Despite myriad challenges, clinicians see room for progress.
Image credit: Shutterstock/David Tadevosian.
New Research In
Physical Sciences
Featured Portals
Articles by Topic
Biological Sciences
Featured Portals
Articles by Topic
Edited by James D. Thomson, University of Toronto, Toronto, Canada, and accepted by the Editorial Board February 10, 2015 (received for review October 10, 2014)
Significance
By using structural characteristics, such as long tubular flowers, plants are known to achieve selective visitation by certain pollinator species. These morphological traits typically arise over evolutionary timescales. We show for the first time, to our knowledge, that at least one plant has also evolved the capacity to recognize pollinator species immediately after visitation, thereby increasing the likelihood that a flower visitor has delivered high-quality pollen. This novel responsiveness by the plant leads to functional specialization in an apparently generalized tropical plant–pollinator network. Such specialized linkages likely facilitate coevolution but also, render pollination mutualisms more vulnerable to environmental change.
Abstract
Understanding the mechanisms enabling coevolution in complex mutualistic networks remains a central challenge in evolutionary biology. We show for the first time, to our knowledge, that a tropical plant species has the capacity to discriminate among floral visitors, investing in reproduction differentially across the pollinator community. After we standardized pollen quality in 223 aviary experiments, successful pollination of Heliconia tortuosa (measured as pollen tube abundance) occurred frequently when plants were visited by long-distance traplining hummingbird species with specialized bills (
The remarkable diversity of angiosperms has been, in part, attributed to the evolution of complex floral structures and the variety of strategies for sexual reproduction (1). The resulting increase in genetic mixing facilitates adaptation to changing environmental conditions, enhances morphological diversification, and leads eventually to speciation (2).
Much research has focused on the genetic benefits afforded by long-distance pollen transfer among individuals, particularly in animal-pollinated plants (3, 4). However, pollen dispersal kernels are often short, resulting in self-pollination or gene exchange among closely related individuals (5, 6). In response, plants have evolved floral traits and attractants that influence the degree of pollinator specialization (7) and act as filters against inefficient pollinator services (8) or enhance pollen transport (9). Coevolution occurs when evolution of pollinator morphology tracks these floral changes, which in turn, drives reciprocal changes in floral traits (10).
Although the potential for coevolution in the most specialized obligate mutualisms is clear (11), the processes by which coevolution occurs in more complex interaction networks remains a central question in evolutionary biology (10, 12). The striking fit (trait matching) between morphologies of some plants and their pollinators in many systems (7, 13) suggests a high degree of plant–pollinator specialization. Such matches between flowers and groups of pollinators are the basis of the identification of floral syndromes (or pollination web modules), which link floral traits with particular types of pollinators (e.g., bird-pollinated and bee-pollinated) (14, 15). However, observational data of pollination mutualisms indicate a high degree of generality, even within floral syndromes (16, 17); plant species may exhibit highly specialized morphological traits (e.g., long, curved corollas) but are visited by many pollinators, most of which lack specialized foraging morphologies (18, 19). The importance of coevolutionary processes in the presence of many pollinator species, each of which may impose conflicting selection pressures, remains much debated (20). This situation is exemplified by the species-rich guild of tropical hummingbirds that shows strikingly high among-species diversity in bill length, bill curvature, and spatial behavior (21); however, both specialized and generalized hummingbird species visit plants with apparently high morphological specialization (22). How can strong morphological coevolution occur if plants are visited by many pollinator species with high trait variation?
In this paper, we report a previously unidentified mechanism that increases the realized specialization between a plant and its suite of floral visitors. Through a series of experiments in a tropical plant–hummingbird system, we show that a keystone understory herb (23), Heliconia tortuosa Griggs, has the capacity to discriminate among floral visitors representing a wide range of morphologies within a functional group. Flowers of H. tortuosa recognize specialized pollinators that potentially carry high-quality pollen and are most likely to facilitate mate selection.
Results
Testing the Pollinator Recognition Hypothesis.
Our discovery of pollinator recognition was the direct result of original hand-pollination experiments designed to test the degree of pollen limitation in H. tortuosa in relation to landscape fragmentation (23). Pollen limitation was measured as the difference between hand pollination of covered flowers and those left unmanipulated with full exposure to pollinators (24). We measured pollination using the abundance of pollen tubes following methods by Kress (25). Surprisingly, hand-pollinated flowers averaged 5.04 times [95% confidence interval (95% CI) = 3.65–7.24] fewer pollen tubes per style than open-pollinated flowers [generalized linear model (GLM): t = 8.36, P < 0.0001; hand:
We hypothesized that such decreased plant reproduction after hand pollination could have two potential causes. The quality of pollen brought by hummingbirds could be higher (5), reflecting either longer distance or more genetically mixed pollen transfer by natural pollinators than in our hand-pollination experiments (the pollen-quality hypothesis). Alternatively, the plant might distinguish pollen quality indirectly based on a physical or chemical cue transmitted by the pollinator (the pollinator-recognition hypothesis). To distinguish these hypotheses, we designed an experiment in which we hand-pollinated flowers as before but introduced pollen-free clean hummingbird pollinators under controlled aviary conditions. Under the pollen-quality hypothesis, visitation by a pollen-free pollinator should not increase pollen tube abundance in flower styles. Under the pollinator-recognition hypothesis, visitation alone by hummingbirds—even in the absence of pollen on the bird—should increase the abundance of pollen tubes over pollinator-excluded controls.
To test these hypotheses, we captured 148 individual floral visitors representing six hummingbird species and one common species of butterfly—Anartia fatima. All species have been observed visiting flowers of H. tortuosa. After cleaning hummingbirds of all pollen (Materials and Methods), they were released individually into aviaries containing a single flower that we had hand pollinated with pollen from 30 to 100 m away. We released butterflies into mesh bags covering a hand-pollinated flower. Flower styles were collected the next day and inspected for pollen tubes using epifluorescence microscopy (25) (SI Materials and Methods).
Hummingbird flower visitation strongly influenced pollen tube abundance [generalized linear mixed model (GLMM): F = 4.57, P < 0.0001], supporting the pollinator-recognition hypothesis. However, this effect was mediated by specific species of hummingbirds (Table 1). For instance, flowers visited by violet sabrewings (Campylopterus hemileucurus) contained 3.10 times (95% CI = 2.33–6.17,
View this table:
Table 1.
Results of GLMM predicting differences in pollen tube abundance as a function of different hummingbird pollinator species released into aviaries with hand-pollinated H. tortuosa
Fig. 1.
Results of aviary experiments, where flowers were visited by pollen-free pollinators after being hand-pollinated under controlled conditions. (A) A bract of H. tortuosa with a male green hermit hummingbird. (B) Pollen tubes, the first step in reproduction, viewed in the style of H. tortuosa using epifluorescence microscopy. (C) Experimental addition of hummingbirds strongly influenced the abundance of pollen tubes, but this effect was species-dependent. Means and SEs are shown. P values for contrasts are reported in Table 1. Green represents those species stimulating pollen tube growth, and red indicates less-effective species. Butterfly, A. fatima; GCBR, green-crowned brilliant; GREH, green hermit (Phaethornis guy); RTAH, rufous-tailed hummingbird; SBRH, scaly-breasted hummingbird; STHR, stripe-throated hermit (Phaethornis striigularis); VISA, violet sabrewing.
Testing the Mechanism Used in Pollinator Recognition.
Next, we tested for the cue used by plants to distinguish among pollinators. Species of tropical hummingbirds differ strongly in their capacity to extract nectar from ornithophilous plants (29), and these differences correspond to the degree of specialization in hummingbird bill morphology (7, 29). The capacity to distinguish visitors that carry high-quality pollen loads from those that do not should be adaptive (5, 30). Morphological specialists are more likely to be faithful to a particular flower species (27), reducing the risk of mixed-species pollen loads. Specialization should also require greater movement distances among plants to acquire necessary resources (30), thereby increasing the potential for gene flow. We, therefore, hypothesized that capacity for nectar extraction is the mechanism used by H. tortuosa to recognize the identity of morphologically specialized floral visitors.
Three lines of evidence support this hypothesis. First, similar to the work by Wolf et al. (29), we found strong differences among pollinator species in their capacity to extract nectar (GLM: F = 81.30, R2 = 0.75, P < 0.0001) (Fig. 2A and Table S1). Bill length directly reflected nectar extraction capacity of pollinators (r = 0.85, P = 0.008). Second, the nectar extraction capacity of each species was correlated with mean pollen tube abundance in experimentally pollinated flowers (Fig. 2B) (r = 0.73, P = 0.039). The outlier in this analysis was the scaly-breasted hummingbird (Phaeochroa cuvierii) (Fig. 2 A and B), which in our aviary experiments, we have only observed robbing nectar by piercing flower bases. Despite the fact that this species removed high nectar amounts, the damage that it inflicts on the flower apparently reduces pollen tube growth. Removing this species from analysis resulted in a stronger correlation between pollinator nectar extraction capacity and mean pollen tube abundance (r = 0.83, P = 0.020). Third, experimental extraction of nectar significantly increased the abundance of pollen tubes in hand-pollinated flowers (GLMM: Z = 2.53, P = 0.011) (SI Materials and Methods). Pollen tubes were 3.67 times (95% CI = 1.38–9.74) more common when we extracted nectar than when flowers were hand-pollinated without nectar extraction (Fig. 2C) (GLMM: Z = 2.67, P = 0.008).
Fig. 2.
(A) Boxplot showing how nectar extraction efficiency in H. tortuosa varies across pollinator species. Boxes show first and third quartiles of data. The bill shapes/sizes of the species are to scale in relative terms. Green represents successful pollen tube growth, and red represents limited growth. (B) Relationship between nectar remaining after pollinator visitation and the number of pollen tubes per style for each species (species abbreviations are the same as in Fig. 1). Nectar extraction capacity of hummingbirds strongly influenced the abundance of pollen tubes (r = −0.73). (C) Effect of hand pollination only vs. hand pollination combined with nectar extraction on pollen tube abundance. Pollen tubes were 3.5 times more common when nectar was experimentally extracted than when flowers were hand-pollinated only. Error bars in B and C are ± SE.
Discussion
To our knowledge, these findings provide the first evidence of pollinator recognition in plants. H. tortuosa is capable of discerning morphologically specialized hummingbird species from those with generalized traits. Elegantly, the traits themselves (i.e., long, curved bills) enable some hummingbird species to extract more nectar, which in turn, is the very cue used by the plant to become receptive. This plant behavior raises the question of whether pollinator recognition confers any contemporary adaptive advantages to the plant. The fact that it is the specialized, traplining species that tend to induce pollen tube growth suggests that pollinator recognition may increase the quality of pollen receipt, thereby enhancing fitness. This advantage could occur through three possible mechanisms. First, this plant behavior could facilitate long-distance gene transfer or at least, reduce the frequency of self-pollination. H. tortuosa is a clonal herb, with plants often occurring in clumps of >10 individuals (25, 31). This high concentration of nectar resources often results in defense of a single clonal clump by territorial hummingbirds, which strongly constrains pollen flow (28). However, the large body size and specialized morphology of traplining hummingbirds require them to move further to acquire necessary resources (21), thus potentially facilitating gene flow and enhancing plant fitness (32). To test this hypothesis, we assembled movement data on all seven pollinator species (SI Materials and Methods). Pollen tube abundance was positively correlated with the median movement distance that each species moved within 1 d (Fig. 3A) (F = 48.98, R2 = 0.87, P = 0.0004). We also found a strong effect of movement behavioral strategy on the number of pollen tubes; traplining species, which regularly move long distances across landscapes to acquire nectar resources (32, 33), elicited greater pollen tube abundance than territorial species (6) (Fig. 3B) (GLMM: Z = 4.52, P < 0.0001).
Fig. 3.
(A) Relationship between median daily distance moved by pollinators and pollen tube abundance (± SE; R2 = 0.87). Species moving longer distances stimulated significantly more pollen tubes than those tending to make short-distance movements. (B) Individual flowers experimentally exposed to traplining species (GREH, VISA, and STHR) grew significantly more pollen tubes than ones visited by territorial species (GCBR, RTAH, and SBRH). Species abbreviations are the same as in Fig. 1.
Second, the capacity to recognize specialized pollinators could also function to maximize the diversity of conspecific pollen received. Because of the placement of the anthers in H. tortuosa and the foraging position of green hermit and violet sabrewing (Movie S1), these species are more likely, on average, to carry high pollen loads than nonspecialized species. Our data on hummingbird pollen loads support this hypothesis; traplining species carried significantly higher individual loads of H. tortuosa pollen (
Third, recognition of morphologically specialized pollinators might reduce the risk of pollen allelopathy or other types of pollen interference, whereby nonspecific pollen is deposited on the stigma by generalist pollinators and interferes with pollen receipt (35). In our study, both trapliners and territorial hummingbird species carried substantial non-Heliconia pollen, and we found no statistical differences between these groups (GLM: t = 1.55, P = 0.121). However, on average, trapliners carried lower loads of non-Heliconia pollen grains (
Together, our results suggest that pollinator recognition by H. tortuosa facilitates mate selection and is most likely to do so by (i) increased outcrossing caused by receipt of longer-distance nonself-pollen or (ii) enhanced conspecific pollen diversity.
Species in the genus Heliconia lack two mechanisms that promote outcrossing in many flowering plants, namely physiological self-incompatibility and spatial/temporal separation of sexual function (25). However, the often long and highly curved flowers of Heliconia species, including H. tortuosa, are a striking floral mechanism to screen out certain visitors. In many bird-pollinated plant species, flower length has been proposed as an adaptation to allow plants to exclude pollinators that are unlikely to be carrying high-quality pollen (29). In H. tortuosa, the long, curved perianth reduces but does not preclude visitation by territorial hummingbirds, which still receive some nectar rewards (29). Repeated deposition of pollen by such locally foraging species of hummingbirds would clearly increase the levels of inbreeding in the plants as well as cause a reduction in the diversity and abundance of conspecific pollen. Because of the energetic costs of fruit and seed development (36), a mechanism that enables a plant to distinguish low- from high-quality pollinators before investing in seed production would confer a considerable adaptive advantage.
Plant recognition of pollinators may occur in other plant taxa, particularly in relatively stable tropical systems with high pollinator diversity. One hypothesis is that the fitness gains afforded by pollinator recognition in terms of increasing mutualist specialization and possibly, outcrossing rates may have provided an initial mechanism for corolla lengthening in other plant families. Minor microevolutionary increases in corolla length should carry no fitness benefits until they accumulate sufficiently to induce switches by poor-quality pollinators to alternative flower species (30). However, if plants use minor differences in nectar extraction as a cue to indicate visitation by a high-quality pollinator, corolla lengthening in tandem with pollinator recognition would have immediate benefits. An alternative hypothesis is that pollinator recognition may have evolved to more effectively prevent pollination by poor pollinators in plants that have already evolved long corollas. Regardless of the initial evolutionary mechanism, candidates to examine for such pollinator recognition are those with long corollas combined with high nectar rewards (e.g., Acanthaceae, Rubiaceae, and Malvaceae) that would result in strong pollinator motivation and a subsequent reduction in morphological filters.
Research over the past decade has emphasized the importance of understanding plant–pollinator interactions as networks of species rather than tight, parallel specializations (16). Such networks are highly nested, which means that the most specialized plant species are visited by generalist pollinators and vice versa. This structure has been hypothesized to buffer networks against loss of individual species (37). Our results indicate that, in this tropical system, plant–pollinator relationships are more specialized than assumed given the observational data used to quantify most pollination networks (16). Although we have frequently observed all six species of hummingbirds carrying pollen and visiting the flowers of H. tortuosa (Fig. 4A), pollination and successful fertilization are dominated locally by only two traplining species (i.e., violet sabrewing and green hermit). Indeed, when we compensated for this functional pollination effect, 80.1% of the reproductive contribution to Heliconia was provided by only two species (Fig. 4B); the contribution of all other species combined dropped from 53.7% to 19.9%. This hidden specialization has two important implications. First, pollination and subsequent plant demography could be more vulnerable to population declines or disruptions to movement of specialized pollinator species than would be expected given observations of floral visitors. Indeed, our previous work indicates that interpatch movement of traplining species is disrupted by tropical forest fragmentation (33, 38), with consequent negative impacts on seed set (23). Second, plant–pollinator mutualisms in this system may not be as generalized as superficially apparent, which may result in greater potential for rapid reciprocal selection and therefore, coevolutionary change in H. tortuosa and a few key specialized pollinators.
Fig. 4.
Pollination network showing interactions between the six hummingbird pollinators that we examined (top row of black squares) and plants (bottom row of black squares). Width of connections represents strength of interactions. (A) Pollen-load data collected from the bills, nares, and heads of individual hummingbirds show that H. tortuosa seems to be a pollinator generalist, with contributions to its reproduction spread across all six hummingbird species. However, after taking the differential rates of plant investment after pollinator recognition into account (B), violet sabrewings and green hermits are likely responsible for 80% of successful reproduction. Pollinator recognition, therefore, promotes high levels of functional specialization within this complex network. GCBR, green-crowned brilliant (H. jacula); GREH, green hermit (Phaethornis guy); RTAH, rufous-tailed hummingbird; SBHU, scaly-breasted hummingbird; STHE stripe-throated hummingbird; VISA, violet sabrewing.
It is now well-known that the high cognitive capacity of many vertebrate pollinators allows them to recognize and specialize on particular flower species (30). However, a growing body of research indicates that plants may also exhibit complex decision-making behavior (39, 40). Here, we show for the first time, to our knowledge, that a plant has evolved an effective behavior that allows the recognition of specific hummingbird pollinators and thereby, regulates reproduction accordingly.
Materials and Methods
We conducted the study in the landscape surrounding the Organization for Tropical Studies Las Cruces Biological Station in southern Costa Rica (8° 47' 7'' N, 82° 57' 32'' W).
Hand-Pollination Experiments.
To conduct our initial test of pollen limitation in H. tortuosa, we randomly attributed hand-pollination treatments to 159 flowers during the dry season (January to March) from 2011 to 2014. H. tortuosa flowers open for only a single day before abscising. Treatments constituted covering all inflorescences with fine-mesh bags the night before pollination. We then collected pollen from conspecific flowers 30–100 m away (to ensure no self-fertilization) and applied it immediately (41) to flower stigmas using a toothpick. Stigmas were cleaned of self-pollen using a cotton swab before pollination. All flowers were then rebagged, and styles were collected the next day. We compared treated flowers with 746 flowers that were allowed full pollinator access and collected from the same study area and time period. We applied a similar or greater amount to what we typically observe on captured green hermits and violet sabrewings. To test whether under- or overabundance of pollen during hand supplementations negatively affected pollen tube growth, we conducted an additional experiment, in which we hand-pollinated flowers using the methods above but left them open to pollinators. Our pollinator-accessible hand pollinations (n = 24,
Aviary Experiment.
We captured 128 individual hummingbirds representing six species using a combination of 12-m nets and hall traps (23, 33). Individuals were fitted with unique aluminum bands to allow identification of recaptures and hence, nonindependent samples. We randomly assigned birds to individual flowers within aviaries and randomly assigned treatment to flowers. In this experiment, treatments comprised (i) hand-pollinated flowers with pollen outcrossed from a conspecific flower collected from within 30–100 m and with pollinators excluded (n = 92) and (ii) hand-pollinated flowers using the same methods but with bird visitation (n = 202). To minimize the risk of pollen degradation (41), pollen was applied immediately after removal from pollen donors. Again, we cleaned stigmas with a cotton swab before pollination; although this process could have negatively affected reproduction, it does not constitute a bias, because it was conducted in all treatments. Floral emasculation is conducted in many hand-pollination studies to remove a potential confounding effect of self-pollen (42). However, in H. tortuosa, emasculation alters the positioning of the style and damages the flower, and both of which could result in estimates of reproductive success that are biased. Finally, floral emasculation risks altering pollinator behavior (42, 43).
In bird visitation treatments, we took extreme care to ensure that birds were completely clean of pollen (SI Materials and Methods). We removed pollen using fuchsin jelly (for later use in pollen samples), a photographer’s brush (Fig. S1), and disposable lens-cleaning cloths. Bills, nares, heads, and throats were inspected with a hand lens after cleaning to ensure that no pollen grains remained. Birds were then released into the aviary and permitted to visit experimental flowers (Movie S1). Only one specific treatment flower was available to each bird within an experiment. We used three portable aviaries, each of which was assembled to cover individual plants. Aviaries were 2 × 2 × 3 m and covered in shade cloth mesh. Birds typically visited flowers in <30 min, and if they had not visited within 1 h, we fed and released them. Birds were permitted to visit individual flowers more than one time (number of visits:
In total, we conducted 223 aviary experiments comprising the following treatments/species: green hermits (n = 105), violet sabrewing (n = 39), rufous-tailed hummingbird (n = 24), green-crowned brilliant (n = 16), stripe-throated hermit (n = 12), scaly-breasted hummingbird (n = 6), and A. fatima (n = 21) (SI Materials and Methods and Fig. S2). All aviary experiments were approved under Oregon State University Animal Care and Use Protocol 4266.
Pollinator Nectar Consumption Observations.
We measured nectar consumption by hummingbirds and butterflies by observing pollinator visitation to previously excluded flowers and then, measuring the nectar remaining after a single visit. We measured the volume of nectar using 70-μL capillary tubes and tested sugar content using a refractometer.
Pollination Network Data.
We collected and identified 417 individual pollen samples for six species of hummingbirds from across 14 study sites surrounding Las Cruces Biological Station and preserved them in semipermanent slides of glycerin jelly (43). We then calculated a quantitative web using the number of times that each plant–pollinator interaction was detected normalized by the number of captures of each species (44) (SI Materials and Methods). To quantify the influence of pollinator recognition on web structure, we constructed a second web that accounted for the fitness contribution of each pollinator species by multiplying the proportion of pollen tubes per style for each species by the initial quantitative pollen web (Fig. 4B). Finally, to test the hypotheses that trapliners carry more Heliconia pollen and less heterospecific pollen than territorial species, we summed the number of Heliconia and non-Heliconia pollen grains for each individual bird and tested for statistical differences between these functional groups.
Statistical Methods.
Pollen tube abundance data were Poisson-distributed, so we used generalized nonlinear mixed models [in the lme4 R package (45)] to test for differences in tube abundance as a function of pollinator species. We tested for the effects of pollen source (self-pollen vs. outcrossed) by including this term as a covariate in the model (Table 1). To account for lack of statistical independence caused by individual birds and plants being used for multiple trials, we specified individual bird and individual plant as partially crossed random effects. To limit the number of tests, we conducted pairwise comparisons with only two species: green-crowned brilliant and rufous-tailed hummingbird. We expected the green-crowned brilliant to be intermediate in pollination effectiveness because of its body size and bill length. Alternatively, we expected the rufous-tailed hummingbird to be the poorest of the hummingbird species because of its short bill length. This approach still resulted in a total of nine comparisons, which increases the risk of type I error. Sequential Bonferroni-type multiple comparisons are often used to account for such error inflation, but they are highly conservative (46). Therefore, we used a false discovery rate procedure (the graphically sharpened method) (46), which does not suffer from the same loss of power but corrects for multiple comparisons.
Models assuming a Poisson distribution sometimes suffer from lack of fit because of inflated zeros, sparse very high counts, or lack of independence among study subjects (47). We tested for model overdispersion (
We tested for differences in nectar consumption capacity across species using GLMs with a Gaussian distribution. Green hermit males and females were included separately in analysis of nectar extraction, because they show strong sexual dimorphism in bill length, which is likely to influence nectar extraction efficiency (50). Sexes of this species have different movement behavior, with male home ranges larger than female home ranges (33). We tested assumptions of regressions by inspecting regression residuals for normality against a q-q plot.
We tested the effect of experimental nectar extraction on pollen tube abundance using GLMMs with a Poisson distribution. The individual plant was specified as a random effect to account for occasional repeat sampling of the same plant. These data were analyzed two ways. First, we predicted pollen tube abundance as a function of the amount of nectar removed. Second, we tested the effect of nectar extraction treatments vs. hand pollination-only treatments.
Finally, we tested whether territorial species carried more non-Heliconia pollen than traplining species using GLMs with a Gaussian distribution. Data were log(x + 1)-transformed to meet model assumptions. We used the same modeling approach to test whether traplining species carried more Heliconia pollen than trapliners.
Acknowledgments
C. Argo, A. C. Betts, A. M. Betts, and M. Betts, C. Birkett, K. DeWolfe, C. Dourhard, S. Frey, J. Greer, A. Jack, T. McFadden, K. O'Connell, M. Paniagua, and E. Sandi assisted with data collection. E. Jackson and N. Volpe provided a portion of the hummingbird movement data. We thank M. Harmon, D. Hibbs, F. Jones, U. Kormann, A. Moldenke, and L. Reid for comments on the manuscript and A. Muldoon for statistical advice. The manuscript benefitted from comments from J. Thomson, N. Waser, and an anonymous reviewer. We thank the staff of Las Cruces Biological Station for facilitating collection of field data. This work was funded by National Science Foundation Grants DEB-1050954 (to M.G.B. and W.J.K.) and DEB-1457837 (to M.G.B., A.S.H., and W.J.K.).
Footnotes
- ↵1To whom correspondence should be addressed. Email: matt.betts{at}oregonstate.edu.
Author contributions: M.G.B. and A.S.H. designed research; M.G.B., A.S.H., and W.J.K. performed research; M.G.B. and A.S.H. contributed new reagents/analytic tools; M.G.B. analyzed data; and M.G.B., A.S.H., and W.J.K. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. J.D.T. is a guest editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1419522112/-/DCSupplemental.
Freely available online through the PNAS open access option.
References
Pollinator recognition
Sign up for Article Alerts
Article Classifications
- Biological Sciences
- Ecology
Jump to section
You May Also be Interested in
Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Using CRISPR, researchers showed that a region some used to label “junk DNA” has a major role in a rare genetic disorder.
Image credit: Nathan Devery.
Mara Reed and Michael Manga explore why Yellowstone's Steamboat Geyser resumed erupting in 2018.
Some songbird parents might improve their own fitness by manipulating their offspring into leaving the nest early, at the cost of fledgling survival, a study finds.
Image credit: Gil Eckrich (photographer).