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:

Pop! goes the seed pod

Earlier this week, I posted about the profusely blooming Impatiens capensis (jewel-weed), particularly a few visitors I managed to film visiting the flowers.

Today, I want to share something rather different. It's not as much in my area, but it is a rather awesome feature of this and some other plants: explosive seed dispersal. Yes, that's a thing.

The biological purpose of a flower, of course, is reproduction. Remember from the last post that I. capensis individual plants make male flowers, which donate pollen to fertilise ovules, and they also make female flowers, which produce ovules that, when fertilised with pollen, will develop into seeds.

Impatiens capensis male flower (middle) and female flower (right).

Impatiens capensis is an annual, so any given individual won't grow back in the spring; consequently, it won't compete directly with its offspring for suitable growing space. The seeds are all at least half-siblings, however, so it's in the interest of the genes not to have (half-)siblings too close together.

Basically, there's good reason to suppose that a strategy that disperses seeds within a few meters of the plant (i.e., close to where suitable conditions for growth and reproduction were found, since the parent grew and successfully reproduced there, and because the plant is an annual there's no major incentive to disperse offspring further from the parent plant to avoid parent-offspring competition), but not all too close to one another (since they're at least half-siblings and share genes, so the genes would spread better through a population if they don't spend too much energy directly competing with each other), would be advantageous for this species.

There are all sorts of seed dispersal mechanisms. Explosive seed dispersal (a.k.a. projectile dispersal) is one of my favourite, however, because it's very dramatic. Here's what a seed pod looks like in I. capensis:

Impatiens capensis seed pod

Inside this elongated structure, there are a bunch of seeds (somewhere around 8-10, if I remember correctly). Each plant can produce quite a lot of these. So the explosive seed dispersal may be how I. capensis got one of its common names, "touch-me-not", but I think that's a misnomer because it's so fun to pop them that I highly recommend that anybody who gets a chance should definitely touch them.

They pop quite audibly:

So how does this even work? I tried to slow my videos down so that it's a bit easier to see what's happening, but it's so rapid that I have limited success. Watch for the seeds and pod flesh flying off:

In order for the seed pod to explode like this when touched, it has to be storing energy. Fortunately for me, I don't have to speculate too much in explaining what's happening here, because New Phytologist just published an article by Hugo Hofhuis and Angela Hay on the topic of explosive seed dispersal in Cardamine hirsuta, a species with extremely similarly shaped seed pods to I. capensis (though the two species are not closely related). I'm going to presume that the broad strokes, at least, are pretty similar in I. capensis. The article is really neat and I highly recommend that you read it, but here's my very brief summary of the findings from the article that may apply to I. capensis explosive seed dispersal.

The TL;DR is that these seed pods (likely) have specially shaped cells and extra lignin in places; essentially they're shaped so that they're always just on the very edge of curling up together, and touching them disturbs the delicate balance that is holding the seed pod's shape. Notice what happens to the fleshy parts of the pods afterwards:

Impatiens capensis seed pod after explosion is triggered

Neat, eh?

Impatiens capensis pollination (Bonus: even bees can be clumsy)

I know I haven't blogged in quite a while. Life got very hectic for a while. In the months my last post, I have finished my M.Sc., gotten published, and moved to the University of Toronto to start my Ph.D.!

Over the weekend I got a chance to take a long walk with my patient and long-suffering husband, who indulged my snagging his new blackberry to take a ton of footage of bees visiting the tens of thousands (at least!) of Impatiens capensis (common name jewel-weed) in the ravine park near our new home. I made all sorts of exciting videos, but today I'm going to share just a few simple ones, as the others will take quite a bit of research and time to write up. I will post these throughout the fall because they're very exciting.

NOTE: I have been informed that my videos don't work on mobile. I'm working on it, but in the meantime they do run on desktop.
UPDATE: try clicking the title of the video instead (treat as link) on mobile. Opens in youtube app. If you don't have youtube app, please report back telling me what it does when you click the video link!

To start, here's a picture of the plant itself:

Impatiens capensis whole plant view

Let's take a quick look at some general reproductive biology of I. capensis. The plant is monoecious, meaning that each plant reproduces through both male and female function; however, each individual flower is unisexual (i.e., any given flower is either male or female but not both). In the photo below, I show three flowers on the same individual. If you look at the top of the "mouth" of each of the lower two flowers in the picture, you will see that each has a different structure; the middle flower has a large, bulbous, whitish structure, while the rightmost flower has a slender green structure.

Impatiens capensis male (middle) and female (right) flower

The middle flower is a male flower; the whitish deposit on it is pollen, ready to be deposited on the back of a pollinator that climbs into the flower looking for nectar (the nectar is in the nectar spur, the little narrow tube curling off the back of the flower, visible on the middle flower). The rightmost flower is a female flower, with a stigma ready to pick up pollen from the back of a visiting insect.

The flower has some rather complex floral anatomy I won't get into right now. There's a pretty good explanation of which parts are sepals and which parts are petals here for those interested. The important thing to note is the lower lip, made of two structures wrapping around the front of the flower, one on each side, that form a sort of landing area of pollinators. They also restrict the width of the flower opening (see photos below).

Impatiens capensis male flower front view. Note that the two sides of the "landing" petals on the front are not fused, just overlapping, and that their shape, because they come down from above around the opening of the cone, reduces the size of the entrance into the flower

Impatiens capensis male flower side view. Notice that the lower "landing" petals are not attached to the conical structure behind.

So I'm going to skip over all sorts of exciting stuff about this plant (why does it have unisexual flowers? Why place pollen on a visitor's back? What's up with that super-complex floral shape?) in order to move straight to some awesome video of assorted Hymenopterans (bees, wasps, ants) visiting this awesome flower!

So I noted above that the '"landing" petals form not just a place for a pollinator to land on the flower, but also a constriction around the opening of the conical part; remember that the nectar is all the way at the back of that cone, in the little nectar spur curling down under the flower. There are several strategies to get past the opening to access this nectar (and then leave again after): one is to simply be small enough to fit through the constriction made by the landing petals; that's how Apis mellifera (honeybee) is doing it (note at 10:00 that you can really see the pollen on this honey bee's back!):

Backing out of the flower can be quite tricky. I managed to get some footage of a visiting wasp finding an alternate method of exiting, which capitalises on the fact that the landing platform and the conical structure behind are not attached to each other:

The Bombus sp. (bumblebee) workers I saw visiting the plants, however, were too big to fit through the opening. But, have no fear! They worked it out anyway. Here's one worker diligently visiting lots of flowers. She's making more room for herself by using her strong back legs (2 pairs) to push the landing petals apart a bit, so that she can shove her head and thorax into the flower and get at the nectar. You'll notice that she doesn't have much difficulty leaving, either, since she's well placed with four legs outside the flower. As far as I can tell, she's just dropping right out of the flower and then flying away.

Here's a longer video of the same bee, diligently visiting a lot of flowers in a row. There's also a little bonus at the end of this video. If you've been clumsy and felt ridiculous for it recently, I have something to comfort you: even bees can be clumsy. If you watch closely at the end, you'll see her climb into a flower, and then she and the flower both fall off the plant to the ground!