Cheating in mutualisms? Nectar-robbing and nectar-thieving

As a pollination ecologist, I study the mutualistic relationship between plants and their pollinators. Mutualism is roughly defined as an interaction between organisms in which both partners benefit in some way. Pollination is often treated as a classic case: the pollinator gets nectar (i.e., food), and the plant gets pollination (i.e., reproduction).

However, it's worth remembering that neither participant is engaging in the interaction for the benefit of the other: in broad terms, the plant doesn't offer nectar to help out the pollinators, it does it because offering nectar improves the plant's success; the pollinator doesn't pollinate in order to help out the plants, it does it because foraging for food in flowers improves the pollinator's success. I've talked about plants that are jerks a few times before (1, 2, 3); today I'm going to talk about the flip-side of that, the 'pollinators' who are jerks. In this case, when I say that a plant or a pollinator is a "jerk", I mean that it has developed an adaptation that allows it to gain the benefits of the plant-insect interaction without offering the interaction partner any benefit -- in other words, it's a cheater. Deceptive plants fall under this umbrella, because they deceive pollinators by seeming to offer a reward, but without actually doing so and thus without incurring the cost of making the reward (usually nectar). There's some really cool research that has been done on the evolution of cheating in mutualistic relationships, which I may talk about another time. For today, I'm going to focus more narrowly on floral larceny.

So what is floral larceny? The general idea is that the putative pollinator is obtaining the reward without offering the service. So a floral visitor gets nectar without moving any pollen. Nectar-robbing is a frequently-studied form of floral larceny: the visitor, rather than trying to get in through the regular opening of the flower, just cuts a hole near the nectary and sucks up the nectar, avoiding contact with the reproductive parts of the flower and consequently providing no pollination service. In principle, certain floral shapes are adaptations that exclude bad pollinators and improve the fit of good ones by orienting them in particular ways in the flowers, but at least some of these flowers, particularly with long, tubular flowers, and especially the more rewarding ones, are more likely to be the targets of nectar robbers (Rojas-Nossa et al. 2016), so the extent to which they're actually excluding bad pollinators, as opposed to converting them into nectar robbers (which might be worse? Or not, see below), is unknown. Actual measured consequences of floral larceny on floral fitness actually range from negative to positive, which further complicates interpretation of nectar-robbing behaviour (see Irwin et al. 2010 Annual Reviews of Ecology, Evolution, and Systematics).

I managed to get some footage of a nectar robber on Impatiens capensis (jewel-weed). You can see that the robber bites a hole in the flower to get at the nectar; it's quite clear that the nectar-robbing wasp is bypassing the reproductive parts of this flower, but I witnessed several wasps engage both in nectar-robbing, and then in the more standard foraging that involved entering the flower and possibly transporting pollen. 

Similarly, if you look at the Xylocopa virginica (carpenter bee, notably one of the largest insect pollinators in this region; there are several shown in the videos below) on the hostas in the video below, first you can really clearly see in the slow-motion video as she pushes her tongue through the flower into the nectary, but in the next video in real-time, you can see that in some instances she may be brushing her very large abdomen over the reproductive parts of the plants anyway, and you can actually see some pollen grains on her shiny abdomen as she engages in this nectar-robbing behaviour, so it's not really clear whether she's truly failing to provide pollination services here, even while she engages in fairly classic nectar-robbing.

Another form of floral larceny is nectar thievery: the visitor enters through the normal floral opening, but does not make contact with the reproductive parts of the flower and consequently transfers no pollen. 

I have some footage of visitors engaging in nectar thievery on the hostas in my back yard. The video shows a relatively classical case, where the nectar thievery arises because of a morphological mismatch (i.e., the shape of the insect and flower don't match up correctly);this nectar thief is just too small to contact the reproductive parts of the flower, but of course that doesn't prevent it from foraging for nectar on the flowers.

There are also forms of floral larceny relating to pollen-robbing (which causes damage in the course of pollen removal, and in which the pollen isn't transmitted elsewhere), and pollen-thieving (no damage, but pollen is not transferred). There is very little information on these phenomena, probably because they would probably be extremely hard to confirm. Unfortunately, I don't have any footage of these. Pollen-thieving in particular might actually be quite common, depending on how we define it: here's some footage of X. virginica (carpenter bee) grooming pollen off herself; grooming is a common bee behaviour. Bees collect pollen to stock their nest cells with it (i.e., it's food for developing larvae), so a large quantity of the pollen they collect ends up not on other flowers but instead in the bees' nests. This might be considered a form of pollen theft, depending on how you want to define it. Pollen thieving is a rather understudied area, but there's an interesting review for those interested (Hargreaves et al. 2009).

Bonus, partial answer to one of the questions I raised in my first post about I. capensis (why are they shaped like this), here's Apis mellifera (honeybee) grooming herself after visiting I. capensis. Notice that the big patch of pollen between her wings isn't getting removed. Possibly, then, the shape of I. capensis helps to ensure that pollen is deposited on a part of the pollinator where it's less likely to get groomed off and therefore lost as food for bee larvae. The shape could also be at least partially driven by improved accuracy of pollen deposition onto stigmas; if the pollen ends up just anywhere on the pollinator, it might not be very accurately transmitted onto the stigmas of other flowers.

For fun, here's some footage of a Bombus sp. (bumblebee) worker who is definitely picking up pollen as she goes, though it's less obvious whether she's successfully depositing it on stigmas. Look at all that pollen on her abdomen! Pretty much whenever she enters and leaves the flower, she's brushing right up against the reproductive parts of the hosta: