How to efficiently obtain accurate estimates of flower visitation rates by pollinators

Abstract Regional declines in insect pollinators have raised concerns about crop pollination. Many pollinator studies use visitation rate (pollinators/time) as a proxy for the quality of crop pollination. Visitation rate estimates are based on observation durations that vary significantly between studies. How observation duration relates to the accuracy of the visitation rate estimate is, however, unknown. We studied this relationship using six day-long observations (06:00 h–19:00 h) in leek-seed production fields (totalling 78 h). We analysed beyond which point in time observing longer did not significantly improve the accuracy of the visitation rate estimate (minimum observation duration). We furthermore explored the relationship between the minimum observation duration and visitation rate, time of day and temperature. We found that the minimum observation duration (mean ± SD: 24 ± 11.9 min) was significantly related to visitation rate, where the observation time required to obtain accurate estimates decreased with increasing visitation rate. Minimum observation duration varied greatly between days and between fields but not within days. Within days, the visitation rates differed significantly only between the hour-intervals 06:00 h–07:00 h (lowest visitation rate) and 09:00 h–11:00 h (highest rate). Minimum observation duration decreased up to around 22 °C beyond which it remained fairly stable. Surprisingly, even after three day-long observations on the same plant we found new pollinator species visiting the flowers, suggesting that species-richness estimates based on plant observations alone probably underestimate true species richness. Because especially between-day variation in visitation rate on single plants can be large, reliable estimates of the pollinator visitation rate during the plant’s flowering time require observations on multiple days. Standardising the number of pollinators rather than the time to observe (standardised pollinator timing approach: time to n -pollinator visits) may provide more consistent accurate assessments of visitation rate, especially for studies that use gradients in visitation rates to examine the contribution of pollinators to crop pollination.

[1]  L. Carvalheiro,et al.  Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms , 2016, Science.

[2]  N. Blüthgen,et al.  High diversity stabilizes the thermal resilience of pollinator communities in intensively managed grasslands , 2015, Nature Communications.

[3]  C. Herrera Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. , 1990 .

[4]  J. Brewster,et al.  Onions and Other Vegetable Alliums , 1994 .

[5]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[6]  James Regetz,et al.  Landscape effects on crop pollination services: are there general patterns? , 2008, Ecology letters.

[7]  Emily A. May,et al.  Delivery of crop pollination services is an insufficient argument for wild pollinator conservation , 2015, Nature Communications.

[8]  P. Simon,et al.  Flowering, seed production, and the genesis of garlic breeding , 2010 .

[9]  Breno M. Freitas,et al.  Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance , 2013, Science.

[10]  A. Klein,et al.  Importance of pollinators in changing landscapes for world crops , 2007, Proceedings of the Royal Society B: Biological Sciences.

[11]  David R. Anderson,et al.  Estimation of Density from Line Transect Sampling of Biological Populations. , 1982 .

[12]  Hannah R. Gaines,et al.  Wild bee pollinators provide the majority of crop visitation across land‐use gradients in New Jersey and Pennsylvania, USA , 2007 .

[13]  R. Moll Receptivity of the individual onion flower and some factors affecting its duration , 1954 .

[14]  Teja Tscharntke,et al.  Functional group diversity of bee pollinators increases crop yield , 2008, Proceedings of the Royal Society B: Biological Sciences.

[15]  J. Biesmeijer,et al.  Global pollinator declines: trends, impacts and drivers. , 2010, Trends in ecology & evolution.

[16]  H. Wright Commercial Hybrid Seed Production , 2015 .

[17]  Marti J. Anderson,et al.  Measures of precision for dissimilarity-based multivariate analysis of ecological communities , 2014, Ecology letters.

[18]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[19]  J. Ghazoul,et al.  Impact of forest fragments on bee visits and fruit set in rain-fed and irrigated coffee agro-forests , 2013 .

[20]  T. Ricketts Tropical Forest Fragments Enhance Pollinator Activity in Nearby Coffee Crops , 2004 .

[21]  Rachael Winfree,et al.  Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. , 2015, Ecology letters.

[22]  Theodora Petanidou,et al.  MEASURING BEE DIVERSITY IN DIFFERENT EUROPEAN HABITATS AND BIOGEOGRAPHICAL REGIONS , 2008 .

[23]  C. Dormann,et al.  Bee diversity effects on pollination depend on functional complementarity and niche shifts. , 2013, Ecology.

[24]  A. Berti,et al.  Degradation of soil fertility can cancel pollination benefits in sunflower , 2015, Oecologia.

[25]  David R. Anderson,et al.  Estimation of Density from Line Transect Sampling of Biological Populations. , 1981 .

[26]  Chris S. Elphick,et al.  How you count counts: the importance of methods research in applied ecology , 2008 .

[27]  J. Cane The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields , 1997 .

[28]  M. Aizen,et al.  Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forest. , 2005 .