Bees can't taste pesticides, and how albatrosses get aloft
In the eLife Podcast this month, signs that bees are oblivious to pesticides in nectar, sea anemone stinging strategies, a new means of cell-cell communication to share growth factors and other signals, how plants make a comeback when ice sheets retreat, and how the world's biggest bird uses wind and waves to good effect to minimise the costs of takeoff...
In this episode
00:40 - Do bees taste pesticides?
Do bees taste pesticides?
Rachel Parkinson, University of Oxford
Modern pesticides, like the neonicotinoids, are extremely effective for protecting crop yields against hungry insects. The problem is that not all hungry insects are unwelcome: some, like bees, are providing a hugely important service through pollinating the plants, which drives up yields. And there’s therefore a risk that they will be indiscriminately poisoned. But the risk might be reduced if bees can taste - and therefore learn to avoid - plants laced with pesticides. So can they? Speaking with Chris Smith, Rachel Parkinson…
Rachel - Lots of different pesticide compounds are used on crops in order to deter pest insects from feeding on them. But other insects, most notably sort of beneficial insects like pollinators, so like bees, will also be feeding on these plants and could be exposed to pesticides. And a question that was sort of unanswered was can bees even taste pesticides in nectar? Would they be able to avoid drinking these pesticides by knowing that they're present based on their taste?
Chris - Does that seem like a reasonable hypothesis to you or would you think It seems a bit spurious because if the other insects are not able to taste and avoid these pesticides, then why should bees be any different?
Rachel - That's a good question. We don't know necessarily that other insects don't taste the pesticides, so that actually could be one potential deterrent effect of the pesticide, for example. We would expect that they should taste bitter to a bee. So if you put something bitter in the nectar, it might make the nectar taste bad. And so if the bee has a mechanism for detecting it, then they might avoid drinking that nectar altogether.
Chris - And obviously if they were able to learn to avoid it in that way, that would be good because it would argue that we can worry a bit less about using pesticides and not taking down our friendly pollinators in the process?
Rachel - Absolutely. So one of the crops that these pesticides are used on is oil seed rape, and this crop actually does not require insect pollination. It fares a little bit better when there are insect pollinators present, but it's not required. So if bees could taste the pesticide and the nectar and then just choose to forage on other food sources, other flowers that were not laced with these pesticides, then this would really be very protective for the bees.
Chris - How did you test it then? How did you try to find out whether they can detect these pesticides?
Rachel - It's not so easy to ask a bee whether or not it can taste something. So one of the ways that we do this is actually by recording from the taste buds. So on insects they also have a tongue and the tongue has various components to it rather than there just being one tongue. They have various mouth parts and these mouth parts are covered in what are called sensilla. So these are like the bees taste buds and we can record from individual sensilla and sort of test whether or not the responses are different when you just have a sugar solution or if you have a sugar solution that contains a pesticide.
Chris - Do they have different taste buds detecting different tastes? So how do you know you are recording from the right one or does one taste bud do everything?
Rachel - That's a really great question as well. So the taste bud itself or the sensillum itself will contain several different neurons. And then each neuron is thought to respond to one type of taste sense. But they use all potentially all of the neurons inside of these sensilla to taste sugars. So they're tasting sugar in a really, really specialised and intricate way. And we tested a whole bunch of different sensilla over different mouth parts so we're not just zooming in on one single taste bud but rather taking a sample from across the the mouth parts.
Chris - What do you do then dunk the sensilla in a sugar solution which has or hasn't got pesticide in it and see if the nerves fire off?
Rachel - Yeah, pretty much. So we make these little electrodes out of these very fine glass tubes and the glass tube can then be filled with whatever we want them to taste. So whether it's the sugar solution or the sugar solution containing the pesticide and then we put an electrode inside one end of that tube and the other end, the sharp end of the tube, we put it just over top of the sensillum so then we can both stimulate the sensillum using the sugar solution that's inside of the capillary and record the electrical activity of the neurons at the same time.
Chris - And did you make sure that the concentration of pesticide that you were putting in there was kind of relevant to what a bee would encounter for real in the environment?
Rachel - Yes, absolutely. So we used quite a broad range of pesticides across all of the sort of measured environmental field levels. We also tried a really high concentration just to kind of have, you know, another, another point of comparison because we thought well maybe they can't taste the really low ones but surely they can taste this really high concentration.
Chris - So you covered all those bases. Did they respond though? Did you get activity changes from the sensillum when you did this proving the bees could taste these pesticides?
Rachel - Sadly, no. It seems as though across the whole range of potential field-relevant concentrations and as well this very high concentration of pesticides, the responses were essentially the same whether we stimulated with just the sugar solution or the sugar solution plus the insecticides.
Chris - So bees cannot taste these pesticides. That would be your conclusion?
Rachel - That's the conclusion, yes. And we also tested this using behaviour to see if well maybe they have a different kind of mechanism or maybe we're not going after the right sensilla, you know, just to see is there any concentration that they will avoid drinking. So we, we also came out at it from the, the aspect of behaviour
Chris - And what are the implications then? Does this mean that bees are basically gonna go and forage from fields that have been sprayed and they're gonna potentially poison themselves?
Rachel - Yes, yes, exactly. So this is the implication if, if they won't avoid drinking the pesticide-laced nectar and they don't seem to really get the kind of what we call post ingestive feedback. So this is, you know, if you eat something and a couple hours later you feel really sick, you'll probably associate that with whatever the last thing was that you ate. This kind of post ingestive feedback is, is another way that bees can associate something negative with what they're feeding on. And, unfortunately, we find that when we give them this window of time in which to feed on the solution and then potentially react also to these post ingestive feedback mechanisms, they still don't avoid drinking the solution. So it's really quite concerning because a bee foraging in the field during its foraging bout will not get sufficient information from what it's feeding on in order to stop feeding on it and you know, avoid coming back there again.
08:18 - Sea anemone stinging strategy
Sea anemone stinging strategy
Lily He, Harvard University
Some sea anemones are predators: they lash out selectively with venomous harpoons to grab morsels to eat. Other species, though, are less discriminating: they’re more like a stinging nettle, and they envenomate anything that comes within stinging distance. One strategy better suits an exposed animal that wants to ward off everything, while the other approach rewards a species where predation is less of a problem and conserving energy is what matters most. And, speaking with Chris Smith, Lily He, from Harvard University, has worked out how - and why - both approaches are achieved...
Lily - The stinging cells have a really large organelle that actually takes up most of the cell's composition. And that stinging organelle is called a nematocyst. It has a stinging barb that is inverted and coiled inside that cyst. And then when there are changes in osmotic or hydrostatic pressure within that cyst, the stinging tube can actually shoot out at a really fast rate. It actually can penetrate things like shrimp or predators.
Chris - They're essentially then cell-sized hypodermics?
Lily - Yeah, that's a really good analogy for it! Yes.
Chris - And how might the animal's strategy of using them differ then?
Lily - So that was actually part of our study here where we looked at a couple different anemones. And these two different anemones are evolutionarily highly related. But they can have very different behaviour. And so like for example, one type of anemone requires both like a touch and like a chemical signal simultaneously - both signals - to be able to sting. And then the other anemone actually only requires like a touch signal to be able to sting. We looked at these two different animals and did some mathematical modeling and were able to find that for one of the anemones - the one that requires both that touch and chemical stimulus or signals to be able to sting - is primarily stinging for predation in the sense that they're mostly stinging things that they would eat; whereas the other species of anemone would be primarily stinging for self-defense. So it would be stinging things like butterflyfish or any animal that's trying to eat it.
Chris - And have you got a feel or did you manage to find out how that distinction is achieved? So the predatory species only discharges when both the chemical stimulus and the touch stimulus are present, whereas the other one is more indiscriminate, it's just defending itself. Did you manage to find out what the physiological basis of that discrimination is?
Lily - Our current hypothesis is that there is a certain type of protein that's found in both types of anemones but there are differences. And so what we found was that in one species this protein generally serves as sort of like a gate for sort of mediating these signals. And so in the case of that predatory anemone, that protein is serving as sort of a gate or a filter. And so it only is activated in the case of those simultaneous chemical and touch signals. And then in the other case that anemone that's primarily stinging for defensive purposes or self-defense that anemone uses a different variation of that protein that isn't as sensitive to chemical signals. And so it is essentially able to be activated upon just a touch signal.
Chris - Would it be possible to swap 'em round - the particular protein you're referring to - between the two and then demonstrate you get the reverse behaviour?
Lily - Yeah, we would've loved to do that. That was a dream experiment to be able to knock down or deactivate production of the protein in the predatory anemone and then have that predatory anemone somehow be able to produce or express the protein that's found in the anemone that's stinging primarily for defense. But, unfortunately, it wasn't necessarily practical to do those experiments. Some of the current genetic manipulations that are required for that are actually not really like fully developed at this point.
Chris - So work for another day then to, to follow that one up. Mm-Hmm. <Affirmative>, does it fit or can you pull together the evolutionary path by which these individual creatures have arrived at the strategy they've got? Does it fit with where we find them, their hunting strategy, which presumably it does, and how they came by this particular adaptation?
Lily - That anemone that's primarily predatory it actually usually buries itself in the mud or sand and really only has its tentacles, which is where all the stinging cells are exposed in the environment. And so it has a very different lifestyle from the other anemone, which stings primarily for defense. And that other anemone is usually exposed to the environment doesn't necessarily hide or bury itself because it actually has these algal endosymbionts, so that means that these algae live inside the anemones tissues and provide actually most of the nutrients for the animal. And so the animal needs to provide some sort of protection for the algae. And in turn the algae provide a lot of nutrients for the animal. And we sort of hypothesise that the algae is providing enough nutrients so that this animal can actually have essentially less discriminate stinging. And that's largely driven by the idea that the animals that sting for mostly for defense do not have sort of as high of an energy barrier to producing new stinging cells.
14:32 - CD133: A new way for cells to share molecules
CD133: A new way for cells to share molecules
Gen-Sheng Feng, University of California San Diego
One of the masters of regeneration in the human body is the liver. It’s so good at it, that if you cut out 80% of someone’s liver, they’ll grow a new one from what’s left. In fact surgeons take advantage of this quite often when carrying so-called “living” liver transplants. We know why it does this: it’s frequently injured by all the toxins we ingest, including alcohol. But how does it do it? About 10 years ago, team at UCSD thought they had the answer in a gene that, knocked out, seemed to disable liver regeneration, at least in the dish. But when they looked in vivo, Gen-Sheng Feng and his colleagues were surprised to see that regeneration was still taking place, albeit slowly, and the regenerating cells all formed in clusters. They’ve now looked a bit more closely, and made a potentially staggering discovery: a protein called CD133 appears to be forming small bubble-like vesicles inside - and crucially between - the regenerating cells. He thinks this might be a new way that cells can share limited resources. In this instance, some compensatory growth signal is spreading through the clusters. But the bigger picture is that this same molecule is also active in cancer cells. So, as he explains to Chris Smith, is this also how tumour populations operate, and even become drug resistant?
Gen-Sheng - Some of these cells can still proliferate without that gene. So means what? By knocking out that gene, we found the liver regeneration was impaired, delayed but not completely blocked. It can still finish or complete the liver regeneration, although the time lapse was longer. So we want to understand why these cells can do without the important gene.
Chris - Do you think that's because there's something making up for the absence of that gene in some cells or do you think something else is going on?
Gen-Sheng - Yeah, that's so called compensatory mechanism, right. So in dissecting that mechanism, we found that in the gene knockout liver, these dividing liver cells will all form clusters in the liver, When we dissect the liver section to look at specifically. So at the beginning we thought these cells must be derived from, so-called progenitor cells or stem cell. But then with that hypothesis, we searched for a lot of biomarkers for stem cell or progenitor cells. Indeed. But we only found CD133 in these dividing cells. These dividing cells are actually negative for all the other progenitor cell markers that we screened and eventually we found that these are mature liver cells. They are not progenitor cells, not stem cells. So that led us to dig into a new field and eventually we found that actually CD133 labels a vesicle that these cells produce in response to the deficiency of cell division.
Chris - So let's unpack that a bit then. You knocked out what you thought was the linchpin behind regeneration and were quite surprised then to see that some liver cells limp along and managed to regenerate anyway and they're all in bunches in clusters. So you thought, aha, there must be some kind of stem cell that's doing that, but you couldn't find any evidence it was a stem cell. They all looked like grownup mature cells, except they did have this magic marker CD133 MM-Hmm <affirmative>. And you are saying this unlocks some special new field. What's the CD133 doing then?
Gen-Sheng - CD133 is a cell surface protein. It has five transmembrane domains. But how CD133 functions in stem cell or non stem cells is not clear no matter how and nobody knows what's the function of CD133, how it regulates, even if it's important. Right. And we found actually CD133 labelled vesicles in many cases inside the cell. More importantly, we found at the low resolution microscope CD133 labelled bridges between these dividing cells. So that's led us to hypothesise that CD133 may mediate a new mechanism of cell cell communication.
Chris - Goodness. So you are saying this molecule, which is sometimes on cell surfaces, in your hands in these experiments ended up around little packets inside the cells and occasionally you could see threads connecting the cells. Mm-Hmm. <Affirmative>. Mm-Hmm. <Affirmative>. So there's like a portal being opened up between adjacent cells. Is that a physical connection? Can things go between cells down those connections then?
Gen-Sheng - Yes. That's a great question. We presented some data but not sufficient. We need to do further experiment to demonstrate that this vesicle is indeed migrating between cells, so letting cells share materials, for example messenger RNAs and the proteins that are required for cell proliferation. That's what we are still working on.
Chris - So your hypothesis then is the reason that some of these cells regenerate is because mm-Hmm, <affirmative>, they've got enough, even though there's a knockout of the particular linchpin gene, there is some compensatory growth mechanism which is being shared by these cells and it's enabling them to grow nonetheless. And that's why you see these clusters of cells connected together in this way using this new mechanism you've identified, possibly mediated by this CD133 conduit as it were to share resources between the cells?
Gen-Sheng - Yes, actually we do have evidence that demonstrate these deficient cell missing different material like this cell missing A, another cell missing B. So if they mutually share, then they are not missing A or B, they have all the material that are essential. So that's why I think we discovered a new function of CD133, and why this is so important.
Chris - CD133 has had the finger pointed at it in a number of different settings, particularly as a cancer stem cell marker or a progenitor marker. Do you think then, this is partly how cancer cells work as well. Are they sharing growth resources or compensating for some genetic lesions that mean that the cancers grow robustly and even develop resistance against chemotherapy by using things like CD133 in order to reinforce the cancer as a population of cells?
Gen-Sheng - Indeed, that's a real question and the issue that make us excited about this discovery, because cancer stem cell are a new concept in the cancer research field, but there are disagreements about this concept or data. There are indeed controversial data about the existence of cancer stem cell. However, there is a very good evidence to correlate the CD133 expression and the tumour recurrence. So with our data now we can explain all the controversy, I believe, because once you have the compensatory mechanism mediated by CD133 positive vesicles turned on, they will become resistant to the drugs and that will lead to tumour recurrence. So this kind of recurrence does not need new mutation in cancer cells. So that's why I think this will be a very quick mechanism to develop drug resistance and therefore cancer recurrence.
22:30 - How quickly do plants replace melting glaciers?
How quickly do plants replace melting glaciers?
David Harning, University of Colorado, Boulder
Climate change means the world is warming, and one very visible manifestation of that is the retreat of glaciers and ice-sheets. But how rapidly will they disappear, and how long will plants take to reclaim the naked ground revealed as they go? This matters not just for aesthetic and biological reasons but because plants also alter the energy balance of the land they grow on, and that in turn alters the temperature and therefore the pace of further deglaciation: data that could prove very valuable for climate and other models. And although we often describe the present circumstances as unprecedented, the Earth has been through many warm spells in the past, which means there is already a template laid down in the geological record for how this tends to happen. And the key is DNA from ancient species trapped in ancient lake sediments. Speaking with Chris Smith, David Harning…
David - One particular question is, what happens when ice sheets recede? And how quickly do plants come in and colonise those areas? This is a really important question for understanding large scale energy balance of the earth. So ice sheets reflect energy that comes from the sun back to space; whereas plants absorb that energy. So you can imagine if energy's being reflected back, that's keeping the planet relatively cool, versus if plants are there absorbing it, that's gonna keep it relatively warm. So sort of like sitting in a car in the middle of the summer if the seats are black.
Chris - What can you study to give you insights though? Because obviously we're not seeing this other than in real time at the moment. So how do you go back in time to look at this?
David - We look at past sedimentary records. So in particular we go to lakes where mud that is comprised of all the living material in and around the lake at any given time. When that organic material dies, it sinks to the bottom of the lake and it accumulates, layer by layer. So the deeper you go down into the lake, the further back in time you go. And we've just identified a number of places in the northern hemisphere where glaciers are present and being able to address the question we're after about plants replacing glaciers at high latitudes, these go back to the last glaciation 10,000, 12,000 years ago. To identify basically what's there, you can use a number of available tools which we call proxies. So proxies for a past environment or a past climate state. And in particular in this study we use DNA, so DNA that is being produced by plants living in and around the lake. And just as I said before, when that material dies, it goes to the bottom of the lake and old DNA is preserved, see which plant was actually growing there. And then if you have a nice way to date your lake sediment, so be able to say like, well, this step was 5,000 years ago and this step below that, it's 10,000 years ago; you can actually say when certain plants were there and maybe when they weren't.
Chris - So the DNA tells you who's around? Mm-Hmm. The mm-Hmm. <Affirmative> dating of the mud via various methods can tell you who is around when. So how do you know what the climate was doing at each of those time points?
David - One of the major things that we use in our group is looking at the molecular structure of lipids or fats produced by bacteria and algae. A great example is if you have a plate of margarine and a plate of butter, both at cold temperature, so you stick 'em both in the fridge, you take 'em out. Butter is really, really hard to spread. Margarine is really easy to spread, and that has to do with number of double bonds or unsaturations in the actual chemical structure of those fats. So just the same way that those saturations have been modified by humans in margarine, different animals, different bacteria, different algae, they also adjust their saturations at a cellular level in the membranes to adapt to that environmental temperature. And by extracting and looking at these molecules, or we know who's producing them through time, we can use that, the changes in the saturations of the molecules to actually reconstruct temperature.
Chris - And when you do that, what picture emerges of how the plants do come back and, and recover or recolonise a previously glacial area? And is it just random or are there specific founder species that come in as pioneers first and then they're replaced? What does the picture look like?
David - Yeah, so there are pioneer species first. Those are often grasses, which, you know, can establish and root themselves in pretty desolate landscapes. So you imagine, you know, after an ice sheet retreats, there's really nothing there. It's a fresh slate, if you will, minimal soil development. So there's minimal nutrients available for the plants. So there's plants that are adapted to that low nutrient landscape. And then as those pioneer species establish themselves, the soil begins to develop organic content increases, nutrients increase, the soil becomes richer and more mature. And that allows plants that require that richer soil to move in. And many of those plants are actually influenced by the temperature.
Chris - And going back to the temperature effect of plants versus ice, what is this now revealing to you about how the dynamics of that work?
David - As you can imagine, plants absorb more energy than the ice. So that will actually elevate the temperatures more than what they would be otherwise if the plants weren't there. And going back to the original question about trying to understand the pace of plant colonisation, when ice retreats, it's generally been assumed to be very rapid. All these plants move in very quickly, particularly the woody taxa. So trees that really are absorbing a lot more energy, say than grasses. What we found in our study was a little different, that the trees, their arrival was spread out over several thousand years versus all of them coming in together. And this suggests that where ice sheets are currently retreating, such as in Greenland and Antarctica, the migration of these woody plants in particular may not be so quick. So as temperatures continue to rise and the ice sheets melt, and that's replaced with these higher energy absorbing plants, the warming may dampen the ultimate magnitude of future warming. So it may not be as rapid.
29:17 - How albatrosses get airborne at sea
How albatrosses get airborne at sea
Leo Uesaka, University of Tokyo
Wandering albatrosses are one of the farthest-flying birds on Earth; some studies estimate that certain individuals may circumnavigate the southern ocean multiple times each year, covering over 100,000 kilometres in the process. Some of that flying prowess is down to their huge wingspan and ability to soar on air currents to stay aloft with relatively little effort. But they do have to descend periodically to land on the ocean surface to feed, and how they get airborne again is more of a mystery. Now, thanks to the University of Tokyo’s Leo Uesaka, we have a better idea. As he explains to Chris Smith, by equipping the birds with monitoring backpacks to track their trajectories he’s been able to show that they use the prevailing wind, and waves, to launch themselves back up into the air…
Leo - Albatross is known as largest seabird on earth. Its wingspan actually reach like three metres or more. So they can fly very efficiently. They usually use the ocean winds to fly.
Chris - That's a lot isn't it? Because we think pterosaurs, way back at the time of the dinosaurs, they had an 11 metre wingspan. Mm-Hmm <affirmative>. But three metres is still very, very large. Yeah. How much does an albatross weigh?
Leo - It's about nine kilograms to 11 kilograms.
Chris - And where are they distributed?
Leo - They're usually distributed around the Indian ocean or we call the sub Antarctic area like 30 to 50 degrees south.
Chris - And do they spend their entire life at sea or do they have periods when they come towards land? What's their average year?
Leo - They breed once in a year around the Indian oceans island.
Chris - And what was the unknown then that you felt that this study was able to address?
Leo - We don't know how their fine scale behaviour like taking off is affected by ocean environment.
Chris - Presumably - because they eat fish, don't they? - presumably there are gonna be periods when they have to come down to the water and land Yeah. Yes. To, to catch their prey and then they've got a problem of taking off again. And so yeah. Is is that one of the issues then that we need to understand that a bit better?
Leo - Yeah, taking off is quite energy consuming behaviour for albatrosses. So we need to find how the taking off effort change along the changing environment.
Chris - How did you do that?
Leo - We tagged small devices on albatrosses and tracked their motion and we also estimated their surrounding environment like winds and waves from their motion records.
Chris - How did you get the devices on the albatrosses in the first place? Did you have to go out to sea to do that?
Leo - We attached the small tags on their backs using a waterproof tape and recapture it again. And recover the tags.
Chris - And those tags. What data do they collect?
Leo - We mainly use the GPS data and acceleration data in this study.
Chris - And what was the question you were asking?
Leo - Well, my question is how severe weather they experience when they take off from the sea surface and how the takeoff effort change in the various environment. Like if the wave is quite high, how the albatros is taking off efforts changed.
Chris - And how did that then enable you to form a picture of what their behaviour is under these different environmental conditions?
Leo - They're taking off effort actually decreased under a high wave condition or windy wave condition. And only when wind and waves are quite gentle, their takeoff effort increased. Wind and wave helps their taking off.
Chris - When a pilot takes off in an aircraft, they point into the wind if they can to get more wind over their wings and more lift. Do the birds do the same, do they use the ambient conditions to help them?
Leo - Yeah, we also find that they always take off into the wind so that they can get enough lift force.
Chris - I can understand why the wind helps them get airborne, but why does wave action help as well? Is it literally because they're higher off the water at certain points and so they've got almost a launch pad?
Leo - I still don't have any clear explanation and any clue, but I, we, we guess that a higher wave condition makes a complicated wind condition right over the ocean surface and the complicated wind condition may help the albatross in taking off, even in very weak wind condition.