Journal of Applied Ecology 2012, 49, 126–134
doi: 10.1111/j.1365-2664.2011.02066.x
Spatial and temporal variation in pollinator effectiveness: do unmanaged insects provide consistent pollination services to mass flowering crops? Romina Rader1,2*, Bradley G. Howlett2, Saul A. Cunningham3, David A. Westcott1,4 and Will Edwards1 1
School of Marine and Tropical Biology, James Cook University, PO Box 6811, Cairns 4870, Australia; 2The New Zealand Institute for Plant & Food Research Limited, Private Bag 4704, Christchurch, New Zealand; 3CSIRO Ecosystem Sciences, PO Box 1700, Canberra, ACT 2601, Australia; 4CSIRO Ecosystem Sciences, PO Box 780, Atherton, Qld 4883, Australia
Summary 1. Recent declines in honeybee populations have focused attention on the potential for unmanaged insects to replace them as pollinators of food crops. The capacity of unmanaged pollinators to replace services currently provided by honeybees depends on the spatial and temporal variability of these services, but few quantitative assessments currently exist. 2. We investigated spatial variation in pollinator importance by comparing pollinator efficiency and effectiveness in stigmatic pollen loads, stigmatic contact and visitation rate between honeybees and the seven most abundant unmanaged taxa in 2007. We assessed temporal variability in pollinator visitation using floral visits recorded three times a day over four consecutive years (2005–2008) in 43 ‘Pak Choi’ Brassica rapa ssp. chinensis mass flowering fields in the Canterbury region of New Zealand. Further, we compared the aggregate effect of the unmanaged pollinator assemblage to the managed honeybee. 3. Pak Choi was visited by many insect species that vary in abundance and effectiveness as pollen transfer agents. There was spatial variation in the four measures of pollinator importance. Pollen deposited on stigmas and flower visits per minute were not significantly different comparing the unmanaged assemblage to honeybees, although stigmatic contact and visitor abundance per number of open flowers were greater in honeybees. 4. Unmanaged taxa were frequent visitors to the crop in all 4 years. The pooled services provided by the unmanaged assemblage did not differ within a day and were equal to or greater than those provided by honeybees in 2 of the 4 years. Pollinator importance changed little irrespective of the spatial and temporal variations among taxa. 5. Synthesis and applications. The results of this study suggest that some unmanaged insect taxa are capable of providing consistent pollination services over a 4-year period in a commercial mass flowering crop. As these taxa already contribute substantially to the pollination of food crops, they offer a safety net in the case of sudden collapse of managed honeybee hives. To optimize pollination services, we recommend pollinator-specific farm management practices that consider the needs of both managed and unmanaged pollinator taxa. Key-words: Brassica, diptera, diversity, ecosystem function, efficiency, honeybee, native, pollen, stability, wild
*Correspondence author. Department of Entomology, Rutgers, The State University of New Jersey, 93 Lipman Drive, New Brunswick, NJ 08901, USA. E-mail:
[email protected] 2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society
Spatial and temporal pollinator effectiveness 127
Introduction The current global pollination crisis highlights the advantages of the provision of pollination services by a suite of unmanaged pollinators (McCann 2000; Klein et al. 2007). This is because the intrinsic differences between taxa in their ecological tolerances should result in populations of individual species responding differently to environmental change, such that changes in abundance will not be temporally or spatially coordinated across species (Herrera 1990; Tylianakis, Klein & Tscharntke 2005; Hoehn et al. 2008). Both abundance and behavioural-mediated mechanisms can enhance the stability of pollination services. Assemblages that contain a wide range of species with different ecological requirements could maintain pollination services as environmental conditions change over time because (i) declines in abundance of some taxa can be offset by increases in others (Yachi & Loreau 1999; McCann 2000; Elmqvist et al. 2003) and (ii) interspecific interactions can enhance net pollinator services (Greenleaf & Kremen 2006). This is the basis of the biological insurance hypothesis with respect to pollination as an ecosystem service (Walker 1992; Lawton & Brown 1993; Naeem & Li 1997; Naeem 1998). Ascertaining the reliability of unmanaged, multi-species, pollinator assemblages requires an assessment of their overall contribution to pollination and the upper and lower limits of spatial and temporal variability associated with each species’ contribution (i.e. their reliability; Watanabe 1994; Allen-Wardell et al. 1998; Naeem 1998; Elmqvist et al. 2003; Memmott et al. 2007). While the potential for unmanaged insects to act as crop pollinators has been addressed (Klein et al. 2007; Winfree et al. 2007; Hoehn et al. 2008; Rader et al. 2009), few studies have assessed the consistency of pollination services in these systems (but see Kremen, Williams & Thorp 2002; Winfree & Kremen 2009). This is probably due to the inherent temporal variability in abundance estimates for unmanaged taxa (Cane & Payne 1993; Roubik 2001) that can obscure general patterns. This variability is especially prevalent in intensive agricultural systems because the ephemeral nature of floral resources (Corbet 2000; Williams & Kremen 2007; Ricketts et al. 2008) can alter pollinator foraging behaviours (Diekotter et al. 2010) and reduce the presence of habitat specialists (Tylianakis, Klein & Tscharntke 2005). ‘Pak Choi’ Brassica rapa L. ssp. chinensis L. (Hanelt.) (Brassicaceae) in New Zealand is visited by many insect species that vary in abundance and effectiveness as pollen transfer agents (Rader et al. 2009). However, the capacity for a suite of unmanaged taxa to provide consistent pollination services to agricultural crops across a landscape, within a day and over a period of years, has to our knowledge not been demonstrated previously. We maintain that for this consistency to be applicable to industry and land managers, (i) unmanaged pollinators must be able to perform in commercial agricultural crops where productivity is directly linked to economic outcomes (Aizen et al. 2008; Allsopp, de Lange & Veldtman 2008; Gallai et al. 2009); (ii) unmanaged pollinator services need to be com-
parable to existing managed pollinator services if they are to offer a safety net in the case of managed pollinator collapse. Managed pollinators are, therefore, an ideal benchmark by which to assess any potential economic gain or loss provided by unmanaged taxa. In this study, we compare the pollination services provided by the managed honeybee to unmanaged pollinator taxa in commercial mass flowering B. rapa seed crops to ask the following questions: 1. Are unmanaged pollinator taxa capable of providing consistent pollination services to a mass flowering crop across several locations and over time? 2. Are these services likely to provide pollination rates equal to that of the managed honeybee? These questions are important to assess the likelihood that unmanaged pollinators can provide commercial level pollination services to a mass flowering crop.
Materials and methods STUDY SPECIES
Brassica rapa is a mass flowering crop. This and other species of Brassicaceae are grown commercially in New Zealand for use as forage, seed, vegetable and oilseed production (Stewart 2002). Brassica rapa is an ideal crop to examine spatial and temporal changes in pollinator visitation as it attracts a diverse assemblage of insects (Feldman 2006; Howlett et al. 2009; Rader et al. 2009), displays increased seed set in the presence of insect pollinators (Free 1993) and is ubiquitous in most agricultural landscapes as a crop ⁄ environmental weed (Heenan, Fitzjohn & Dawson 2004; Feldman 2006; Sutherland, Justinova & Poppy 2006).
FREQUENTLY VISITING POLLINATORS
Eight pollinators were considered ‘frequent visitors’ in this study as they were responsible for 79Æ8% of all flower visits. These include four bees: Apis mellifera Linnaeus, 1758, Bombus terrestris (Linnaeus, 1758), Lasioglossum sordidum (Smith, 1853) and Leioproctus sp. and four flies, Dilophus nigrostigma (Walker, 1848), Melangyna novaezelandiae (Macquart, 1855), Eristalis tenax (Linnaeus, 1758) and Melanostoma fasciatum (Macquart, 1850).
POLLINATOR EFFECTIVENESS
We used four measures to characterize overall pollinator effectiveness. Two of these were related to pollen transfer efficiency as follows: (i) amount of pollen deposited on stigmas per single visit and (ii) stigmatic contact, and two others related to the rate of visitation: (iii) flower visitation rate (number of flower visits by an individual pollinator per minute) and (iv) visitor abundance per number of available open flowers (measured by observed visits to a 10 · 10 m quadrat per 10 min and corrected for the no. open flowers in the quadrat; Rader et al. 2009). To simplify terminology relating to the rate of visitation, we refer to (iii) as ‘flower visits per minute’ and (iv) as ‘visitor abundance per number of open flowers’. As these measures have been used widely in the literature to quantify and rank individual pollinator contributions to overall pollination services (Primack & Silander 1975; Herrera 1987; Vazquez, Morris & Jordano 2005; Ne’eman et al. 2010), we use
2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society, Journal of Applied Ecology, 49, 126–134
128 R. Rader et al. all four measures in an attempt to understand the spatial and temporal patterns relating to the provision of pollinator services by unmanaged taxa.
SPATIAL DIFFERENCES IN POLLEN TRANSFER EFFICIENCY AND VISITATION RATE
To investigate spatial variation in pollen transfer efficiency and visitation rate, we observed flower visitors in four commercial B. rapa fields (two in Lincoln (Lincoln site 1: 4337¢53Æ92¢¢S; 17229¢03Æ96¢¢E; Lincoln site 2: 4337¢28Æ52¢¢S; 17228¢12Æ46¢¢E) and two in Gore (Gore site 1: 4607¢00Æ13¢¢S; 16852¢58Æ74¢¢E; Gore site 2: 4606¢28Æ89¢¢S; 16853¢35Æ70¢¢E) on the South Island of New Zealand between December 2006 and February 2007. Fields were selected according to their size (2 ha) and location adjacent to pasture (predominately Lolium perenne) without neighbouring flowering crops. Common flowering weeds were present within field margins at low densities. These included white clover Trifolium repens L., shepherds purse Capsella bursa-pastoris L. (Medik.), hedge mustard Sisymbrium officinale L. (Scop.) and Mallow Malva spp. Because of the large number of honeybee hives operating in close proximity to all four study sites (range 3–8), we assume all honeybee visits were from managed hives. All floral visitor observations were made on sunny or partly cloudy days when the temperature was >16 C and wind speed 10 time periods per year) in all 4 years. The seven frequent visitors in addition to A. mellifera were one introduced bee, B. terrestris, two native bees, L. sordidum and Leioproctus sp. and four flies, D. nigrostigma, M. novaezelandiae, E. tenax and M. fasciatum. Honeybees were responsible for 40Æ6% of all visits, and the seven unmanaged taxa were responsible for 39Æ2%. Visitation rates of the remaining 35 species (see Table S1, Supporting Information) were highly variable. Fourteen species visited with high frequency (>10 time periods per year) in two or three of the 4 years, 12 were frequent in 1 year only,
Stigmatic pollen loads (no. pollen grains)
600
(a)
while the remaining nine species were always observed in low numbers (
