Extraordinary creatures: hummingbirds Free

Doug Altshuler, could tell me what you find most interesting about hummingbirds and what makes them different from other birds?

DA: I think it all comes down to hovering. Flight, in general, is such an extraordinary adaptation of animals. And it's extraordinary because it has required a radical transformation of so many of their systems, including their physiology, neurobiology and anatomy. We see these extraordinary features whether we're looking at fruit flies, dragonflies, bats, pterosaurs or, of course, birds. You then have this one animal that is the only bird that's capable of sustained hovering flight. And what I mean by that is that hummingbirds can hover for a long time without the assistance of background air flow to keep them in place. It's not a momentary behaviour that they can just muscle through; they can actually sustain it.

What do hummingbirds do that allows them to hover that other birds do not?

DA: It's all about the ability to produce force. And hummingbirds are really adept at producing and controlling force with their wings. They're able to produce force on both the upstroke and the downstroke. So they really have exquisite control over the magnitude, time course and direction of the forces they produce. They have to produce enough upward force to overcome the force of their body weight pulling them down. So basically, they have to balance that force. They're generating exactly their body weight in upward force – then they can hover.

How fast do they need to beat their wings to stop themselves bobbing up and down?

DA: It depends on the species, but in routine hovering for Anna's hummingbirds (the birds we now work with most often), it's around 40 to 45 beats s⁻¹. When I was a PhD student, I did some work with the giant hummingbird down in South America. I think the lowest wingbeat frequency I got was 11 or 12 beats s⁻¹. Rufus hummingbirds are often beating their wings during hovering at around 60 beats s⁻¹. The world's smallest hummingbird is the Cuban bee hummingbird; I don't think anyone has yet measured its wingbeat frequency, but I think Chris Clark (University of California, Riverside) has done some estimations and is pretty sure it can get up to about 80 beats s⁻¹ during routine hovering.

What allows them to be so manoeuvrable?

DA: There really is no one measure of manoeuvrability. It really makes the most sense if you can break it down into different types of manoeuvrability, so things like accelerating in a straight line or a banking turn, or a type of pivot turn that a lot of flying animals do. The way hummingbirds sometimes turn is they'll be flying along, and then slow down and lean back and then turn and go in a different direction. This is an example of a pivot turn. Once you have these different features of manoeuvrability, you also need some performance measures for them. For example, what is the highest acceleration the birds can do in a straight line, or how much time does it take to make the turn? Once the manoeuvres are broken down into different components, you can then measure features of those different components. What we found is that there's actually a relatively small number of attributes that seem to best explain how good a hummingbird will be at each manoeuvring feature. The thing that explains many aspects of their manoeuvrability is the amount of muscle force that they can generate quickly. We measure that using a method called load lifting that I learned from Peng Chai and Robert Dudley (University of California, Berkeley). We put a small harness around a hummingbird, and then attach it to a chain of colour-coded weights. When we put a hummingbird on the floor of the flight chamber, their natural escape response is to take off. So, they take off and up, and as they fly up, they're lifting progressively more weight. We know how much weight is left on the ground, and therefore, by subtraction, how much weight they are lifting. It turns out that how much they can briefly lift explains many aspects of their manoeuvrability.

Can you tell me what's happening in the brain as they're flying? What are they sensing?

DA: The easiest way to actually explain that intuitively is in terms of behaviour. When they're hovering, they're trying to hold their position by stabilising the environment. There's a well-known stabilisation response that we do with our eyes, called the optokinetic response, or optokinetic nystagmus. If you are viewing a screen with moving dots or bars, your eyes will involuntarily track them and then shift back and track them and shift back. There's a version of that that we do with our neck and shoulders as well, called the optomotor response. Hummingbirds essentially do an optomotor response during hovering. They're trying to stabilise their environment. They're intending to be hovering, so if they observe their whole environment moving – a visual signal called optic flow – they interpret that as if they're drifting out of place and will try and stabilise it. During forward flight they don't use the same strategy. In forward flight, they're expecting to see optic flow due their own voluntary movement. Imagine you're driving through a city; your environment is moving around you as you're going along. That would be totally normal. If you tried to stabilise that, you would just stop moving, right? So, hummingbirds have to use a different type of strategy in forward flight. What hummingbirds do is they generate a prediction of how the world should look as they move through it. It's called a forward model because it's a prediction. So, they give themselves a prediction of their forward velocity. And if there's a mismatch, they stop and try to make a new model before moving on.

Ken Welch, in your opinion what are the most intriguing aspects of hummingbird physiology other than hovering flight?

KW: I'd say very much intertwined with that is their amazing metabolism and their ability to process energy, fat and sugar to make that energy-intensive flight possible. The two are linked in the physiology of the bird, being the link between muscle activity and the ability to consume energy and turn that into ATP and muscle work, and are also intimately tied to the diet and to their coevolution with the flowers that they pollinate.

So, their flight abilities allow them to eat what they do?

KW: Yeah. I mean, you don't get one without the other. You don't get a hummingbird that can hover without it being an animal that is intimately tied to the plants that it forages on. They hover, they sustain that with sugar, and then they need to go sit and absorb the sugar that they get from their nectar meals to power the next foraging bout. And then at the same time, many species can turn around and migrate long distances, particularly the North American species that we have here in Canada and in the USA. Many of them are long distance migrants and can power flights of perhaps several 100 km burning, it seems, only fat. So, this flexibility to live on basically Coke all day long, and then turn around and over a day or two, complete a migratory flight, running just on fat is really, really impressive considering the differences in the metabolic pathways involved using those fuel sources.

How do hummingbirds manage to survive only on nectar?

KW: The answer is they don't survive only on nectar. Nectar is just too poor in micronutrients and other essential nutrients. You need your amino acids and your vitamins, and nectar provides very little of that. Certainly, hummingbirds either intentionally, or more likely unintentionally, ingest some pollen as they're shuttling it from flower to flower, and that does provide some important amino acids. But we also know that hummingbirds regularly feed on small arthropods and small insects. They will catch small flies in mid-flight, like Daniel LaRusso in the Karate Kid, catching the fly with the chopsticks. They are also uniquely well suited to plucking spiders right off their webs, which they will do as well. They even use the spider silk to build their nests. They eat insects almost every day. They can go a few days without much nitrogen intake, but they do need that little bit that they rely on. And at certain times of the year, particularly when the migratory species are first arriving in their more temperate breeding grounds, flowering might not be very strong yet in those areas in the early spring, and insects that are abundant at that time may become a more important component of their diet. So, they definitely show flexibility and the ability to, at least temporarily, become much more omnivorous. That said, we know that in an average day, a hummingbird is consuming many times its body weight in floral nectar. So, most of the time 90% or more of their calories in a given day is coming in the form of nectar.

If they're eating multiple times their body weight per day and yet not becoming multiple times their body weight per day, where is all that food going?

KW: Well, the key thing to remember is that the floral nectar that they're feeding on is a relatively dilute solution of sugar water. It's about 20% or so sugar to water by volume, if you want to measure it that way. That means that the vast majority of what they're taking in is water, and so hummingbirds, unsurprisingly, have kidneys that are not very good at concentrating their urine. You don't need to concentrate when you are drinking as much as hummingbirds are drinking in a typical day. So, hummingbirds pee all the time. And in fact, every time they go out on a foraging bout, they come back and sit, and they will inevitably pee a short time later. There's a very rapid need to get that water out of their system so that they don't become bloated and too heavy to fly.

How many calories do they need to consume in a day?

KW: One example I'll give is that some of the small hummingbirds that we have here in North America, e.g. Anna's hummingbird and the ruby throated hummingbird, exhibit metabolic rates during hovering that are 10 to 15 times higher than an elite marathoner can sustain if you take their different weights into account. That's an incredible amount of aerobic metabolism in terms of the amount of sugar – the glucose or fructose – it takes to sustain hovering. If you were to make a hummingbird as large as a healthy adult male human, 70–75 kg, you would basically have to drink a 16-ounce bottle of Coke every minute and be burning those calories in real time. Estimates of their metabolic rate in the wild by Don Powers (George Fox University, USA) back in the 1980s are about 32 kJ per day for wild Anna's hummingbirds. That's about 7.6 kilocalories per day, and humans need about 2000. But we are 17,100 times heavier, so a human-sized hummingbird would need to eat 130,000 kilocalories per day. That's 65 times the amount that's recommended.

How do they get the nectar from flowers?

KW: For flowers, or for your backyard hummingbird feeder, the hummingbird is going to insert that long bill – or that long curved bill if it's one of the species that has the curved bill that seems to have co evolved with those Heliconia flowers with a very curved shape to the nectary – into the flower. The hummingbird's tongue is very, very different from many other birds’ tongues, and it's really cool – the base of the tongue actually wraps up around behind the skull. And there are muscles sitting on the skull that are helping to power the movement of the hummingbird tongue to slide out between the two bills, which are opened not much more than is necessary to accommodate the tongue. The tongue plunges through the meniscus and into the nectar. And the end of the hummingbird tongue is forked – the forks are like towels rolled along the long axis of the tongue, parallel to the tongue at the end. When these enter the nectar, the rolls open up and nectar flows in. And that surface tension also helps to wick that up the grooves in the tongue. That bolus of nectar that has been wicked up the tongue and has been collected in the trap (the fluid trap at the end of the tongue) then, as it leaves, is retracted from the pool of nectar at the bottom of the flower or at the bottom of your hummingbird feeder. The hummingbird pulls its tongue back up and its bills open a bit wider to accommodate the plumper tongue, which has got this fluid attached to it. So, the next extension of the tongue out with the bill closed a bit more helps to basically remove some of the nectar from the tongue. The hummingbird tongue goes in and out 14 times per second.

Has bird flu affected the hummingbirds you work with at all?

KW: Certainly there have been concerns now because of bird flu, and we had to adopt a quarantine for our birds that we captured this last year, though I would have considered it remarkable for anyone to be able to capture a hummingbird infected with H5N1, because, from my experience, whenever a hummingbird does become infected with something, the progression is so rapid that they're 24 h from being a dead bird.

Other birds don't get sick and pass away so quickly do they? Could it be related to their fast metabolism?

KW: I think that's part of it, and it's also size. I mean, the birds that I've heard about in the news recently that are caught alive and are tested and found to have H5N1 tend to be the larger birds, like geese. Because hummingbirds feed at feeders, if a sick bird fed at that feeder, there's great reason to worry that that could be a potential spreading event, the same way that backyard bird feeders filled with seeds are also potential places where sick animals can come together. And it's not practical to try and police feeders, etc. It's certainly the case that if you take away that supplemental food, you're likely to cause immunological stress, certainly metabolic stress, that can lead to immunological stress in all those populations too.

What are you hoping to learn next about hummingbirds?

KW: Well, a lot of what I've been interested in most recently has been how they're processing sugars, not just the glucose. To some extent, at least, there's a limit to that blood glucose use anyway, but unlike in us, where fructose has historically been more of an irregular treat, fructose is a daily component of their diet. It's about 50% of the calories they take in. Nectar typically has an equal mix of glucose and fructose, and we know from metabolomics studies we've done in my lab that circulating levels of both glucose and fructose spike to values that are 3 times higher than someone having an acute diabetic episode, and that's normal blood glucose for them. Blood fructose is typically much lower in our circulating blood because it's effectively pulled out of circulation by our kidneys and doesn't ever get to escape. Your liver and your kidneys express the transporters that can take up the fructose, but before we can use the energy in the fructose, we need to turn it into something else – like glucose ­– which is sent back out into the bloodstream. But in hummingbirds, their muscles regularly see blood fructose levels in the several millimolar range, which is at least 1000 times higher than you see in the average human. It begs the question, what are their muscle cells actually utilizing for fuel? Are they directly burning fructose taken up from the blood? Well, unlike in us, the glucose transporter protein that is known to transport fructose is expressed at similar levels in the muscle and heart as they are in the hummingbird liver and kidneys, which is where we express them. So, unlike in humans, it seems like the hummingbirds have the transporters to import fructose into their cells and see circulating fructose levels that are high enough to support the high rates of uptake into the cells. So, what's going on in the cell? I would love to get that answer, and to figure out, are these guys actually using fructose in their muscles in real time to fuel metabolism? And more importantly, what in the world comes with high fructose levels like this?

Doug Altshuler and Ken Welch were interviewed by Jarren Kay. The interviews have been edited and condensed with the interviewee's approval.