Papers from the Bernhardt/Meier laboratory record the bee species visiting a plant species but also record whether each bee captured carried the host flower's pollen or the pollen of other species mixed with the host flower.  This information is easily quantified.  Based on pollen load analyses like this it's a relatively easy matter to determine which bee species are generalists (polylectic) and which species are oligolectic.  Here are some recent publications emphasizing pollination of some rather rare plants by polylectic foragers.

Edens-Meier, R.E., Joseph, M., Aduser, M., Westhus, E. & Bernhardt, P. 2011. The pollination biology of an annual endemic herb, Physaria filiformis (Brassicaceae), in the Missouri Ozarks following controlled burns. The Journal of The Torrey Botanical Society 138: 287-297. 76).

Bermhardt, P., Meier, R. & Vance, N. 2013. Pollination ecology and floral function of Brown’s peony (Paeonia brownii) in the Blue Mountains of northeastern Oregon. Journal of Pollination Ecology. 1: 9 – 20. 78).

 Bernhardt, P., Edens-Meier, R., Westhus, E. & Vance, N. 2014. Bee-mediated pollen transfer in two populations of Cypripedium montanum Douglas ex Lindley. Journal of Pollination Ecology 13: 188-202..

Our research tends to indicate that plants are more dependent on bee species than any single bee species is dependent on a particular plant species.  Flowers limit which bees can enter and remove rewards but that does not stop certain bees from pollinating a broad number of unrelated but co-blooming species.  Consider the flowers that offer pollen but no nectar.  Some are vibratile (buzz-polinated) flowers dependent only on Bombus or Lasioglossum species but the same bee species carry the pollen of up to 5 cob looming species upon capture.

Bernhardt, P. & Montalvo, E.A. 1977. The reproductive phenology of Echeandia macrocarpa Greenm. (Liliaceae) with a reexamination of the floral morphology. Bulletin of the Torrey Botanical Club 104: 320-323.

Bernhardt, P. & Walker, K. 1984. Bee foraging on three sympatric species of Australian Acacia. International Journal of Entomology 26: 322-330.

Bernhardt, P. 1986. Bee-pollination of Hibbertia fasciculata (Dilleniaceae). Plant Systematics & Evolution. 152: 231-241.

Mutualisms between some (many?, all?) plant species and their pollinators appear to be asymmetric with the plant species undergoing far more modification over generations compared to the pollinators.  This seems especially common in the orchid family.  See our new book...

Edens-Meier, R. & Bernhardt, P. (editors) 2014. Darwin’s Orchids: Then & Now. University of Chicago Press, USA.

I have seen nectar robbing only in social species, namely short tongued bumble bees and honeybees in flowers with long corolla. Usually the bumblebees bite the hole in the corolla to reach the nectar and later on also honeybees use it. I have never seen solitary bee species using the hole, but wouldn't swear this isn't the case. Though in the description of the behaviour I've read, they talked always about bumblebees making the hole because of their strong mandibles. But this was always more anecdotal evidence, don't know if there are any papers.

I would like to add a fundamental answer to this question. Active pollination is extremely rare and known for example from yucca moths and fig wasps which not only actively pollinate flowers but also deposit their egg in the flowers. Flowers thus have to manipulate bees in order to get pollinated and bees that find a more efficient than the legetimate way to visit a flower will do it. And in contrast to other pollinators bees do not drink only nectar but also collect large amounts of pollen. To make things worse the pollen that has been stort in the scopa, the pollen transport organ, is no longer available for pollenation at least not in corbiculate bees that use regurgitated nectar to compact the pollen in their corbiculae.

Klaus

Mutualists (highly efficient pollinators) and antagonists (nectar thieves and robbers, pollen thieves, etc..) are mostly no distinct groups; mutualisms and antagonism are rather the extremes of a continuum, especially if bees are considered. Thus, it is hard to tell, which proportion of the flowering plant species that are visited by a bee species is actually pollinated by that bee (i.e. presence / absence of pollination). I would suggest a ranking from highly efficient to inefficient would be more appropriate. You should have a look at the literature on pollinator efficiency, for example these:

Junker, RR, R Bleil, CC Daehler, and N Blüthgen (2010) Intra-floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness. Ecological Entomology 35:760-767.

Kandori, I (2002) Diverse visitors with various pollinator importance and temporal change in the important pollinators of Geranium thunbergii (Geraniaceae). Ecological Research 17:283–294.

Madjidian, JA, CL Morales, and HG Smith (2008) Displacement of a native by an alien bumblebee: lower pollinator effciency overcome by overwhelmingly higher visitation frequency. Oecologia 156:835–845.

Reynolds, RJ and CB Fenster (2008) Point and interval estimation of pollinator importance: a study using pollination data of Silene caroliniana. Oecologia 156:325–332.

Sahli, HF and JK Conner (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanismum (Brassicaceae). American Journal of Botany 94:203-209.

Hi! Thanks for all inputs and references, great discussion! Taking together the comments from Claudia Garrido and Robert Junker, I agree with the continuum idea, moreover, my perception and the data I have collected so far based on pollen transported by bees and its role on the flowers where they get the pollen from suggests a drastically different role for social and solitary bees. Going with Klaus fundamental point, bees tend to become more and more efficient in collecting pollen, and that seems to be clear among eusocial (clean and tidy) bees. So, maybe to scape from eusocial bee visitation could be a great evolutive solution and will agree with Peter suggestion on plants being more vulnerable in the pollination relationships... Although we already have a reasonable amount of plant-community interaction webs I would like to see proper assessments of pollination continuum. For sure bees are numerically more interactive, but not sure they always reach the high importance attributed to them at the community level... Are you aware of community assessments of pollinator importance based on good proxies for pollination? Just to complete, by mutualism I was not meaning the active pollination mutualism but a more broadly definition following Jander and Herre: a reciprocal exploitative relationship where both interacting species have liquid benefits. 

Hi guys, Don´t forget that some nectar robbers, with his awkward movement up the flowers, end up becoming a good pollinators!

Navarro, L. (2000) Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators. American Journal of Botany 87(7): 980-985.

One could also mention the mutualistic indirect impacts, right? Some nectar-robbers attract small bees looking for nectar otherwise inaccessible to them, which then pollinate the flowers when they collect simultaneously for pollen.

Some interesting discussion here which I don't have a lot to add to, most bases have been covered.  Except that there's an interesting question related to this that hasn't been mentioned: are pollen-specialist bees better or worse pollinators of the plant on which they specialise, compared to other flower visitors on that plant?  So for example, is the Ivy Bee (Colletes hederae) a better or worse pollinator than the wasps and flies that also visit ivy?  Has this question ever been tested?

In regard to Andre´s and Jeff´s comment I would like to add that most social bees transport the collected pollen in the corbiculae of their hindlegs in a compacted manner and by this way withdraw these pollen grains from pollination. The spiny pollen of the Malvaceae family and other plant families seems to be a mechanical protection against being collected by corbiculate bees, since honeybees and bumblebees are unable to store the spiny pollen in their corbiculae. Pollination is not affected: The pollen grains adhere very well to the bees´ bristles, but cannot be compacted (paper attached). In this view pollinatin by bees seem to be an evolutionary race between optimization of pollen collection in bees and optimization of safe pollen transport on bees´ bodies between flowers. Maybe we don´t not yet know all the arms that have been used in this evolutionary ping-pong.

Klaus

Yes, happy with the high level of this discussion! Agree with Luis, Is it just bad for the plants? I´m aware of Klaus paper on spiny pollen, so plants have also evolved defensive mechanisms... The only reference I know comparing specialized solitary bees and other flower visitors is on Knautia arvensis and the solitary bees seems to be more efficient in transport pollen but less frequent on female flowers. So, I feel there is a gap to be filled with the data I have on plants collected and plants pollinated by tree species of social bees in Brazil. I suspect the very efficient collecting behaviour of eusocial bees and its ubiquitous occurrence, being normally the dominant bees in terms of abundance have something to do with the evolution of specialised flower morphologies. Thanks for the great discussion!

The question on a community-wide assessment of pollinator efficiency by Andre Rech is definitively something to do, i.e. combining a network study with careful measurements of pollination success per plant-animal pair. It has been debated whether visitation frequency is a good proxy for pollination effectiveness as suggested by Vazquez et al. (2005 Ecology Letters) or whether it is single-visit pollen deposition as proposed by King et al. (2013 Methods in Ecology and Evolution). Again, I think that this is a kind of continuum as well: poor single-visit quality can be compensated by a high frequency of visits and vice verse.

A few years ago, we made an attempt of quantifying both visitation frequency and behaviour at flowers (behaviour most likely leading to pollination vs. behaviour most likely harmful to the flowers) for a high proportion of links in a German flower-visitor community (unfortunately never published). We assumed (and I still do so) that pollinator effectiveness can be best estimated by the product of quantity (visitation frequency) and quality (efficiency per visit), see also Junker et al. (2010 Ecological Entomology). Here we found a continuum in pollinator effectiveness. What we also found was a high “behavioural diversity” of flower visitors meaning that many flower visits do not involve just only the collection of resources. Their behaviour ranged from sleeping, having sex to just destroying the flowers (many ants and beetles did so). This may be something to repeat and I would be happy to share my experience.

Alternatively, another way of approaching this community-perspective on pollinator effectiveness is to compare flower-visitor networks with networks constructed from pollen grains attached to bodies of flower visitors as done for example by Alarcon (2010 Oikos). This may be a bit more feasible and definitively a good start to answer this question.

Finally, a note on the terms pollinator effectiveness and efficiency. These terms are somehow used as synonyms, while other authors clearly have unique definitions. In my point of view, and as written above, effectiveness is the product of quantity (visitation frequency) and quality (efficiency per visit): effectiveness = frequency * efficiency, which is also defined like that by other authors. Maybe anybody has something to add?

I have studied the pollination of Hibiscus by Ptilothrix bees. They are truly effective pollinators due to their high foraging abundance, but individually they are rather inefficient pollinators. Curiously, their pollination efficiency (stigmatic pollen loads and host seed set) triples or more when males and females fight or copulate in blooms.  I also found that floral specialist and generalist bees tend to be equitably efficient pollinators at blueberry at least on a per bee basis.  I hope this helps.   All the best,  blair

Thank all! I would like to add a references to bring even more complexity to Vazquez and King. http://www.ncbi.nlm.nih.gov/pubmed/23928839