ical value of a χ 2 distribution with df = 4 (considering the number of possible tran-sitions between the states; Pagel 1999; Giv-nish et al. 2014).
Since a major difference between day and night pollination is the light level at which pollination occurs, and since plants need light for photosynthesis, can the type of photosynthesis help to explain the observed patterns of nocturnal pollination? Of the 113 plant families with evidence of noctur-nal pollination, 109 (96.5%) engage in C3 photosynthesis (with or without C4 or CAM photosynthesis), nine families employ the C4 photosynthesis system, and 21 fam ilies employ CAM photosynthesis (with three families that had exclusively CAM photo-synthesis; Table 2). It is clear therefore that nocturnal pollination is mostly represented
in families with C3 photosynthesis. Moreover, of the 31 angiosperm families in which CAM photosynthesis has been reported (Silvera et al. 2010), nocturnal pollination is present in 21 families (Table 2). In two CAM families where nocturnal pollination is absent, the plants are aquatic and exhibit aquatic CAM. Therefore, 21 of 31 families (67.8%) with CAM are nocturnally pollinated. We found that over the phylogeny, CAM and nocturnal pollination are correlated traits (marginal likelihood values for the dependent model = -342.7, and for the independent model = -353.1; BF = 20.7, p < 0.001 under a χ 2
dis-tribution). Of the 17 angiosperm families in which C4 photosynthesis has been reported (Sage 2001), three are monocots (Poaceae, Cyperaceae, Hydrocharitaceae) that are mostly pollinated by wind and have no nocturnal pollination; the remaining 14 families (Amaranthaceae, Euphorbiaceae, Asteraceae, Polygonaceae, Acanthaceae, Portulacaceae, Caryophyllaceae, Zygophyl-laceae, Boraginaceae, Aizoaceae, Nyctag-inaceae, Scrophulariaceae, Molluginaceae, and Capparaceae) are dicots of which 10 families have examples of nocturnal pol-lination; there appears to be a prepon-derance of nocturnal pollination in dicot families with C4 photosynthesis (71.4%).
Since CAM and C4 photosynthesis are be-lieved to be adaptations to warm and dry conditions (Sage 2001; Lüttge 2004; Sage et al. 2014), this therefore led us to ask whether there is a preponderance of noc-turnal pollination in families whose repre-sentatives are reported within xerophytic conditions or have specific adaptations to hold water, e.g., succulence. We catego-rized the 113 families in which nocturnal pollination has been reported into: helo-phytic families if most plants in this fam-ily appeared to be living near streams and
Figure 3. Schematic of the Changes in (from Top to Bottom) Wind Speed, Relative Humidity, Air and Surface Temperature, and Temperature Gradient
A normal gradient means that temperature decreases with elevation above the surface while inversion indicates that a warmer air layer is found at higher elevation. Note that sunrise and sunset hours (approximately indicated by gray shaded areas) as well as the amplitude of all of these changes differ considerably between latitudes and time of the year. Gradients also differ with absolute humidity and elevation over sea level. For instance, in the wet tropics, the temperature changes are much smaller than in a dry climate. Wind speeds also strongly depend on surface topography.
Nymphaeaceae h h, p, m C3 lSchisandraceae m h, p C3 o, mPiperaceae m p, b CAM o, mMyristicaceae m p C3 o, m, lMagnoliaceae m h, p C3 o, mEupomatiaceae m b, p (staminode material) C3 oAnnonaceae m h, p C3 m, r, o Siparunaceae m b C3 o Monimiaceae m f C3 o, mLauraceae m p, n C3 o, mAraceae m h, p C3, CAM lBurmanniaceae m n C3
Velloziaceae x n C3
Cyclanthaceae m h, m, b, f C3 l, mPandanaceae m n, p C3 mColchicaceae m n, p C3
Liliaceae x n C3
Orchidaceae x n C3, CAM mAsteliaceae x n C3 mIridaceae x n C3 m, oXeronemataceae x n C3 Xanthorrhoeaceae x n, p C3, CAM mAmaryllidaceae m n C3 m, lAsparagaceae x n C3, CAM mArecaceae/Palmae x h, m, b, n, f, p C3 mHaemodoraceae x n C3 m?Strelitziaceae m n C3 mHeliconiaceae m n C3 mMusaceae m n C3 l, mCannaceae m n C3 mZingiberaceae m n C3
Bromeliaceae x n CAM mRanunculaceae m n C3
Proteaceae x n, p C3 sCrassulaceae x n CAM mZygophyllaceae x n, p C3, C4 mFabaceae/Leguminosae x n, p C3 m, r, o Rosaceae x n C3 mRhamnaceae x n C3 mMoraceae m b, n C3 m, lCucurbitaceae x n, p C3, CAM lCelastraceae x n C3 m, lElaeocarpaceae x n, p C3 mRhizophoraceae h n C3 mEuphorbiaceae x n C3, C4, CAM m, lPhyllanthaceae m n C3 mChrysobalanaceae m n C3 mPassifloraceae x n, p C3, CAM mSalicaceae x n C3 m, r, h, oViolaceae m n, p C3 m, oAchariaceae m n, p C3 mCaryocaraceae x n C3 m, r?
continued
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Clusiaceae/Guttiferae x n, p? C3, CAM l, r, oGeraniaceae x n C3, CAM m, oCombretaceae x n C3 h, mLythraceae x n C3 mOnagraceae x n, p C3 m, oVochysiaceae x n C3 m, sMyrtaceae x n C3 m, l, oMelastomataceae x n, p C3 m, oStrasburgeriaceae m n s, mStachyuraceae m n C3
Anacardiaceae x n C3 l, r, mSapindaceae x n C3 m, lRutaceae x n C3 m, oMeliaceae m n C3 m, l, rCytinaceae m nMalvaceae x n, p C3 m Thymelaeaceae x n C3 mDipterocarpaceae m n, p C3 r, mCaricaceae x n C3 lSalvadoraceae x n C3
Capparaceae x n, p C3, C4 mCleomaceae x n C3, C4
Brassicaceae/Cruciferae x n C3 m
Balanophoraceae m n, p, bSantalaceae x n C3
Loranthaceae x n C3 mNepenthaceae h n C3
Caryophyllaceae x n C3, C4 mAizoaceae x n C4, CAM mNyctaginaceae x n C3, C4
Cactaceae x n C3, CAM l, mLoasaceae x n, p? C3
Balsaminaceae m n C3 h, mMarcgraviaceae m n C3 mPolemoniaceae x n C3 mLecythidaceae m n C3 mSapotaceae m n?, f C3 l, m, rPrimulaceae x n C3 h, sEricaceae x n C3 m, oRubiaceae x n C3, CAM mGentianaceae m n C3 m, oLoganiaceae x n C3 mApocynaceae x n, p C3, CAM l, mBoraginaceae x n, p C3, C4 mConvolvulaceae x n, p C3 lSolanaceae x n, p C3 m, oGesneriaceae m n C3, CAM rPlantaginaceae x n C3, CAM hScrophulariaceae x n C3, C4 o, hLamiaceae/Labiatae x n C3, CAM h, o
have an affinity for water; mesophytic fami-lies if plants in this family occupied habitats of intermediate water regimes, neither too wet nor too dry; and xerophytic families if there was evidence that at least some plants in this family are xerophytes and oc-cupy areas where water is scarce (Table 2). We found that 67 families with nocturnal pollination have xerophytic representa-tives, four families are mostly helophytes, and 42 are mesophytic. When we scored these traits over the entire phylogeny (and pooled helophytic and mesophytic traits into one category), we found that noctur-nal pollination and xerophytism are highly correlated traits (marginal likelihood val-ues for the dependent model = -427.1, and for the independent model = -472.8; BF = 91.5, p << 0.001 under a χ 2
distribution). Therefore, xerophytism is more likely to occur in families with nocturnal/crepuscu-lar pollination than those with helophytic or mesophytic representatives. We there-fore scored the occurrence of the follow-ing features that may aid plants to cope with water stress or function as an adap-tation to water regimes: mucilage, resin, hydathodes, secretory canals, laticifers, or any other special feature for water storage (Table 2). We found that plants in 92 out of the 113 nocturnally pollinated families
(81.4%) have at least one of these features, while in only 21 of these families was there either no information on their occurrence or none of these features occurred. We sim-ilarly found that nocturnal pollination and the occurrence of any water-holding trait (Table 2) in angiosperm families are highly correlated traits (marginal likelihood val-ues for the dependent model = -467.4, and for the independent model = -520.9; BF = 107.0, p <<< 0.001 under a χ2
distribution).
The Arid Hypothesis for Nocturnal Flowering and Pollination
We therefore propose the arid hypoth-esis for nocturnal flowering and thereby nocturnal pollination, according to which plants that are water-stressed should pref-erentially flower at night since they can reduce water loss by doing so. Flowering is a water-demanding process requiring wa-ter at all stages from flower bud maturation to flower opening, and also for mainte-nance of turgor in floral organs as well as nectar production (Mohan Ram and Rao 1984; Galen et al. 1999; Galen 2000; De la Barrera et al. 2009). Such water de-mands can only be met from the vegeta-tive parts of the plant after water loss by evapotranspiration.
Orobanchaceae m n C3 hLentibulariaceae h n C3
Acanthaceae x n C3, C4 m
Bignoniaceae m n, p C3
unique phloem for holding water
Verbenaceae x n C3 mCampanulaceae x n C3 lAsteraceae/Compositae x n C3, C4, CAM lEscalloniaceae m n C3
Adoxaceae m n C3
Araliaceae x n C3 s, rApiaceae x n? f? C3, CAM s, r, m
*h = helophytic; m = mesophytic; x = xerophytic#h = heat; p = pollen; m = mating site; b = brood site; f = floral tissue; n = nectar+l = laticifer; o = oil; m = mucilage; r = resin canal; h = hydathode; s = secretory canal. Blanks indicate no information.*Linear sequence of families follows Haston et al. (2009).
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In the Polemoniaceae, a family with C3 photosynthesis, the influence of water stress has, for example, led to flower sizes of di-urnally opening flowers in Leptosiphon bi-color being smaller in sites with lower soil moisture than in those with higher soil moisture (Lambrecht 2013). Large flow-ers could only be produced in dry sites if leaves closed their stomata during the day to prevent water loss (Lambrecht 2013). Similarly, Galen et al. (1999) showed that flower size in the diurnal Polemonium vis-cosum (Polemoniaceae) is positively related to water uptake during bud expansion and anthesis; plants with larger flowers take up more water. In another set of five species of unknown photosynthesis type, flower size was larger in sites with greater moisture content (Lambrecht and Dawson 2007). Clearly, flowering imposes a heavy water cost on plants. In avocado trees, 13% of transpirational water loss was due to loss from floral organs (Whiley et al. 1988). This may be a general trend across plants.
In Agave deserti (Asparagaceae), a noc-turnally pollinated CAM plant, a mature plant requires about 18 kg of water during flowering; this is mainly supplied from leaf water stores; 4 kg of this water is taken up by the leaves of which 80% is transpired (Nobel 1977). Abundant watering of A. de-serti can cause these plants to shift from the CAM mode of nocturnal stomatal opening to diurnal stomatal opening (Hartsock and Nobel 1976), affirming that CAM photo-synthesis is a response to water stress (Her-rera 2009). The large flowers of the diurnal CAM plant Opuntia ficus-indica (Cactaceae) lose 15% of their mass by transpiration during anthesis (De la Barrera and Nobel 2004). It can be clearly seen that water is a limiting factor on flower size and this may be more so for C3 plants in which stomata are necessarily open during the day. In such plants, opening flowers at night and engaging in nocturnal pollination would be a valuable water conservation strategy. It is not surprising, therefore, that noctur-nal pollination is mostly represented in C3 families as we have shown earlier. Fur-thermore, if nocturnal blooming is an ad-aptation primarily to deal with water stress
then, by having flowers open at night when transpiration losses are likely to be much lower than in the day, the constraint on flower size may be lifted. This may conse-quently also allow for the production of larger flowers or inflorescences with abun-dant nectar, which may support larger noc-turnal pollinators such as bats and large moths. Plants with C4 photosynthesis have greater water use efficiency (defined as the ratio of the rate of carbon assimilation by photosynthesis to the rate of water loss by transpiration); sustaining high rates of pho-tosynthesis even when stomatal conduc-tance is low results in lowered transpiration and protection of the hydraulic system un-der water stress conditions, allowing C4 plants to colonize dry environments (Os-borne and Sack 2012). It is also possible that those plants in which stomata are open at night (as happens during CAM photosynthesis) would be predisposed to nocturnal flowering. Considering that noc-turnal pollination is significantly more frequent in those families that occupy water- stressed environments, it is reasonable to speculate that opening flowers at night helps to relieve water stress. It appears nec-essary to learn much more about water as an important cost of flowering to under-stand the evolution of nocturnal flowering and nocturnal pollination in plants.
Despite the fact that water is so important in the process of flowering, it is phloem and not xylem that supplies water to nectar (De la Barrera and Nobel 2004). However, floral nectar is not merely excreted phloem sap, and considerable synthesis of nectar com-ponents probably occurs within the nectary itself (Escalante-Pérez and Heil 2012; Cha-nam et al. 2015). Floral nectar, especially that produced by succulents, is copious; e.g., Aloe marlothii in southern Africa pro-duces 50–100 liters of nectar/ha resulting in 100,000–200,000 kj/ha in terms of en-ergy production (Wolf and Hatch 2011). Therefore, plants that can save water by opening during the night could support populations of nocturnal pollinators by pro-ducing sufficient quantities of nectar. This may have resulted in the radiation of large nocturnal nectarivores such as bats and large
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moths. Bat-pollinated plants, at least in the Neotropics, also tend to be more repre-sented in arid habitats (Fleming et al. 2009).
Since nocturnal pollination also occurs in a wide range of families, it is possible that a variety of plant species that experience varied amounts of water stress, depending on which habitat or habitat stratum they occupy, may profit from flowering at night and hence may make the switch from di-urnal to nocturnal flowering. For example, low availability of water is an important stressor in epiphytes (Zotz and Hietz 2001) even when they occur in rainforests (Lüttge 2010); consequently, many epiphytes adopt CAM photosynthesis (Lüttge 2004) espe-cially when they are in dry forest canopies (Nadkarni et al. 2001), while C3 photosyn-thesis prevails in epiphytes in the canopies of cloud forests (Nadkarni et al. 2001). It would be interesting to speculate on the specific occurrence of nocturnal pollina-tion in different habitats and even different habitat strata with varying levels of water stress. Information about abiotic factors is clearly required to predict the occurence of nocturnal pollination.
Given the huge diversity of families that show examples of nocturnal pollination, it is difficult to make general statements about floral traits of nocturnally pollinated plants. However, nocturnally pollinated flow-ers tend to be light/pale/white in color (Baker 1961). Since flower pigments such as flavonoids provide floral organs with pro-tection against heat stress resulting in higher pollen performance and seed production (Coberly and Rausher 2003), it is tempting to suggest that by flowering at night, plants are removed from the constraints of produc-ing pigmented flowers and could therefore produce white or pale-colored flowers, which may also have the added advantage of being highly conspicuous during the night. Since flower pigment genes also have pleiotropic effects (Coberly and Rausher 2008), the tar-gets of selection on white-colored flowers may be varied; however, all else being equal, it is worth considering the lower tempera-ture at night as a positive selection pressure for white corollas. On the other hand, dark red flower color may have been retained in some bat-pollinated flowers as a relic of an-
cestral bird pollination (Tschapka and von Helversen 1999) or to prevent discovery by sphingid nectar robbers (von Helversen 1993). Clearly, the visual and overall sensory sys-tems of pollinators need to be taken into consideration to understand these flower color tran sitions.
Nocturnal Pollinators
For nocturnal pollination, plants have to recruit nocturnal animals as pollinators by offering rewards. Considering the di-versity of animals that are active at night, the taxonomic representation of known nocturnal pollinators is limited (Table 3). Among the invertebrates, moths and bee-tles are the major nocturnal pollinators. Moths are well studied while beetle pollina-tion is generally understudied with respect to diurnal versus nocturnal activity. Of the hymenopterans, several species of smaller and larger bees such as Sphecodogastra or Megalopta are crepuscular pollinators (Kel-ber et al. 2006), but the large carpenter bee Xylocopa tranquebarica is currently the only known nocturnal bee to be active even during moonless nights (Somanathan et al. 2008a). Yet, even the generally diurnal rock honey bee Apis dorsata and the African race of honey bee Apis mellifera adansonii can forage and act as pollinators during half-moon nights (Dyer 1985). In the Diptera, gall midges and fungus gnats are impor-tant nocturnal pollinators (e.g., Yuan et al. 2008; Luo et al. 2010; Duque-Buitrago et al. 2013). A few plants are nocturnally polli-nated by mosquitoes and calliphorids, cock-roaches and orthopterans (a cricket and a weta), and ants (Table 3, Appendixes 1 and 2).
Of the vertebrates, bats are the most im-portant nocturnal pollinators (Table 3). In the order Chiroptera, nectar foraging has evolved independently more than once in the Old World family Pteropodidae, and in the New World family Phyllostomidae (Fleming et al. 2009; Fleming and Kress 2013). Several nocturnal nonflying mam-mals such as marsupials, lemurs, shrews, and rodents also participate in pollination (Carthew and Goldingay 1997; Goldingay
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2000). In a few cases, geckos engage in nocturnal pollination (e.g., Eifler 1995; Godínez-Álvarez 2004). Rodent pollination is prevalent in geophytic plants (e.g., Turner et al. 2011), as is the case for ant pollina-tion (e.g., de Vega et al. 2009).
Many examples of unusual pollinators such as geckos occur in habitats such as islands (Whitaker 1987), where there may be a dearth of regular nocturnal pollina-tors. Other such examples include rodents substituting for bats in a cloud forest (Lu-mer 1980), moths substituing for bats on remote Japanese islands where bats are ab-sent (Norio 2004), or weta pollination in stressful habitats such as high-altitude for-ests in New Zealand (Lord et al. 2013). Such unusual pollinators may be referred to as opportunistic, i.e., being in the right place at the right time. In some cases, these unusual pollinators are nectar specialists as in the New Zealand Hoplodactylus gecko that feeds on honeydew when nectar is scarce (Gardner-Gee and Beggs 2010).
The requisites for pollen transfer, which are mobility as well as pollen adherence, may restrict the types of taxa that can be effective during nocturnal pollination. This is why, for example, although thrips are found in flowers during the night, they cannot move long distances between plants since they are dependent on the wind for transportation, making them rather unreliable for cross- pollination (Sakai et al. 1999; Webber et al. 2008) since wind speeds are lower at night.
The vast majority of nocturnal pollinators consume nectar as a reward, although Hy-menoptera, some rodents, gall midges, and beetles collect pollen and, in some families, floral tissue or staminodes are also rewards (Table 2). Some pollinators utilize floral re-sources as mating sites and/or brood sites where eggs are laid and offspring develop; heat produced by floral tissue is a reward in several systems (Table 2).
The basal or ANITA grade angiosperm families are mostly pollinated by Diptera and Coleoptera (Thien et al. 2009) with gall midges and beetles engaging in noc-turnal pollination in several families (Ap-pendix 1). Insect pollination may have occurred as early as the Permian (250–300 million years ago; Labandeira 2013).
Long-proboscid nectar-feeding insects may have pollinated angiosperm flowers since the Cretaceous over 100 million years ago (Labandeira 2010, 2013) and it is possible that some of these (for instance, nematoc-erans) were nocturnal. In contrast, the first nectar-feeding phyllostomid bats evolved from initially insectivorous bats less than 30 million years ago in the early Miocene (Datzmann et al. 2010), and other noc-turnal vertebrates were recruited as polli-nators possibly even later. How the more ancient origin of insect versus vertebrate nectar feeding has affected the divergence of nocturnally pollinated plant lineages is completely unknown, and may be signifi-cant given that nectar is an important re-ward in most nocturnally pollinated plant families.
Sensory and Physiological Adaptations and Constraints
of Nocturnal PollinatorsNocturnal pollinators, obviously, have
to combine traits that enable them to: use nectar and/or pollen or other rewards of-fered by nocturnal flowers; move pollen efficiently between flowers and plants; and be active and do all of this at night. For all of the major groups of pollinators, there is copious literature including several re-cent books on the first two topics, i.e., the general adaptations to a nectar or pollen diet and to moving pollen (e.g., Waser and Ollerton 2006; Patiny 2012; Fleming and Kress 2013). Therefore, we will focus on the third topic, the sensory and physiolog-ical adaptations of pollinators to a noctur-nal lifestyle.
Adaptations to features of the night in nocturnal pollinators include adaptations to locomotion in low temperature and low humidity, adaptations to sensing flowers, and to navigation between them in dim light and with low wind speeds. Although nocturnal birds and bats prey upon noctur-nal pollinators, the night may be a temporal niche with lower predation pressure (e.g., Wcislo et al. 2004). Nocturnal pollinators include a diverse range of animal groups (Table 3), among which moths and bats are most species-rich and quantitatively most
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TABLE 3 Taxonomic groups with nocturnal pollinators
Order Family References (see also Appendixes 1 and 2)
Class InsectaOrthoptera Gryllacrididae Micheneau et al. 2010Blattodea Blattellidae Vlasáková et al. 2008Hymenoptera Formicidae de Vega et al. 2009
Vespidae Nakase and Kato 2012Andrenidae Kelber et al. 2006Halictidae Kelber et al. 2006Apidae Somanathan and Borges 2001; Kelber et al. 2006; Somanathan et al.
2008a,bColletidae Linsley and Cazier 1970
Coleoptera Scarabaeidae Hirthe and Porembski 2003; Gottsberger et al. 2011Anthicidae Armstrong and Drummond 1986Curculionidae Bergstrom et al. 1991; Franz 2007
Lepidoptera Noctuidae Faegri and van der Pijl 1979GeometridaeSphingidaeProdoxidae yucca moths Pellmyr 2003Gracillariidae Kawakita and Kato 2004Pyralidae Kawakita and Kato 2002
Diptera Culicidae Branjtes and Leemans 1976; Kato 1996Cecidomyiidae (gall midges)
Feil 1992; Yuan et al. 2008
Mycetophilidae(fungus gnats)
Vogel and Martens 2000; Duque-Buitrago et al. 2013
Sciaridae (fungus gnats) Vogel and Martens 2000; Duque-Buitrago et al. 2013Tipulidae (craneflies) Primack 1983Calliphoridae Kato 1993
Class ReptiliaSquamata Gekkonidae Newstrom and Robertson 2005Class MammaliaInfraclassMarsupialiaDidelphimorphia Didelphidae Carthew and Goldingay 1997Diprotodontia Phalangeridae Carthew and Goldingay 1997
Petauridae Carthew and Goldingay 1997 BurramyidaeAcrobatidaeTarsipedidae
Dasyuromorphia DasyuridaeInfraclass EutheriaChiroptera Phyllostomidae Fleming et al. 2009
MystacinidaePteropodidae
Macroscelidea Macroscelididae (elephant shrew)
Carthew and Goldingay 1997; Johnson et al. 2011
Rodentia Muridae (mice and rats)Gliridae (dormice) Carthew and Goldingay 1997
Cricetidae (voles) Carthew and Goldingay 1997
Petauristidae Ganesh and Devy 2000
continued
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important, and we will mainly concentrate on adaptations in these groups but mention other cases, such as the repeated evolution of nocturnal activity in bees (e.g., Kelber et al. 2006). Animal groups that could not adapt to all of these demands do not con-tribute to nocturnal pollination. As pointed out earlier, we need to keep in mind that the features of the night differ between lat-itudes and climate zones. Perhaps the most obvious difference in the duration of the night is reflected in the activity patterns of crepuscular pollinators, which are active during dawn and dusk periods. Although crepuscular moths have a long activity pe-riod in northern Sweden, their activity win-dows can be as short as half an hour close to the equator ( Johnson and Nilsson 1999; Kelber et al. 2006; Martins and Johnson 2007).
locomotion at low temperatures and humidity
For efficient pollen transfer, pollinators are required to move between plants; thus most pollinators—with the exception of some in-sects (such as ants), geckos, and nonflying mammals—use flight for locomotion. Lo-comotion at night functions under very dif-ferent constraints in different climate zones. In tropical rainforests, temperature does not change much between day and night. How-ever, in temperate and dry habitats, night temperatures are considerably lower than day temperatures (see earlier sections), and here nocturnal or crepuscular flight may be an adaptation to avoid high temperatures and low humidity during the day (Willmer and Stone 1997).
Many nocturnal insect pollinators have good temperature control and preheat flight muscles prior to taking flight. For instance, hawkmoths fly at 40°C muscle temperature allowing for fast long-distance flight, and they can easily overheat at high environ-mental temperatures (Heinrich 1971). A direct example of insects using the crepus-cular period to escape overheating is seen in the hawkmoth Macroglossum stellatarum, which is generally purely diurnal but has an activity peak after sunset under Medi-terranean hot summer conditions (Her-rera 1992). In colder climates, nocturnal or crepuscular insects often have an insu-lating layer of cuticular hairs as in moths (Heinrich 1993). Also, the truly nocturnal Asian carpenter bee X. tranquebarica, which can fly at low temperatures, is more densely pubescent than its diurnal congeners (per-sonal observations). Thick pelage, thoracic shivering, and counter-current exchangers that slow down heat flow to the head and ab-domen enable moths to fly at low tempera-tures (Heinrich 1987). Geometrid moths may fly at low temperatures by having un-usually low wing loading that enables low en-ergy expenditure for flight even if thoracic muscle temperature is at ambient freezing temperatures (Heinrich and Mommsen 1985). Midges and mosquitoes that fly at low temperatures have high metabolic rates, and scarab beetles can also raise thoracic temperatures and fly at low temperatures (Morgan 1987; Heinrich 1993).
Freeze tolerance has independently evolved at least six times among the insects (in the Blattaria, Orthoptera, Coleoptera, Hymenoptera, Diptera, and Lep idoptera; Sinclair et al. 2003). The New Zea land weta
Carnivora Viverridae Carthew and Goldingay 1997Procyonidae Carthew and Goldingay 1997
Primates Cheirogaleidae (Dwarf lemurs) Carthew and Goldingay 1997; Heymann 2011
Lemuridae Carthew and Goldingay 1997; Heymann 2011Galagidae
Lorisidae (potto)Aotidae (night monkey)
TABLE 3 Continued
Order Family References (see also Appendixes 1 and 2)
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that pollinates megaherbs at night on the subantarctic Campbell Island is active at temperatures of 3 – 4°C (Lord et al. 2013). In tropical and humid habitats, tempera-tures do not change much between day and night. It is therefore interesting that only freeze-tolerant groups of insects are in-volved in nocturnal pollination, which may imply that these groups have wider thermal tolerance than other insect groups, facili-tating their locomotion and functionality even at extremely low temperatures.
Among mammals, nectar feeders have body temperatures that, although higher than those of carnivores, are lower than those of other herbivorous species (Clarke and O’Connor 2014). The high energy demands of both large hawkmoths and bats indicate that nocturnal flowers have to produce rel-atively large amounts of nectar, especially since nectar-feeding bats, unlike some other bats, consume their body fat on a daily basis (Voigt and Speakman 2007) and do not have the ability to go into a state of torpor when inactive to save energy when resting (e.g., Bartholemew et al. 1970). Copious nectar production has long been known for bat-pol-linated flowers (e.g., Faegri and van der Pijl 1979; Winter and von Helversen 2001), but may be more variable among groups polli-nated by moths (Haber and Frankie 1989). Since large body size is also correlated with low ambient temperatures in ectotherms (Atkinson 1994), some nocturnal pollinators may also be larger than their diurnal coun-terparts. For example, larger body size and thick pelage enable cold tolerance in bees (Bishop and Armbruster 1999).
Stratum of flight at night also needs to be understood in terms of pollinator phys-iological capabilities and thereby stratum of pollinated flowers; e.g., nocturnal Meg-alopta bee species were found in high can-opy traps at 30 m as well as in low traps (Roubik 1993). Mycetophilids and sciarids (both fungus gnats), on the other hand, fly close to the ground (Peng et al. 1992; Eberhard and Flores 2002) and being weak fliers (Lewis 1967) are suitable for pollina-tion of the Araceae and terrestrial orchids (Appendix 2). Craneflies or tipulids are also weak fliers and keep to ground levels
(Heath and Derraik 2005) while nocturnal moths fly at all strata (Ashton et al. 2016).
sensory adaptations for finding flowers at night
Pollinators sense flowers mostly by vision and olfaction. Visual cues become less reli-able when light intensities are low, thus noc-turnal pollinators—just as other nocturnal animals—have a number of adaptations for seeing well in dim light: large eyes relative to body size, large pupils relative to focal length, highly sensitive photoreceptors, and neural mechanisms for pooling signals in space and time (e.g., Kelber and Roth 2006; Warrant 2008). This allows them to reliably detect the highly reflective noctur-nal flowers against the dark backgrounds of the night sky and vegetation. In addition, larger nocturnal pollinating insects, such as hawkmoths and large carpenter bees, can discriminate colors even in dim light when humans and most other animals are color blind (Kelber et al. 2002; Kelber and Roth 2006; Somanathan et al. 2008b).
Although vision becomes less reliable in the dim light of the night, flower odor may become a more reliable and more long- ranging cue. Wind speeds are lower at night, but there is less turbulence (Nadeau et al. 2011); thus odor plumes are carried longer distances with less disturbances (see above) allowing pollinators to find flowers from further away. It is therefore not sur-prising that nocturnal moths—in contrast to diurnal species—rely more on olfaction than on vision, both innately and after learning a food source (Balkenius et al. 2006). Despite this preference, the majority of nocturnal pollinators use both olfactory and visual stimuli (e.g., Kelber et al. 2002; Raguso and Willis 2003; Riffell and Alarcón 2013). Additionally, nocturnal hawk moths use gradients of CO2 that indicate floral respira-tion (Thom et al. 2004; Goyret et al. 2008) and gradients of humidity arising from nec-tar evaporation (von Arx et al. 2012) to lo-cate flowers at closer range. Moreover, once having found flowers by using long-distance cues, nocturnal moths appear to also use tactile cues from flowers to a greater extent
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than diurnal moths (Balkenius et al. 2006; Goyret 2010; Goyret and Kelber 2011) sug-gesting that successful nocturnal flower vis-itation may demand the recruitment of a greater number of sensory modalities.
Among bats, the Pteropodidae also use a combination of visual and olfactory cues for flower detection (Fleming et al. 2009), but in dim light they use their rod photorecep-tors restricting them to the use of brightness instead of color cues (Winter et al. 2003). Interestingly, although many bat-pollinated flowers are white or brightly colored, others have dull colors, and thus are more likely to rely on their scent to attract bats. In addition to visual and olfactory cues, the Phyllostomi-dae can also use echoes from flowers (von Helversen and von Helversen 1999; Simon et al. 2011), yet this is necessarily a shorter- distance cue compared to vision or olfaction.
Gall midges are weak fliers and are likely attracted by scent (Luo et al. 2010). They have very sensitive antennae (Hall et al. 2012) and also a unique type of fused sensillum called the circumfila (Boddum 2013). Gall midges also have infrared (IR) receptors (Zahradnik et al. 2012) and may use these to find the large thermogenic flowers of the Schisandraceae (Takács et al. 2009). At night, such flowers present a higher IR contrast against the background and this may be used as an effective flower location signal. Al-though the eyes of diurnal and nocturnal mosquitoes differ (Land et al. 1999), whether they use vision to find flowers is unknown. Nocturnal mosquitoes are, however, attracted by floral scents (Brantjes and Leemans 1976; Jhumur et al. 2007). Very little work has been done on color vision in flower-visiting beetles (e.g., Dafni et al. 1990; Keasar et al. 2010; Martínez-Harms et al. 2012), while considerably more is known about olfactory attraction in beetles, including those visiting flowers at night (Maia et al. 2012; Pereira et al. 2014). The spread of the olfactory sig-nal may also be helped by thermogenesis in some beetle-pollinated flowers.
In addition to finding flowers, nocturnal pollinators need to be able to move between flowers at night, demanding good orienta-tion, navigation, and a spatial memory. These topics have generally attracted relatively lit-
tle research, but both hawkmoths and bats are known to have good spatial memories (hawkmoths: Balkenius et al. 2004; bats: Win ter and Stich 2005). Nocturnal moths (see Warrant and Dacke 2011), bees (Baird et al. 2011), and bats (Fleming et al. 2009) use visual cues for flight control and naviga-tion emphasizing the necessity for large, highly sensitive eyes in nocturnal pollinators.
Gaps and the FutureThe night is a temporal niche in which
light, wind, and temperature levels are gen-erally lower while humidity levels are higher than during the day. Although it is a niche that frees plants from water constraints, a night-flowering plant is unlikely, for instance, to be wind-pollinated. If plants are to be biot-ically pollinated at night, they need the ser-vices of those pollinators that can overcome the physiological constraints imposed by the entire night or certain parts of it (see Table 4 for known and suggested traits of noctur-nally pollinated plants and pollinators). For example, some plants may open flowers in the early evening or morning (dusk and dawn) and use the services of those pollina-tors that are not fully visually adapted to the night but have just high enough visual sensi-tivity to navigate in twilight. On the pollina-tor side, very small species may often lack the capacity to see well enough at night. What constrains the evolution of nocturnal activity across pollinator taxa is not well understood. We are not aware of any attempt to explain why common diurnal pollinator groups such as birds have not expanded their activity into the night, or why there is scarce evidence of taxa such as wasps being engaged in noctur-nal pollination.
Some plants may inhabit areas where cli-matic conditions are harsh both during the day and night; such plants, as in the high Andean Espeletia (a giant caulescent rossette plant) may utilize the services of diurnal and nocturnal pollinators since pollinator num-bers are usually low in such extreme con-ditions (Fagua and Gonzalez 2007). Many plants that inhabit similarly challenging en-vironments in South Africa such as the Ka-roo employ nocturnal rodents as pollinators
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(Kleizen et al. 2008). It would be interesting to investigate whether plants have shifted flowering to particular parts of the night or day in response to the availability of physio-logically capable pollinators, or vice versa. It is also possible that there is a gradient in flower
opening times, flower sizes, and rewards that corresponds to a gradient in the energetic needs and sensory capabilities of the polli-nators that would also partly scale with their body sizes. Even within a single habitat, we may expect gradients in drought and expo-
TABLE 4Plant and pollinator traits that could facilitate nocturnal pollination
Plant traits Pollinator traits
Low light levels
a) High conspicuousness of flowers by increased achromatic contrast
b) If flower pigments are selected for protection against heat and ultraviolet damage, then at night, these constraints are removed; therefore, flowers can afford to be pigmentless (i.e., white) at night
c) Large floral display per plant (many small flowers or few large flowers) for high conspicuousness
d) Flowers easily accessible and therefore readily visible
e) Visual signalling likely to be coupled with chemical signaling in the form of scents produced by floral and associated tissues
a) Simple eyes: large eyes, large pupils, short focal length, long photoreceptor outer segments, spatial and/or temporal pooling
b) Compound eyes: for moths: superposition optics; for bees: large ommatidia, large rhabdoms, spatial and/or temporal pooling; for mosquitoes: large interommatidial angles, wide fused rhabdoms, strong adaptation changes
c) Large ocelli
d) Well-developed olfactory system
e) Well-developed ability to sense temperature differentials such as infrared detection
Reduced wind a) No reliance on wind pollination or on biotic agents that are wind-assisted in flight
b) Pollen donation is not profligate
c) Pollen likely to be sticky
d) Pollen receipt structures likely to be commensurate with more specialized donation
e) Adequate rewards to fuel nonwind-assisted flight of pollinators
a) Ability to fly without wind assistance: suitable wing loading, wing musculature, fuel reserves
Lower temperature
a) Flowers should not be open during conditions of frost or when temperatures are very low
b) If flowers are thermogenic, then heat can be a reward for pollinators under lower temperatures
a) Larger body size for adequate heat retention, heat generation under low temperatures
b) Thick chitinized cuticle for reduced temperature loss
c) Thicker pubescence (bees), scales (moths), or fur (mammals) for heat retention under low temperatures
d) Greater cold tolerance
e) Ability to sense temperature differentials using infrared (IR) detectors
f ) Moths and bees: ability to preheat flight muscles
Higher humidity
a) Flowers should not be open during rain
b) Flowers should be downfacing to prevent damage by water droplets or nectar dilution
a) Ability to cope with dew and/or rain
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sure that favor nocturnal pollination, e.g., in bromeliads (Graham and Andrade 2004). It would be interesting to examine the prob-ability of transitions between diurnal and nocturnal pollination and correlated evo-lution between functional traits such as water-holding capacity or type of photosyn-thesis at lower taxonomic levels. This is be cause, even within a family, transitions from nocturnal to diurnal pollination can occur (Rentsch and Leebens-Mack 2014). We need much more data on the match-ing of traits between plants and pollinators and their evolutionary trajectories. Addi-tionally, there appears to be a hemispheric
difference in cold tolerance in insects with many more insects adapted to the cold in the Southern Hemisphere as compared with the north (Sinclair and Chown 2005); it is possible that there may be more plants pollinated at night by insects in the south compared with the north. For example, New Zealand wetas and cockroaches show great cold tol erance (Wharton 2011) and pollinate plants at night.
Since the night may also feature greater humidity, flowers may also be downfacing to prevent nectar dilution by water drop-lets (Aizen 2003) or have structures that prevent pollen damage by rain (Mao and
Box 1Gaps in our knowledge and a sample of questions to be answered
and C4 photosynthesis already confers plants with protection against drought, why are there many examples of plants with nocturnal pollination in families with CAM and C4 photosynthesis?
-phological and physiological constraints or adaptations necessary for diurnal or nocturnal blooming?
closing times that match the activity periods of their pollinators based on differ-ences in the length of dawn and dusk periods and other abiotic factors character-istic of the night at these different geographical locations?
how do they compare with diurnal networks in the same habitat?
a single habitat; how does this availability change with seasonal variation in abun-dance and diversity of pollinators?
-tles, orthopterans, rodents, geckos, and primates?
taxa mentioned above?
these understudied groups of nocturnal pollinators?
plants compare?
the degree of specialization based on the taxon of pollinator and on the macro-habitat (geographical location) and microhabitat (understory versus canopy, for example)?
Do floral traits of such plant species differ from flowers that are strictly open only at night or in the day?
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Huang 2009). Whether these features also occur in flowers that open at night and ex-perience greater humidity in the form of dew (Berkelhammer et al. 2013) is not yet known. Flower orientation is another trait that needs greater investigation (Fenster et al. 2009). Many flowering species also have flowers that remain open for several days, and are open both during the day and the night; here pollination can also occur during the day and night (Valdivia and Niemeyer 2006), such that different pollinators may vary in pollination services. Pollinator services can differ even between nocturnal pollinators. For example, in the parasitic Balanophora, ants and cockroaches contribute to geitonogamy or movement of pollen within a single plant while pyralid moths contribute to outcrossing (Kawakita and Kato 2002). In the Nyctaginaceae, Aclei-santhes longiflora is cleistogamous (closed flowered) in summer when pollinating noc-turnal hawkmoths are rare; therefore, in this case, cleistogamy may be an adaptation to a seasonal lack of nocturnal pollinators (Douglas and Manos 2007).
In this paper, we have sketched broad pat-terns, and there are many gaps (Box 1). Just as there is no information on pollination for many plant families, and also for many plant
species within well-investigated families, there is a complete paucity of information on the physiological capacities of many taxa of potential nocturnal pollinators. These la-cunae become even more important given the rapid erosion of biological diversity since we would be unable to predict which plant–pollinator nodes are more vulnerable in a nocturnal plant–pollinator network.
We can only begin to understand noc-turnal pollination patterns and processes if there is collaboration between pollination biologists, sensory biologists, plant ecophys-iologists, and animal physiologists. This will enable us to make sense of the correlation pleiades within and between plant and pol-linator traits (sensu Berg 1960; Armbruster et al. 2014). There are good signs that this is happening, but there is a long way to go. We hope that this review will stimulate re-search in this very important area.
acknowledgments
This review emerged out of thinking about nocturnal pollination following our joint work along with Eric Warrant on a nocturnal carpenter bee that has color vision under starlight. We thank Rob Raguso for crit-ical comments on this manuscript, as well as Yuvaraj Ranganathan and Vignesh Venkateswaran for assis-tance with Figure 1 and the Bayesian analyses.
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