Why do avian responses to change in Arctic green-up vary?

Global climate change has altered the timing of seasonal events (i.e., phenology) for a diverse range of biota. Within and among species, however, the degree to which alterations in phenology match climate variability differ substantially. To better understand factors driving these differences, we evaluated variation in timing of nesting of eight Arctic-breeding shorebird species at 18 sites over a 23-year period. We used the Normalized Difference Vegetation Index as a proxy to determine the start of spring (SOS) growing season and quantified relationships between SOS and nest initiation dates as a measure of phenological responsiveness. Among species, we tested four life history traits (migration distance, seasonal timing of breeding, female body mass, expected female reproductive effort) as species-level predictors of responsiveness. For one species (Semipalmated Sandpiper), we also evaluated whether responsiveness varied across sites. Although no species in our study completely tracked annual variation in SOS, phenological responses were strongest for Western Sandpipers, Pectoral Sandpipers, and Red Phalaropes. Migration distance was the strongest additional predictor of responsiveness, with longer-distance migrant species generally tracking variation in SOS more closely than species that migrate shorter distances. Semipalmated Sandpipers are a widely distributed species, but adjustments in timing of nesting relative to variability in SOS did not vary across sites, suggesting that different breeding populations of this species were equally responsive to climate cues despite differing migration strategies. Our results unexpectedly show that long-distance migrants are more sensitive to local environmental conditions, which may help them to adapt to ongoing changes in climate.

A circumpolar study unveils a positive non-linear effect of temperature on arctic arthropod availability that may reduce the risk of warming-induced trophic mismatch for breeding shorebirds.

Seasonally abundant arthropods are a crucial food source for many migratory birds that breed in the Arctic. In cold environments, the growth and emergence of arthropods are particularly tied to temperature. Thus, the phenology of arthropods is anticipated to undergo a rapid change in response to a warming climate, potentially leading to a trophic mismatch between migratory insectivorous birds and their prey. Using data from 19 sites spanning a wide temperature gradient from the Subarctic to the High Arctic, we investigated the effects of temperature on the phenology and biomass of arthropods available to shorebirds during their short breeding season at high latitudes. We hypothesized that prolonged exposure to warmer summer temperatures would generate earlier peaks in arthropod biomass, as well as higher peak and seasonal biomass. Across the temperature gradient encompassed by our study sites (>10°C in average summer temperatures), we found a 3-day shift in average peak date for every increment of 80 cumulative thawing degree-days. Interestingly, we found a linear relationship between temperature and arthropod biomass only below temperature thresholds. Higher temperatures were associated with higher peak and seasonal biomass below 106 and 177 cumulative thawing degree-days, respectively, between June 5 and July 15. Beyond these thresholds, no relationship was observed between temperature and arthropod biomass. Our results suggest that prolonged exposure to elevated temperatures can positively influence prey availability for some arctic birds. This positive effect could, in part, stem from changes in arthropod assemblages and may reduce the risk of trophic mismatch.

Unexpected diversity in socially synchronized rhythms of shorebirds.

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parent's incubation bout varied from 1-19 h, whereas period length-the time in which a parent's probability to incubate cycles once between its highest and lowest value-varied from 6-43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light-dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

Drought at a coastal wetland affects refuelling and migration strategies of shorebirds.

Droughts can affect invertebrate communities in wetlands, which can have bottom-up effects on the condition and survival of top predators. Shorebirds, key predators at coastal wetlands, have experienced widespread population declines and could be negatively affected by droughts. We explored, in detail, the effects of drought on multiple aspects of shorebird stopover and migration ecology by contrasting a year with average wet/dry conditions (2016) with a year with moderate drought (2017) at a major subarctic stopover site on southbound migration. We also examined the effects of drought on shorebird body mass during stopover across 14 years (historical: 1974-1982 and present-day: 2014-2018). For the detailed comparison of two years, in the year with moderate drought we documented lower invertebrate abundance at some sites, higher prey family richness in shorebird faecal samples, lower shorebird refuelling rates, shorter stopover durations for juveniles, and, for most species, a higher probability of making a subsequent stopover in North America after departing the subarctic, compared to the year with average wet/dry conditions. In the 14-year dataset, shorebird body mass tended to be lower in drier years. We show that even short-term, moderate drought conditions can negatively affect shorebird refuelling performance at coastal wetlands, which may carry-over to affect subsequent stopover decisions. Given shorebird population declines and predicted changes in the severity and duration of droughts with climate change, researchers should prioritize a better understanding of how droughts affect shorebird refuelling performance and survival.

Human Activity and Habitat Characteristics Influence Shorebird Habitat Use and Behavior at a Vancouver Island Migratory Stopover Site.

Pacific Rim National Park Reserve on Vancouver Island, British Columbia, Canada, has 16 km of coastal beaches that attract many thousands of people and shorebirds (S.O. Charadrii) every year. To identify locations where shorebirds concentrate and to determine the impact of human activity and habitat characteristics on shorebirds, we conducted shorebird and visitor surveys at 20 beach sectors (across 20 total km of beach) during fall migration in 2011-2014 and spring migration in 2012 and 2013. Using zero-inflated negative binomial regression and a model selection approach, we found that beach width and number of people influenced shorebird use of beach sectors (Bayesian information criterion weight of top model = 0.69). Shorebird absence from beaches was associated with increasing number of people (parameter estimate from top model: 0.38; 95 % CI 0.19, 0.57) and decreasing beach width (parameter estimate: -0.32; 95 % CI -0.47, -0.17). Shorebirds spent more time at wider beaches (parameter estimate: 0.68; 95 % CI 0.49, 0.87). Close proximity to people increased the proportion of time shorebirds spent moving, while shorebirds spent more time moving and less time foraging on wider beaches than on narrower ones. Shorebird disturbance increased with proximity of people, activity speed, and presence of dogs. Based on our findings, management options, for reducing shorebird disturbance at Pacific Rim National Park Reserve and similar shorebird stopover areas, include mandatory buffer distances between people and shorebirds, restrictions on fast-moving activities (e.g., running, biking), prohibiting dogs, and seasonal closures of wide beach sections.

Adult Ovenbirds (Seiurus aurocapilla) show increased stress-responsiveness in logged forests.

Forest harvesting is a form of anthropogenic disturbance, yet the effects of such disturbance on the endocrine physiology of wildlife have been infrequently studied. We investigated the effect of two methods of forest harvesting ('intensive' and 'typical' group-selection silviculture) and un-harvested control sites on the glucocorticoid levels of adult Ovenbirds (Seiurus aurocapilla), a forest interior bird species. We collected blood samples from adult males immediately after capture to examine baseline corticosterone, and then following a standardized capture and restraint protocol, to examine stress-induced levels. There was no significant repeatability in either baseline or stress-induced corticosterone levels for eleven individuals measured in both years of study. Despite no differences across harvesting treatments in male body mass or baseline corticosterone levels, males captured in sites subjected to intensive harvesting had significantly higher stress-induced corticosterone levels than males in other treatments. Currently, the mechanism driving differences in stress-reactivity is unknown although we hypothesize that the size of gaps resulting from intensive group-selection silviculture may increase perceived predation risk. In comparison to our previous work on nestling Ovenbirds, adults respond differently to stress from group-selection silviculture.

Habitat alteration and fecal deposition by geese alter tundra invertebrate communities: Implications for diets of sympatric birds.

Over the last 60 years, Arctic goose populations have increased while many sympatric tundra nesting bird populations have declined. Hyperabundant geese have well-documented effects on tundra habitats, which can alter habitat use by sympatric bird species. These habitat changes may also alter invertebrate communities and abundances, with potentially important, but as of yet, undocumented effects on insectivorous birds such as shorebirds. Here, we determined the effects of goose-induced habitat alteration on invertebrate communities and relate the observed changes to shorebird diet. At sites and habitat types representing a gradient of goose influence, we identified goose-related changes in ground cover and linked these factors to variation in invertebrate communities. We then used DNA metabarcoding to characterize the diet of six shorebird species across sites and identify inter-site variation in abundance, biomass, and timing of emergence of dominant shorebird prey items. Invertebrate diversity and richness did not vary either among sites or habitat types. However, for prey items identified as part of the shorebird diet, we found significantly higher abundances and biomasses at a moderately goose-influenced site than at either low or high goose-influenced sites. Biomass of Tipulidae, the dominant prey taxon for shorebirds at the study sites, was 7.5 times higher at the moderately goose-influenced site compared to the site where goose influence was minor. We attribute this enhancement of prey biomass to both the fertilizing effect of goose fecal pellets and the moderate grazing pressure. Many studies have documented adverse effects of overabundant geese, but here we show that a moderate degree of goose grazing can lead to enhanced biomass of invertebrates, with the potential for improved shorebird foraging success and chick growth. These benefits, however, might be outweighed by negative effects of goose-induced habitat alteration and predation pressure.

Flyway-scale GPS tracking reveals migratory routes and key stopover and non-breeding locations of lesser yellowlegs.

Many populations of long-distance migrant shorebirds are declining rapidly. Since the 1970s, the lesser yellowlegs (Tringa flavipes) has experienced a pronounced reduction in abundance of ~63%. The potential causes of the species' decline are complex and interrelated. Understanding the timing of migration, seasonal routes, and important stopover and non-breeding locations used by this species will aid in directing conservation planning to address potential threats. During 2018-2022, we tracked 118 adult lesser yellowlegs using GPS satellite tags deployed on birds from five breeding and two migratory stopover locations spanning the boreal forest of North America from Alaska to Eastern Canada. Our objectives were to identify migratory routes, quantify migratory connectivity, and describe key stopover and non-breeding locations. We also evaluated predictors of southbound migratory departure date and migration distance. Individuals tagged in Alaska and Central Canada followed similar southbound migratory routes, stopping to refuel in the Prairie Pothole Region of North America, whereas birds tagged in Eastern Canada completed multi-day transoceanic flights covering distances of >4000 km across the Atlantic between North and South America. Upon reaching their non-breeding locations, lesser yellowlegs populations overlapped, resulting in weak migratory connectivity. Sex and population origin were significantly associated with the timing of migratory departure from breeding locations, and body mass at the time of GPS-tag deployment was the best predictor of southbound migratory distance. Our findings suggest that lesser yellowlegs travel long distances and traverse numerous political boundaries each year, and breeding location likely has the greatest influence on migratory routes and therefore the threats birds experience during migration. Further, the species' dependence on wetlands in agricultural landscapes during migration and the non-breeding period may make them vulnerable to threats related to agricultural practices, such as pesticide exposure.

Conserving migratory land birds in the new world: do we know enough?

Migratory bird needs must be met during four phases of the year: breeding season, fall migration, wintering, and spring migration; thus, management may be needed during all four phases. The bulk of research and management has focused on the breeding season, although several issues remain unsettled, including the spatial extent of habitat influences on fitness and the importance of habitat on the breeding grounds used after breeding. Although detailed investigations have shed light on the ecology and population dynamics of a few avian species, knowledge is sketchy for most species. Replication of comprehensive studies is needed for multiple species across a range of areas, Information deficiencies are even greater during the wintering season, when birds require sites that provide security and food resources needed for survival and developing nutrient reserves for spring migration and, possibly, reproduction. Research is needed on many species simply to identify geographic distributions, wintering sites, habitat use, and basic ecology. Studies are complicated, however, by the mobility of birds and by sexual segregation during winter. Stable-isotope methodology has offered an opportunity to identify linkages between breeding and wintering sites, which facilitates understanding the complete annual cycle of birds. The twice-annual migrations are the poorest-understood events in a bird's life. Migration has always been a risky undertaking, with such anthropogenic features as tall buildings, towers, and wind generators adding to the risk. Species such as woodland specialists migrating through eastern North America have numerous options for pausing during migration to replenish nutrients, but some species depend on limited stopover locations. Research needs for migration include identifying pathways and timetables of migration, quality and distribution of habitats, threats posed by towers and other tall structures, and any bottlenecks for migration. Issues such as human population growth, acid deposition, climate change, and exotic diseases are global concerns with uncertain consequences to migratory birds and even less-certain remedies. Despite enormous gaps in our understanding of these birds, research, much of it occurring in the past 30 years, has provided sufficient information to make intelligent conservation efforts but needs to expand to handle future challenges.

Consistent declines in wing lengths of Calidridine sandpipers suggest a rapid morphometric response to environmental change.

A recent study demonstrated that semipalmated sandpiper (Calidris pusilla) wing lengths have shortened from the 1980s to the present-day. We examined alternative and untested hypotheses for this change at an important stopover site, James Bay, Ontario, Canada. We evaluated morphometric patterns in wing length and bill length by age and sex, when possible, and assessed if wing shape has also changed during this time-period. We investigated patterns of morphological change in two additional Calidridine sandpipers, white-rumped sandpipers (Calidris fuscicollis) and least sandpipers (Calidris minutilla), to determine if shorter wing lengths are a widespread pattern in small sandpipers. We also examined allometric changes in wing and bill lengths to clarify if wing length declines were consistent with historical scaling relationships and indicative of a change in body size instead of only wing length change. We found that including sex and wing shape in analyses revealed important patterns in morphometric change for semipalmated sandpipers. Wing lengths declined for both sexes, but the magnitude of decline was smaller and not significant for males. Additionally, semipalmated sandpiper wings have become more convex, a shape that increases maneuverability in flight. Wing lengths, but not bill lengths, declined for most species and age classes, a pattern that was inconsistent with historical allometric scaling relationships. For juvenile semipalmated sandpipers, however, both bill and wing lengths declined according to historical scaling relationships, which could be a consequence of nutritional stress during development or a shift in the proportion of birds from smaller-sized, western breeding populations. Except for juvenile semipalmated sandpipers, we did not find evidence for an increase in the proportion of birds from different breeding populations at the stopover site. Given the wide, hemispheric distribution of these sandpipers throughout their annual cycles, our results, paired with those from a previous study, provide evidence for wide-spread reduction in wing lengths of Calidridine sandpipers since the 1980s. The shorter wing lengths and more convex wing shapes found in this study support the hypothesis that selection has favored more maneuverable wing morphology in small sandpipers.

Spatio-temporal responses of predators to hyperabundant geese affect risk of predation for sympatric-nesting species.

The Arctic is undergoing rapid changes, with anthropogenic shifts in climate having important and well-documented impacts on habitat. Populations of predators and their prey are affected by changing climate and other anthropogenic factors, and these changing trophic interactions could have profound effects on breeding populations of Arctic birds. Variable abundance of lemmings (a primary prey of generalist Arctic predators) and increasing abundance of light geese (Lesser Snow and Ross' Geese; a secondary prey) could have negative consequences for numerous sympatric shorebirds (an incidental prey). Using 16 years of predator-prey observations and 13-years of shorebird nest survival data at a site near a goose colony we identify relationships among geese, lemmings, and their shared predators and then relate predator indices to shorebird risk of nest predation. During two years, we also placed time-lapse cameras and artificial shorebird nests at increasing distances from a goose colony to document spatial trends in predators and their effect on risk of predation. In the long-term data, yearly indices of light geese positively influenced indices of gulls and jaegers, and shorebird nest predation rate was negatively correlated with jaeger and fox indices. All three predator indices were highest near the goose colony and artificial nest predation probability was negatively correlated with distance from goose colony, but these effects were less apparent during the second year. Combined, these results highlight the variation in predator-mediated interactions between geese and shorebirds and outline one mechanism by which hyperabundant geese may be contributing to local or regional declines in Arctic-nesting shorebird populations.

Long-distance migratory shorebirds travel faster towards their breeding grounds, but fly faster post-breeding.

Long-distance migrants are assumed to be more time-limited during the pre-breeding season compared to the post-breeding season. Although breeding-related time constraints may be absent post-breeding, additional factors such as predation risk could lead to time constraints that were previously underestimated. By using an automated radio telemetry system, we compared pre- and post-breeding movements of long-distance migrant shorebirds on a continent-wide scale. From 2014 to 2016, we deployed radio transmitters on 1,937 individuals of 4 shorebird species at 13 sites distributed across North America. Following theoretical predictions, all species migrated faster during the pre-breeding season, compared to the post-breeding season. These differences in migration speed between seasons were attributable primarily to longer stopover durations in the post-breeding season. In contrast, and counter to our expectations, all species had higher airspeeds during the post-breeding season, even after accounting for seasonal differences in wind. Arriving at the breeding grounds in good body condition is beneficial for survival and reproductive success and this energetic constraint might explain why airspeeds are not maximised in the pre-breeding season. We show that the higher airspeeds in the post-breeding season precede a wave of avian predators, which could suggest that migrant shorebirds show predation-minimizing behaviour during the post-breeding season. Our results reaffirm the important role of time constraints during northward migration and suggest that both energy and predation-risk constrain migratory behaviour during the post-breeding season.

Comment on "Global pattern of nest predation is disrupted by climate change in shorebirds".

Kubelka et al (Reports, 9 November 2018, p. 680) claim that climate change has disrupted patterns of nest predation in shorebirds. They report that predation rates have increased since the 1950s, especially in the Arctic. We describe methodological problems with their analyses and argue that there is no solid statistical support for their claims.

Effects of geolocators on hatching success, return rates, breeding movements, and change in body mass in 16 species of Arctic-breeding shorebirds.

BACKGROUND: Geolocators are useful for tracking movements of long-distance migrants, but potential negative effects on birds have not been well studied. We tested for effects of geolocators (0.8-2.0 g total, representing 0.1-3.9 % of mean body mass) on 16 species of migratory shorebirds, including five species with 2-4 subspecies each for a total of 23 study taxa. Study species spanned a range of body sizes (26-1091 g) and eight genera, and were tagged at 23 breeding and eight nonbreeding sites. We compared breeding performance and return rates of birds with geolocators to control groups while controlling for potential confounding variables. RESULTS: We detected negative effects of tags for three small-bodied species. Geolocators reduced annual return rates for two of 23 taxa: by 63 % for semipalmated sandpipers and by 43 % for the arcticola subspecies of dunlin. High resighting effort for geolocator birds could have masked additional negative effects. Geolocators were more likely to negatively affect return rates if the total mass of geolocators and color markers was 2.5-5.8 % of body mass than if tags were 0.3-2.3 % of body mass. Carrying a geolocator reduced nest success by 42 % for semipalmated sandpipers and tripled the probability of partial clutch failure in semipalmated and western sandpipers. Geolocators mounted perpendicular to the leg on a flag had stronger negative effects on nest success than geolocators mounted parallel to the leg on a band. However, parallel-band geolocators were more likely to reduce return rates and cause injuries to the leg. No effects of geolocators were found on breeding movements or changes in body mass. Among-site variation in geolocator effect size was high, suggesting that local factors were important. CONCLUSIONS: Negative effects of geolocators occurred only for three of the smallest species in our dataset, but were substantial when present. Future studies could mitigate impacts of tags by reducing protruding parts and minimizing use of additional markers. Investigators could maximize recovery of tags by strategically deploying geolocators on males, previously marked individuals, and successful breeders, though targeting subsets of a population could bias the resulting migratory movement data in some species.

Arctic-nesting birds find physiological relief in the face of trophic constraints.

A climate-induced phenological mismatch between the timing of reproduction and the timing of food resource peaks is one of the key hypothesized effects of climate change on wildlife. Though supported as a mechanism of population decline in birds, few studies have investigated whether the same temperature increases that drive this mismatch have the potential to decrease energetic costs of growth and compensate for the potential negative effects of reduced food availability. We generated independent indices of climate and resource availability and quantified their effects on growth of Dunlin (Calidris alpina) chicks, in the sub-arctic tundra of Churchill, Manitoba during the summers of 2010-2011 and found that when resource availability was below average, above average growth could be maintained in the presence of increasing temperatures. These results provide evidence that chicks may find physiological relief from the trophic constraints hypothesized by climate change studies.

Logging affects fledgling sex ratios and baseline corticosterone in a forest songbird.

Silviculture (logging) creates a disturbance to forested environments. The degree to which forests are modified depends on the logging prescription and forest stand characteristics. In this study we compared the effects of two methods of group-selection ("moderate" and "heavy") silviculture (GSS) and undisturbed reference stands on stress and offspring sex ratios of a forest interior species, the Ovenbird (Seiurus aurocapilla), in Algonquin Provincial Park, Canada. Blood samples were taken from nestlings for corticosterone and molecular sexing. We found that logging creates a disturbance that is stressful for nestling Ovenbirds, as illustrated by elevated baseline corticosterone in cut sites. Ovenbirds nesting in undisturbed reference forest produce fewer male offspring per brood (proportion male = 30%) while logging with progressively greater forest disturbance, shifted the offspring sex ratio towards males (proportion male: moderate = 50%, heavy = 70%). If Ovenbirds in undisturbed forests usually produce female-biased broods, then the production of males as a result of logging may disrupt population viability. We recommend a broad examination of nestling sex ratios in response to anthropogenic disturbance to determine the generality of our findings.

Factors influencing the turnover and net isotopic discrimination of hydrogen isotopes in proteinaceous tissue: experimental results using Japanese quail.

Stable hydrogen isotopes (δ(2)H) are commonly used in studies of animal movement. Tissue that is metabolically inactive after growth (e.g., feathers) provides spatial or dietary information that reflects only the period of tissue growth, whereas tissues that are metabolically active (e.g., red blood cells) provide a moving window of forensic information. However, using δ(2)H for studies of animal movement relies on the assumption that tissue δ(2)H values reflect dietary δ(2)H values, plus or minus a net diet-tissue discrimination value, and that the turnover rate is known for metabolically active tissue. The metabolic rate of an animal may influence both diet-tissue discrimination values and isotopic tissue turnover rate, but this hypothesis has not been tested experimentally. To examine the metabolic hypothesis, an experimental group of 12 male and 15 female captive Japanese quail (Coturnix japonica) was housed at 8.9°C for 90 d to elevate their metabolic rates (mL CO(2) min(-1)), and a control group of 12 male and 13 female quail was housed at room temperature during the same period. For both experimental and control birds, diet-tissue discrimination values were estimated for red blood cells and feathers. To determine turnover rate, experimental and control birds were switched from a (2)H-enriched diet to a (2)H-depleted diet, with red blood cells sampled before and after diet switch. Metabolic rate did not influence red blood cell hydrogen isotope turnover rate (η(2)(p) = 0.24)) or diet-feather isotope discrimination values (η(2)(p) = 0.86). Diet-feather hydrogen isotopic discrimination had a significant sex plus treatment interaction effect; female feathers were depleted in (2)H relative to food regardless of treatment, whereas male feathers were enriched in (2)H. The effect of sex suggested that experimental studies should examine whether coeval males and females differ in blood δ(2)H levels during certain periods of the annual cycle.

Do floral syndromes predict specialization in plant pollination systems? An experimental test in an "ornithophilous" African Protea.

We investigated whether the "ornithophilous" floral syndrome exhibited in an African sugarbush, Protea roupelliae (Proteaceae), reflects ecological specialization for bird-pollination. A breeding system experiment established that the species is self-compatible, but dependent on visits by pollinators for seed set. The cup-shaped inflorescences were visited by a wide range of insect and bird species; however inflorescences from which birds, but not insects, were excluded by wire cages set few seeds relative to open-pollinated controls. One species, the malachite sunbird (Nectarinia famosa), accounted for more than 80% of all birds captured in P. roupelliae stands and carried the largest protea pollen loads. A single visit by this sunbird species was enough to increase seed set considerably over unvisited, bagged inflorescences. Our results show that P. roupelliae is largely dependent on birds for pollination, and thus confirm the utility of floral syndromes for generating hypotheses about the ecology of pollination systems.