It’s time to lift the veil and take a peek at the “man behind the curtain.” Within the realm of biology, that could mean a lot of things, but in this instance, I’m referring to parasites. Huh? The great and powerful Wizard of Oz is a parasite? Just bear with me and this will all make sense by the end of the post.
Up to this point in the blog I’ve kind of danced around the margins of this hidden world; there’s some fun discussion of “feathered tree ticks” and kleptoparasites in the post from last March, and I devoted an entire post to brood parasites a few months ago. But parasites and pathogens (which I’ll just combine into “parasites” for simplicity) play an enormous, if underappreciated and often inconspicuous, role in the natural world. And that’s not simply the case because of the SARS-CoV-2 (coronavirus) pandemic. Parasites impact the length and structure of food chains, they can control host populations (by keeping them from growing too large), they galvanized the evolution of one of the most complex physiological systems in nature (the vertebrate immune system), and parasites may be responsible for the evolution of elaborate sexual displays (think of a scarlet tanager’s bright red plumage), as well as the evolution of sexual reproduction. Oh, and they likely make up more than half of the species on our planet. So yeah, (as my wife, the disease ecologist, reminds me constantly) they’re kind of a big deal.
One of the first tasks to studying parasites in nature is defining what exactly a parasite is. To do this, we can use some ecological criteria. First, a parasite is an organism that is in an intimate (close proximity) and durable (long-term) relationship with another organism (insert marriage jokes here). That is, they are symbionts. But there are many organisms in intimate and durable relationships with other organisms that are not considered parasitic. Corals and their algal symbionts, and anemones and their attending anemonefish (Nemo) are in intimate and durable relationships, but each has a positive effect on the other. Therefore, they are considered mutualists. A parasite exists in an intimate and durable relationship with another organism upon which it exerts a negative effect. What does a negative effect mean in ecology? Essentially, it means that the parasite creates some sort of a cost for the host, usually in the form of energy loss and often manifesting as reduced reproduction, disease, and in some cases, death. The impact of the parasite isn’t always huge, but the net effect needs to be negative. Is a lion eating a gazelle a parasite? Well, it’s intimate and it’s definitely negative, but it’s not durable. The lion kills the gazelle and uses its resources, but the interaction is short-lived and the act of energy transfer is relatively quick. This interaction is, of course, known as predation.
What about a mosquito drawing a blood meal from a person? Are they ‘parasitizing’ us? They are stealing our resources, it’s pretty intimate (the proboscis is literally penetrating our skin), but it’s still not durable. They are considered to be ‘micro-predators’ on us. Ticks, on the other hand, attach to the host for a few days while procuring their blood meal, which is generally long enough to bump them into the true parasite category.
Ticks fall under the group of parasites known as ectoparasites, meaning “outside parasites,” and ectoparasites are any parasitic organisms found on the external parts of their host. In addition to ticks, this group includes some very popular members such as lice, fleas, and mites, to name a few. These parasites usually draw their energy from small blood meals, but they can also consume various parts of the host’s integument (i.e. skin, hair, feathers, scales). Feather lice, for example, consume parts of a bird’s feathers, but the award for most bizarre and extreme form of ectoparasitism has to go to Cymothoa exigua: the tongue-eating isopod. Yep, there’s a parasite that attaches to the host’s tongue, and slowly consumes it. Except, it doesn’t just consume the host’s tongue (and don’t worry—the host is always a fish. So far…); it replaces the tongue. With itself. This may be more information that you ever wanted to know about fish and their tongue-stealing parasites, but it’s extraordinary. By assuming the functional role of the tongue, the parasitic isopod allows the fish to continue eating normally (more or less), thereby ensuring that its home and source of food (the fish) remains relatively healthy.
The other major group of parasites are the endoparasites, or the “inside parasites.” This category includes everything from intestinal worms like tapeworms, to intracellular protists like malaria. Typically, it’s the intracellular parasites that are the most problematic for the host, and are the hardest for the immune system to kill (hiding inside the cells of the host is a pretty good way to avoid detection).
Within the world of parasitology, one of the big questions is: how does the parasite infect a new host? There are few primary ways in which parasites can get to a new host: direct transmission (an infected host touching an uninfected host and transferring the parasite that way); indirect transmission (an infected host contaminating the environment with infective agents that another host can pick-up from the environment); vectored transmission (a biting fly or other biting arthropod carries the parasite from an infected host to an uninfected host); and trophic transmission. And this final form is the one I want to spend some time with.
At its most basic level, trophic transmission simply means that the parasite travels from one host to another by being consumed. Seems pretty straight forward, but let’s take a look at a few examples to get better acquainted. The first example comes from California, but this sort of scenario exists all over the world. The parasite in question is a flatworm; a type of trematode called Euhaplorchis californiensis. The parasite’s lifecycle includes three types of host; a snail is the first host, a fish is the intermediate host, and birds are the definitive host. Ultimately, the parasite wants to wind up in a bird, where it hopes to meet others of its kind and begin reproducing (the bird’s gut is like a singles bar for these worms). But how does the parasite get from a snail to this feathered singles bar?
First, an infected bird poops eggs of the trematode into the salt-water marsh habitat that the snail lives in. The eggs are accidentally consumed by the snail as it grazes on algae (or in some cases the egg hatches in the environment and the snail is infected by a swimming miracidium), and once inside the snail, the next stage of the parasite begins developing in the snail’s gonads. Here, in this large gonadal space, the parasite consumes the host’s reproductive tissue (testes and ovaries) and converts that reproductive matter into the parasite’s next infective stage: the cercariae. The cercariae are released into the water, and these free-swimming, sperm-resembling parasites seek out the next host: a California killifish. Once they’ve found a killifish, they burrow into the tissue, lose their tail, and head for the fish’s head. The parasites are actually looking to encyst on the fish’s brain, where they turn into metacercariae.
Recall that the parasite would very much like to get into the stomach of a bird so it can finish its development and begin sexually reproducing. But the fish has no interest whatsoever in going on this bird-stomach road-trip. Given that the parasite is inside the fish, this would seem like a pretty substantial hurdle for the parasite to overcome. And it is here that the parasite begins pulling its puppet strings. Killifish that are infected with the trematode metacercariae start to act a little differently than their school-mates. They exhibit a suite of behaviors that would seem to be at odds with their goal of blending in with the crowd. They begin swimming closer to the surface of the water, and do more darts, twists and turns than their neighbors. All of these erratic, conspicuous behaviors increase the visibility of the bizarre-acting fish (think Alfredo Linguini being controlled by Remy in the movie Ratatouille) and serve to catch the attention of fish-eating birds in the vicinity. Research by scientists at the University of California, Santa Barbara has shown that infected fish are 10-30 times more likely to be eaten by a bird than uninfected fish. And once inside the bird’s gut, the parasites can again find mates, reproduce, and lay eggs that are dropped into the salt marsh, thus completing the Euhaplorchis circle of life.
But let’s talk a bit more about the cysts on the fish’s brain, and that moment when a large bird comes along and eats a weird-behaving and infected fish. Well, the parasite seems to have gotten its wish, but is this purely a product of an infected fish acting weird because it has a bunch of cysts on its brain (which would be understandable), or is the parasite actually manipulating the behavior of the host in specific ways that increase the probability of getting eaten by a bird? The evidence seems to support the latter. Infected fish have different neurochemical profiles than uninfected fish, specifically with respect to serotonin and dopamine. Both of these hormones are linked to swimming behavior and potentially anti-predator behavior, and by reducing serotonin and increasing dopamine, the parasite may be forcing the fish to behave in ways that increase its chances of getting munched. And that’s how you execute the old “snail to fish to bird” maneuver.
What’s more incredible to me than this instance of host behavior modification, is that there are hundreds, and perhaps thousands of similar, but distinct examples of host manipulation by parasites. Another trophically transmitted parasite is Toxoplasma gondii, which causes toxoplasmosis in humans. The definitive hosts (where the parasite reproduces sexually) for T. gondii are cats; house cats, bobcats, mountain lions, African lions, etc. The intermediate host (and in this system, there’s generally just a first intermediate host and the definitive host) is typically a rodent, although there’s some intriguing evidence to indicate that other animals like raccoons, baboons, and even humans may act as intermediate hosts. We were, after all, lower down on the food chain for many, many years, and probably served as a not-too infrequent source of food for big cats like leopards, lions, and tigers.
In the more typical rodent-cat scenario, the rodent gets infected by ingesting T. gondii cysts from the environment. The challenge for the parasite is now getting from its rodent host to the thing that the rodent host is most likely to avoid; a cat. No problem. All the parasite has to do is convince the rodent that the aroma of cat (especially cat urine) is magnetically alluring, and demands further investigation. Indeed, the parasite has somehow managed to pull off this feat (we aren’t sure how the parasite manipulates the hosts’ behavior in this case), and even makes the rodent more likely to approach any cats that happen to be in the area. Bad for rodent, good for parasite. Once the rodent is consumed, the parasite can mature and begin the sexual reproduction phase of its life in the gut of the cat.
The complete T. gondii story is much more complicated and involves fascinating journeys into human behavior; for one, is the “crazy cat lady” actually infected with T. gondii and exhibiting behavior that might have, at one time, increased the chances of her getting eaten by a leopard? It’s certainly possible, although a bit tricky to test. People can also get infected by eating raw or undercooked meat (prevalence of toxoplasmosis in France, where they really enjoy their steak tartare, used to be upwards of 80% of the population, although it appears to be closer to 50% now), and apparently rodents (and perhaps humans) can transmit the parasite via sexual contact.
Not all behavior manipulation is linked to trophically transmitted parasites. Probably the best known example, and now famous from the Girl with all the Gifts book/movie, is the “zombie-fungus” Ophiocordyceps. This genus is composed of over two hundred different fungi that infect insects and spiders, and hijack their bodies. Unlike the Euhaplorchis-killifish system wherein the parasite seems to be controlling the host by manipulating the brain, the fungus appears to use biochemical compounds to interfere with the host’s nervous system, and then takes direct control of the musculature. In an ant host, the fungus forces the ant to seek out a humid spot (good for fungal development) where the ant will clamp onto the vegetation with its jaws. The ant eventually dies, and a few days later, the fungus bursts from the dead ant, sending out fruiting bodies (spores) that will be scattered by the wind to infect a new host.
If you’ve made it this far without blanching at the subject matter, congratulations! I know it can be uncomfortable to confront this amazing and horrifying world in which seemingly normal organisms are being controlled by hidden agents. And while this may all sound like a bad dream, I can assure you, we’re very much still in Kansas.
Next post: The Other Side of the Coin: Host Immuno-ecology
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There are a few things about birds that everyone knows: they have feathers, most can fly, those that do fly like to poop on people and their cars, they lay eggs, and most of them build nests. If I asked you to picture a bird’s nest, you would probably conjure up images of a small nest built of twigs and grass, with a nice bowl-shape to it. This is called an “open-cup” nest and is the quintessential songbird nest. But this is just the tip of the nest-berg; there are mud-pedestal nests, Dutch-oven nests, nests made of saliva, hanging nests intricately woven from grasses, tree-cavity nests, and giant mound nests made of rotting vegetation.
A nest mound constructed from rotting vegetation, built by an Australia Brushturkey. These birds are in the family Megapodiidae, and all members of this family construct some sort of mound nest in which they deposit their eggs, and then leave them. The rotting vegetation produces heat, which provides the warmth needed for incubation. Photo by D. Cowell.
And each nest type is intimately linked to that bird’s ecology and life history (we’ll return to “life history” later on, but essentially it encompasses the patterns of growth, development, reproduction, and death each species exhibits). If passing your genes on to the next generation is the most important task in an organism’s lifetime To-do list, the nest sits atop the list of essential accessories for most birds.
I think it’s easy to take nests for granted. Ultimately, a nest is just a vessel for holding the eggs and nestlings once they hatch. It’s like Nature’s Easter basket; nobody cares about the basket, they just care about the delicious goodies in the basket. But, depending on the species, nests play an important role in hiding, protecting, insulating, and simply retaining a bird’s most precious possessions. As with almost all other facets of bird biology, evolution has shaped every aspect of nest ecology for birds as well; nest placement, materials used for construction, shape, design, etc. Because all of these components of nesting ecology are the result of selection on behavior, the nest can be considered an extension of the bird’s phenotype (quick primer: the phenotype is the physical representation of the genotype). Richard Dawkins, the famous evolutionary biologist, coined the term “the extended phenotype” (and wrote a book titled the same) to help explain how some things made by organisms, such as bird nests, spider webs, and beaver damns, are the product of the same evolutionary forces that produced bird wings, spider silk, or beaver tails.
To help illustrate the importance of nests, we’ll take a little tour of different nest types to explore how a species’ nest impacts other components of its life.
We’ll start with a nest that is likely familiar to many readers; the nest of the American robin. As illustrated in this time-lapse video, robins typically begin with some loose grass and small twigs, and then build it up using mud as a bonding agent. The inside of the cup is lined with soft, dry grass, and the female uses her body to mold the nest cup into a perfect robin-sized shape.
Some robins begin nesting very early in the spring when nighttime temperatures can drop below freezing. These cold temperatures can be lethal to partially developed eggs or nestlings, and the female has to ensure that the occupants of the nest don’t get too cold. It’s possible that the mud used in the nest acts as a form of insulation. Nests vary considerably in the amount of mud that gets incorporated into the structure, and it’s conceivable that some of this variation is linked to expected air temperatures; nests with more mud should be better insulated from very cold temperatures (as well as very hot temperatures). Robins also prefer to place their nests somewhere that is protected on at least two or three sides. The nest is usually built on a platform of some sort—a thick tree branch, a rock outcrop, on the light fixture above your front door- that also has cover above it. This can be in the form of leaves or other thick vegetation, some natural rock or earthen structure, or the eaves of a house or shed. The robin’s nest-location preferences are driven by two principle factors; protection from the elements, and protection from predators. And despite the importance of protection from the elements, nest-predation is thought to be the number one source of nest failure for most avian species.
So, in addition to placing the nest in a spot where it is protected from inclement weather and from the searching eyes of predators, robins (and, in fact, many open-cup nest species) have relatively short incubation periods (the time over which they incubate the eggs) and relatively rapid developmental periods (the time over which a newly hatched robin develops into a fledgling that can leave the nest). For a robin, the incubation period lasts about 10-12 days, and the nestling period 10-16 days. Therefore, in the span of 20-28 days, a robin transitions from a just fertilized egg into a fledgling bird capable of short flights. That is an extraordinary feat for a complex, vertebrate organism. How and why does this critical period of growth and development happen so fast? The “how” question is complicated, and involves rapid rates of tissue differentiation and growth, and frankly is outside my realm of expertise. The “why” question is most likely tied back to the bane of the nesting bird; nest predators.
If nests are Nature’s Easter baskets, the woods, meadows, and even suburban backyards are teeming with chocolate-crazed children looking to ravage the contents of those Easter baskets. Only, these children come with scales, fur, and feathers. In fact, the list of animals that will depredate (eat) the contents of a bird’s nest is staggeringly long. There are the classical nest-predators, which are animals that routinely take advantage of the seasonal abundance in eggs and nestlings that pop up across the landscape in spring and early summer. These “Usual Suspects” include animals like raccoons, skunks, snakes, crows and jays, hawks, weasels, and owls. And then there are some surprising entrants on the list; many species of squirrel, mouse, and rat, fire and army ants, giant African katydids, and even Bambi. Indeed, based on footage collected from camera-traps, our doe-eyed deer friends seem to quite enjoy the occasional egg snack.
Many open-cup nesting species have altricial offspring, which means the baby birds are featherless, blind, and generally helpless upon hatching. As such, they are stuck in the nest for the duration of time they exist in the egg and nestling forms. Only when they have reached the fledgling stage are they capable of moving around under their own power. For nest predators, this means that if they can find a nest during the egg or nestling stage, they have a nice source of protein and fat nicely contained in one convenient (and immobile) package. To find a nest full of juicy nestlings, some predators cue in on the behavior of the parent birds and watch to see where they go. This tactic is most effective during the nestling period when the adults are forced to make frequent trips to the nest to feed their always-hungry offspring. The back and forth movements of the parents provide a target to hone-in on the nest. So how do the parents combat this?
One way birds can reduce the predation threat to their nests is to shorten the length of time that the eggs and nestlings are stuck in the nest. Nestlings that can get out of the nest more quickly may be at a lower risk of getting eaten. Alternatively, it may be that the risk doesn’t change much for an individual nestling, but if the nestlings are no longer contained all in one spot (i.e. the nest), the chances of losing all the offspring is lower, especially during one predation event. Presumably, this is where the expression “don’t put all of your eggs in one basket” originated from.
To illustrate this dynamic, let’s do some simple math. For the sake of this example, we’ll assume that robins experience a constant level of nest-predation risk over the duration of the egg incubation and nestling periods. If that rate of predation is 0.02 (or 2%) per day, the nest has a 0.56 (or 56%) chance of being eaten over a 28-day period. So that’s a greater than 50% chance of nest failure. If the duration in the nest changes from 28 to 20 days, that value drops to 0.40, or a 40% chance of being eaten. Now, instead of a 56% chance of being eaten (and a 44% chance of surviving), the nest has a 60% chance of surviving to the fledging stage. On an evolutionary scale, that’s a huge difference. Even if we shrink that difference and go with fledging in 24 days, that changes the odds from a greater than even chance of being eaten, to greater than even chance of surviving (52% chance of surviving).
Therefore, if species that are generally under high levels of nest-predation pressure can develop more quickly and get out of the nest at a younger age, they may be able to avoid some of that predation and change the odds in their favor. Sounds like a good strategy to me. However, there are almost certainly limitations on how rapidly a bird can develop. Some of these limitations are imposed at a high level of organization—what are called phylogenetic constraints—and are very difficult for evolution to get around. An extreme example of phylogenetic constraint is the evolution of flight in whales. It ain’t gonna happen. But for birds and speed of development, there are limits set by rates of mitosis, cellular differentiation, mitochondrial efficiency, etc., as well as the complexity of building and organizing various tissues and organs. You cannot make an ostrich in a day, or even a week. Another type of limitation comes in the form of developmental and/or life-history costs, and these costs are something I’ve been interested in for the past few years. But we’ll get to those costs in a minute.
This raises the obvious question: if you want to avoid losing your eggs/nestlings to hungry predators, but don’t want to deal with these mystery costs associated with rapid development, what’s a nesting bird to do? Some species place their nests in locations that nest predators don’t want to tread. Black-chinned hummingbirds in Arizona like to place their nests near the nests of Cooper’s hawks and northern goshawks because the hawks pose no threat to the hummingbirds (the hummingbirds are too small for the hawks to bother with), but they are threats to the hummingbirds’ nest predators; namely jays. Up in the Arctic, snow geese will sometimes nest in the shadow of a snowy owl nest, and the owls are thought to protect the geese from mammalian nest-predators. Another strategy is to make your nest hard to access, and lots of birds do this by nesting inside cavities. There are some species, like woodpeckers, that excavate their own cavities inside trees (or cacti, in the case of the gilded flicker), and others, like bluebirds, owls, and tree swallows, that take advantage of old woodpecker holes, other natural cavities, and nest-boxes. By nesting inside these structures, cavity-nesters typically experience reduced rates of predation. One sure sign that cavity-nesters are under lower predation pressure comes from the nestlings themselves; they make an unholy racket from inside the nest hole. I’ve found numerous woodpecker nests by following the sounds of nestlings bellowing for food. If a nestling in an open-cup nest made even a fraction of that amount of noise it would be snapped up in an instant by any hungry predator within earshot.
In addition to building up their vocal cords, cavity-nesters have the luxury of not having to rush their egg or nestling periods. The eastern bluebird, for example, is a relative of the robin (they’re both in the Turdidae family) and builds its nests in pre-made cavities, including bluebird boxes. The egg incubation period lasts for 11-19 days and the nestling period for between 17 and 21 days. Not only are these longer than the corresponding periods for the robin, but the bluebird is much smaller than the robin—about 30 grams in weight compared the robin’s much more substantial 80 grams—and smaller birds typically develop more rapidly than larger birds when comparing within the same family. What does this more relaxed developmental schedule mean for the cavity nesters? For one, when they do emerge from the nest hole, they are usually much more developmentally advanced than open-cup fledglings. Many of the cavity-nesters can fly reasonably well as soon as they leave the nest, which is critically important for avoiding predators. I’ve talked about the role of predators on nest-survival, but predators are also the presumed number one cause of death in fledgling birds as well.
The picture is looking rather rosy for cavity nesters, I would say. They are better protected in the nest, and then better able to avoid predators out of the nest. If I were a robin, I’d start thinking about looking for nest-sites inside tree holes. But there’s more to the story, and this is where the mystery costs of rapid growth and development come in.
Notice to the reader: the rest of this paragraph delves into some complex conceptual ideas and theories about growth and development. If you find your mind beginning to wander, feel free to jump to the next paragraph.
Research over the past few decades has shown that when individuals undergo accelerated rates of growth (relative to the norm for that species), they often suffer from a variety of physiological, morphological, and cognitive issues, and ultimately shortened lifespans. These problems have been linked to an excess of glucocorticoid hormones (such as cortisol and corticosterone; the “stress hormones”), as well as high levels of free radicals, which can damage an organism’s cellular machinery and even its DNA. When we look across species, however, it has been harder to identify what costs, if any, are associated with more rapid rates of growth and development. We do tend to see a pattern for species with more rapid rates of growth and development to have shorter lives, and there is some indication that this may be linked to elevated levels of free radicals produced during the rapid growth periods. Some of my own work indicates that there may be another cost as well; a loss of developmental flexibility. Work done in collaboration with colleagues at the University of Illinois examining rates of growth and development across a range of bird species suggests that those species with faster growth experience a reduction in developmental flexibility compared to species with longer periods of growth. This flexibility is important because it allows individuals to adjust their development to fit the prevailing conditions, especially the availability of food. Individuals with more rigid developmental trajectories may be unable to adjust to changing conditions, and could be more likely to die (which is what I found in similar work in zebra finches).
Now things really look bad for those open-cup nesters! They’re more likely to die in the nest. They’re more likely to die out of the nest as fledgers. And then they’re more likely to suffer from a litany of ailments that ultimately result in death at an early age. Where do I sign up? But the reality is that there’s something called a life-history tradeoff, which means, more or less, that some species live a fast-paced lifestyle, and other live a slow-paced lifestyle. Species that live life in the fast lane grow rapidly, typically have lots of offspring, and die young. The idea is that the relative parental investment is pretty low for a given individual offspring. And this is where a lot of the open-cup nesting species fall; they can make up for the high rates of mortality by producing more offspring. Meanwhile, the species in the slow lane generally live longer, produce fewer offspring per year, but invest more into each individual. Within the bird world, the species on the extreme slow end of the spectrum are seabirds like albatrosses, which can live to be 70 years old, often don’t reproduce until they’re 10+ years old, and raise a single chick over an 8-10 month period. Cavity nesters like bluebirds don’t exhibit that kind of life-history, but they do invest more energy and resources into a given clutch than robins do, simply by way of incubating the eggs for longer, and provisioning the nestlings for longer.
I’ve only scratched the surface in this exploration of avian nesting ecology, but I think I’ll leave it there for now. Hopefully readers will have the opportunity to see some of this nesting ecology in action for themselves over the coming months.
And on a related note, happy belated Mother’s Day to all the mom’s out there, especially my mom! Here’s the link to my Mother’s Day post from last year.
Next post: TBD
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* The next few posts will deviate a little from my normal format and represent a bit of nature travel escapism for those of us feeling a bit cooped up these days. The previous episode ended with the completion of field work in the midland region of KwaZulu-Natal, South Africa
Fact: the hippopotamus is the most dangerous animal in Africa, responsible for killing more people than any other animal. (Note: this doesn’t include diseases carried by vectors like mosquitoes, or the much more dangerous Homo sapiens).
This particular fact was at the forefront of my mind as I watched a pair of hippos slip under the surface of the water about 100 meters away from where I stood. Being this close to hippos wouldn’t have been cause for alarm under normal circumstances, but the circumstances at the moment were far from normal. The primary issue was that I and four companions were in a 20-foot aluminum motorboat named Vixen that was stuck in the middle of a giant, sluggish, milk-chocolate colored river teeming with hippos. Why are hippos so dangerous? It comes down to two things: a rather prickly disposition and meter-long teeth. And unfortunately for those of us stuck in the boat, one thing that really cheeses off hippos is unwanted visitors dallying in their territory, making a ruckus.
At the boat’s helm, and the one responsible for our current predicament, was an overly confident South African man named Greg who now found himself at risk of incurring not only the wrath of the local hippos, but that of his girlfriend Karina as well. Ben, Justin, and I had met the couple the day before while touring around the terrestrial portion of the iSimangaliso Wetland Park (formerly known as the Greater St. Lucia Wetlands Park) in northeastern South Africa. Greg and Karina were sitting on the roof of their Land Rover looking out over a small pond, and when we stopped to watch some waterbuck foraging at the water’s edge, the couple invited us to join them on their mobile viewing platform. We climbed up the ladder and sat down, enjoying the views that the elevated station afforded us. We chatted with the two friendly South Africans, who were probably in their late 30s or early 40s, and they asked if we would like to join them on their boat the following day for a trip up the St. Lucia estuary. This sounded like an opportunity we couldn’t pass up, so we enthusiastically agreed, and arranged for a time to meet them the next morning at the boat ramp.
When we arrived at the boat launch, they had just finished getting the boat in the water, and we jumped aboard, excited by the prospect of seeing some aquatic wildlife up close. Karina, who was the owner of the boat, had acquiesced to Greg’s desire to play captain, and he jumped behind the boat’s wheel. We motored away from the shore and began heading up the estuary. Despite admonitions from Karina to be careful of hidden shallow areas and to stay in deeper water on the right side of the estuary, Greg managed to captain us right into the mud in relatively short order. After a thoughtful assessment of the situation, the skipper decided that the obvious solution to the problem was to rev the motor even more and power us through the unseen mud shoals. Instead of skimming to freedom, we bogged to a whining halt with the propeller now caked in thick, sludgy mud. This was around the time that I noticed the hippos vanishing from sight and began wondering about their abilities to navigate through mud, and if they might be mollified by the sacrificial offering of our wayward captain.
Another fun fact about hippos is that they don’t swim. They run, bound and gallop on the bottom, using fine buoyancy control to adjust how far from the bottom they go during their movements. Despite their tank-like proportions, they are quite graceful, and capable of reaching speeds up to 30mph in the water. Don’t believe that? Check out this video from a few years back:
With my head full of useful hippo facts, various scenarios for how they would deal with us danced through my mind, and in none of them did the hippos offer to tow us out of the mud. To avoid padding the hippos’ grisly statistics, we began working on ways to extract ourselves. The boat had two small paddles that were nominally made from sturdy aluminum, but after attempting to use one to push us backwards through the mud I realized they were constructed from something akin to bendy-straw plastic. My paddle crinkled almost immediately, rendering it entirely useless. I didn’t want to appear as though I wasn’t trying to help, however, so I continued to act like I was working hard to free us with my now flexible paddle. When it became clear that we were not going to paddle ourselves to salvation, we stashed the paddles (I made sure to hide my crumpled paddle under some blankets), and we worked on developing other strategies. Justin came up with the idea of using the boat’s anchor to pull us back the way we had come. He would toss the anchor as far as he could, let it get nice and stuck in the mud, and then we would pull the boat towards the anchor. Once we reached the anchor, we would pull it up and repeat the process. It worked, and within half an hour we were able to get back to deep water. We all congratulated Justin on his brilliant idea, and our fearless captain again pointed us up the estuary, and away we went. We had no more unexpected adventures, but instead enjoyed a beautiful few hours watching hippos, crocodiles, goliath herons (the world’s largest heron), and a host of other wildlife. And I think we all very much enjoyed not being mangled to death.
In classic “This is Africa” fashion, our hippo adventure was only one of many unforeseen wildlife encounters that happened on our trip. In fact, the prior day I had come face to face with an animal that I had never expected to see in the wild, nor had any idea of how to treat. As someone who had spent a good portion of his life outdoors and much of the indoor portions watching nature documentaries, I was unprepared to feel so, well, unprepared for that encounter.
There are no lions in the iSimangaliso Wetland Park, so there are a few places where visitors can get out of their vehicles and walk through the bush. One of those is the Mziki Trail, and Ben, Justin and I were exploring sections of the trail that led to some animal hides overlooking waterholes.
At one point I ventured off a little way from the other two, and slowly wound my way down a side trail. I spotted a Natal duiker (a German shepherd-sized antelope) bounding away through the vegetation. Not far behind was a young bushbuck (another medium-sized antelope) that was also making a hasty exit. I came to a stop. It wouldn’t have been unusual for two antelope to have run away from me, but they hadn’t exactly been running away from me. In fact, they had kind of been running towards me and then altered their course when they saw me in their path. I was trying to sort out what was going on when the answer came ambling around the corner about 50 feet down the trail. It was a honey badger. Those who are familiar with this large member of the weasel family know it is an animal not to be trifled with. Even though these wolverine-like animals only clock in at between 20 and 35 lbs, they have been known to take on lions and hyenas when defending a food source, and there are unsubstantiated reports of attacks on humans. They are also moderately indestructible. They have almost impenetrable skin, an incredibly thick skull, and an attitude that garnered them “world’s most fearless animal” in the 2002 Guinness Book of World Records. Furthermore, they have a sweet tooth for venomous animals. Well, I say sweet tooth, but I actually don’t know if venom falls on the sweet or salty side of things. Regardless, honey badgers routinely go after scorpions and venomous snakes like mambas, adders, and cobras. If an individual happens to get stung or bitten by one of these deadly meals, it might get a little sleepy and take a short nap, but then it’s up and raring to go again.
So, this was the animal that was rapidly bearing down on me, making snuffling, huffing noises as it trotted along the path. Honey badgers do not have very good vision, and this individual’s attention was mostly directly towards the ground, so the prospect of having a close encounter seemed very real. Generally not one to panic, I instead froze, giving my best rendition of a tree or termite mound (my second-grade theater director would have been proud). I was at a complete loss for what to do. Climb a tree? Waive my arms and yell? I had no idea. Ultimately, I did nothing, and to my relief, when the honey badger was within 20 feet or so, it glanced up, saw me, appraised my level of tastiness, and pulled a quick U-turn. I breathed a sigh of relief, silently thankful that I didn’t smell like a big snake or some other animal from the honey badger menu. I think those people who write guides about what do to when bears attack, or when a shark is nibbling on your leg need to include a chapter on what to do when a honey badger is about to smack into you. I, for one, would find that helpful.
We spent two days in the iSimangaliso Wetland Park, and then made the short trip over to the exquisite Hluhlewe-iMfolozi game reserve just off to the west. iSimangaliso had been great, but this was Africa on an entirely different level. Lion, elephant, Cape buffalo, hyena, rhinoceros, zebra, giraffe, leopard…the list of animals present in the reserve was staggering. We struck out on the cats, but we did get to see many other exciting game. The white rhinoceros was relatively abundant in the reserve, and we had a number of thrilling rhino sightings. One of our first encounters was with a massive male who wandered right up next to our car, giving us up-close views of his two-foot long front horn, and layered gray skin.
There are two species of rhino: the white (or square-lipped) and the black (or hook-lipped), and white rhinos are much less ornery than their cousins. The white rhino’s broad mouths are used for grazing vegetation on the ground, while the black rhino’s pointed lips are more dexterous, allowing it to more effectively grasp leaves on bushes and shrubs. We watched the 2.5-ton male clipping grass along the edge of the dirt road for about 20 minutes, and when he had moved along a little, so did we. Towards late afternoon the next day, we came across a mother rhino and her very young calf standing at the edge of a small mud hole. Rhinos love a good wallow in the mud, and the baby had clearly been getting acquainted with this patch of mud. The mom stood watch while the baby bounded around her, testing out his new legs. Occasionally mom would herd him one way or another, using her horn to guide him in the desired direction. We were a good 100 meters away, but mom kept one eye on us and the other on the baby the whole time. After getting our fill of adorable baby rhino, we drove back to our accommodations and got our fill of pasta and beans.
I’ll wrap up this post, as well as this three-part mini-series, with another elephant story. Warning: this elephant story is rated PG-13. We kicked things off a few weeks ago (Down in Africa: Part I) with an angry mother elephant threatening to crush us inside our Toyota Corolla. That experience gave us a very real appreciation for the sheer size and power African elephants possess. But in that case, it was mostly the potential for destruction that captured our attention. The day before that encounter we had witnessed the actual power that elephants are capable of when we came upon two large bull elephants foraging just off of the dirt track we were driving. We saw evidence of their presence long before we laid eyes on them; downed branches, massive dung piles, and trees knocked about like small saplings.
The two bulls did not differ dramatically in size, but one, clearly the older, dominant male, had tusks that were much larger than those of the other, younger bull. The two males slowly made their way through the open savannah, grabbing branches with their trunks and shoveling the leafy vegetation into their mouths. At one point when the two elephants were perhaps 20 meters apart, there was a slightly surreal display put on by the younger bull. I have no idea what precipitated this show, but elephants do communicate in the infrasound range (below our hearing capacity) so it’s entirely possible the older bull said something disparaging to the younger one about the size of his tusks. Whatever was said, the young bull responded with the most unambiguous exhibition of machismo I have ever seen; he began thumping his own belly with his extended penis. Think male gorilla pounding his chest, only not using his hands. We were 100, maybe 150 meters away and could hear the thumping clear as day. I’m no elephant, but I certainly understood what was being said. I wondered if perhaps things would escalate and we would get to see these two behemoths grapple for dominance, but the older bull was unfazed by this youthful display of testosterone, and continued leisurely stuffing food into his mouth.
Just another day in Africa.
Next post: nesting ecology of birds.
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* The next few posts will deviate a little from my normal format and represent a bit of nature travel escapism for those of us feeling a bit cooped up these days. The previous episode ended with my arrival at the Joburg airport and collection by Justin and Ben, with whom I would be working for the next 5 months.
The four-hour car ride from the Johannesburg airport to our new farm home and basecamp in the hills outside Pietermaritzburg passed in a blur of highway medians and sleep-adled haziness. When we did arrive at the gated entrance to the farm, I managed to coax my brain up from the depths of its stupor to take note of the surroundings. The landscape was a matrix of sprawling grassland, forested riparian patches, cattle pastures, and pine plantations layered upon an undulating terrain of hills and valleys. I don’t remember the dimensions now, but the farm must have encompassed hundreds if not thousands of acres.
As we drove down the mile-long dirt driveway, we excitedly pointed out the new birds to one another, and gawked at the cows lazily watching us drive past. We eventually came to the primary farm compound which consisted of a main house and a smattering of smaller buildings and sheds tucked into the outlying trees. The owners—a British South African couple-- came out to greet us, accompanied by their two young daughters and four dogs: two enormous wolfhounds, and two darting terriers. As I came to learn during my time in South Africa, this sort of canine combination is quite common. The small dogs (with their acute hearing) serve as an early-warning alarm system in case of trespassers, and the big dogs serve as a deterrent with their chomping teeth and slobberous quantities of drool.
After the introductions, we were shown to our living quarters, which were in a self-contained apartment unit attached to the main house. I was pleasantly surprised at the accommodations; up to that point in my field biology career I had only ever lived in a tent during field seasons, and hot water was used for cooking, not bathing. Here, however, we were in the Taj Mahal of field houses. Not only did we have beds, a kitchen, and a shower, we had access to the sparkling, sublimely chlorinated waters of the swimming pool just outside our doors. A guy could get used to this, I thought happily.
The first few days were spent getting familiar with our new realm, and delineating where we would focus our work efforts. Waterbuck (a large antelope), duikur (a genus of small to medium sized antelope, ranging from 6 lbs. to 150 lbs.), lizards, an abundance of frogs and toads (many sporting white “racing stripes”), technicolor grasshoppers, giant winged antlions, and myriad new bird species were our field companions as we traversed the grassy slopes and valleys.
We dodged semi-concealed holes in the ground that were the product of burrowing aardvarks, and were constantly on alert for venomous snakes like spitting cobras, black mambas and puff adders. Our target was the nest of the common waxbill, a small, mostly gray-brown finch with a fiery red mask and orange-red bill. Males are also adorned with a splash of red on their belly and chest. As I mentioned in the previous post, common waxbills are hosts to the brood-parasitic pin-tailed whydah, which is another small-bodied finch. Male whydahs, however, are boldly patterned in black and white, with long black tail streamers that are 2-3 times the bird’s body length. Males show off these streamers during mating displays in which they bounce up and down in the air in front of a female. Females are a much less ostentatious brown and tan-bodied bird, with some black streaking thrown in for camouflage in grassy environs. Once a female has selected a sufficiently attractive bouncing male and mated with him, she heads off in search of waxbill nests to deposit her eggs.
I can tell you from experience that locating a waxbill nest in the grassy expanse of the South African midlands is no easy task. Waxbills build grass nests that are woven into the bases of living clumps of grass. These nests are completely enclosed, with a secret grass-tunnel entrance. As if that weren’t challenge enough, they tuck these small globular grass structures underneath a visually impenetrable barrier of overhanging grass tussocks. So what you end up with are essentially invisible grass nests scattered across a seemingly endless grass sea. For an extra psychological kick in the groin, these birds actually seem to derive pleasure in taunting nest-searchers. Unlike most small passerine birds, waxbills appear to have no qualms about venturing far outside any localized home range or territory. On countless occasions during my searches I came upon waxbills with strands of grass in their bill, only to watch them take flight and disappear over a distant ridge, giving me a parting smirk just before they vanished. But even more soul-crushing was watching a bird disappear into the distance with a beak full of cat poop.
Yep, you read that right. Waxbills engage in some bizarre scatological behavior in which they weave carnivore droppings into the outer walls of their nests. They seem to prefer the scat of small to medium-sized wild cats like servals and African wild cats. These felines consume a lot of small mammals, which means that their scat is usually composed of tightly compacted strands of small mammal fur that the waxbills artfully incorporate into their nest. Servals and African wild cats are extremely secretive and rather uncommon, so their scat is a hot commodity for the waxbills. Finding a waxbill with a cat turd in its beak was a joyous occasion because it meant the bird was headed directly back to its nest. When I encountered a be-pooped waxbill (like bespectacled, but with poop in its bill), I would immediately morph into commando mode, dropping to a knee, fixing the binoculars on the bird with laser-like intensity, and preparing to sprint after the bird should the need arise.
The nest of a Common Waxbill. The opening on the top is actually a false chamber, presumably meant to fool nest-predators. The actual entrance is the cascading tunnel dropping down in the front. Notice the carnivore scat at the opening to the false chamber. Also, this is a particularly conspicuous nest. Most were practically invisible. KwaZulu-Natal, South Africa. Photo credit: Justin Schuetz.
It’s hard to appreciate the degree of mental anguish associated with failed nest-searching when you spend long days out in the intense African sun, plodding across boundless grassy slopes without locating a single nest. As such, the stakes feel very high when you find a bird preparing to bring home some new housing décor. However, even when everything goes according to script—the bird carries its prized possession only a hundred meters and drops down into a very identifiable patch of grassland where you can pinpoint the location at which the bird vanished from view—you can fail to find the nest. These birds are masters of visual ventriloquism (if such a thing exists); you think it went one place, and discover later that it is in fact somewhere behind you. The best you can do in these circumstances is to mark the general area that the bird vanished, retreat a hundred meters and place the entire area under surveillance. If that doesn’t succeed, you return another day hoping to perhaps flush the bird from its nest. And if that fails, you curse the birds and the nest-searching gods and move on.
The curious reader will want to know why waxbills go to such lengths to defile their nests with the excrement of an animal that would happily consume them and their offspring. Cat scat, it turns out, deters nest-predation from one of the waxbill’s greatest nest-enemies; small mammals. It may come as a surprise to learn that small mammals can act as nest-predators, but many species of rodent will happily augment their normal vegetarian diet with eggs, and, on occasion, an unfortunate young nestling. (It’s kind of like the “ovo-pollo” version of vegetarianism, which, if we’re being honest, isn’t actually vegetarianism at all.) Because common waxbills nest on the ground, it is thought that they are at increased risk of nest-predation from small mammals. By adding bits of cat feces to their nest, however, they make their nest smell like a small-mammal-eating machine. To test this theory, Justin (the grad student I was working for) did some observational and experimental work examining the efficacy of having carnivore scat in the nest. He found that every natural waxbill nest that successfully fledged at least one chick contained carnivore scat, and that experimental nests with scat added were significantly less likely to get depredated (eaten) than nests without scat. A fascinating rendition of the adage “(the droppings of) the enemy of my enemy is my friend.”
So, having dealt with the small mammal issue, waxbills are left to contend with the parasitic whydahs. Compared to the more virulent cuckoos and honeyguides I covered a few posts back, whydahs are relatively benign. The female whydah sneaks into a waxbill nest, lays an egg, and leaves. She may return to deposit another egg or two, but she doesn’t eat or destroy any waxbill eggs, and once the whydah chicks hatch, they don’t push the other occupants out or pierce their cervical vertebrae. On the whole, they’re rather ok for uninvited houseguests. Whydah nestlings are a bit larger than the waxbill nestlings, and according to some sources they beg more vociferously for food, which may allow them to outcompete the smaller host chicks. But in many instances, the adult waxbills are able to raise all their young, along with the parasites. Where things get interesting is when we take a look into the mouths of these nestlings.
The family of birds to which the waxbill belongs (Estrildidae) is composed of over 100 species spread across Africa, Asia, and Australia, and includes some well-known members of the pet trade, such as the zebra finch and Gouldian finch. The pin-tailed whydahs are in the Viduidae family, which contains about 20 species found throughout Africa, all of which are parasites on Estrildid finches. Many of the Estrildid finch nestlings have startling bright and bizarre markings inside their mouths and lining the flanges of their beaks, and the markings of each species are generally quite distinct. Except, that is, for the markings inside the mouths of the corresponding Viduine parasite. Take our common waxbill and pin-tailed whydah duo; the whydah may parasitize other species, but the common waxbill seems to be the most frequently parasitized host, and the whydah appears to have evolved a remarkable degree of mimicry regarding the mouth markings. When we look at other host-parasite pairings, a similar pattern emerges, resulting in a dazzling example of co-evolution between the two lineages of host and parasite.
But one of the intriguing, and still unanswered questions about these mouth markings is why Estrildid species that are not parasitized (such as those in Australia) also have these elaborate markings. As is usually the case, there are a few possible explanations. One is that the ancestral Estrildid finch had mouth markings, and that as species split and diverged, the markings split and diverged with them. But what purpose would the markings have served in the absence of brood parasites? Well, for one, they could act as targets for the parents inside the dark, enclosed nests that many Estrildid finches use; a “Food Goes Here” sort of beacon. The markings could also be an indicator of the chicks’ condition, allowing adults to preferentially feed the highest quality chicks when resources are limited. In his study, Justin found evidence in support of the idea that the markings are important signals to the parents. He used a non-toxic marker to manipulate the mouth markings of the waxbill nestlings to see if the parents would adjust their behavior towards the chicks with different markings. It seems that they do. While they did not eject the nestlings with the altered markings, those chicks with modified patterns experienced slight but significant reductions in growth, suggesting that the parents were providing more food to the unmanipulated chicks. This finding also provided some evidence for a selective pressure on the parasitic birds to match the markings of the host; without the right mouth pattern, the parasitic nestlings risk getting passed over by the host parents.
Over the course of the three and a half months of searching for waxbill nests, I think I found about 50 nests. It might have been closer to 70, but if we do the math, it was likely less than a nest per day on average. On most days, that didn’t matter. I was, after all, traipsing around South Africa, looking for nests, and thrilling to everyday encounters with wildlife I had only ever seen in a museum or on TV. One day, while watching some suspicious waxbill activity, a duiker came loping through the grass and nearly ran into me before noticing I wasn’t a large boulder. On another occasion I watched a blue duiker squeeze through an opening in a fence. I know that doesn’t sound noteworthy, but when I went to look at the opening the duiker had crawled through, I saw it was no bigger than my fist. Apparently, the limiting factor on the size of an opening a duiker can fit through is its skull, and the little blue duikers have awfully small skulls. I also saw dozens of new bird species, as well as exciting new reptiles and amphibians. But it wasn’t always a walk in the park.
I suffered a few bouts of mild heatstroke, one case of food poisoning (never leave leftover Indian food in the car in the African summer… and then eat those leftovers later), and an annoying allergic reaction to, of all things, the sun. That’s kind of like being allergic to the wind, and it doesn’t work out well if you’re a field biologist. Essentially the problem comes down to a rapid transition from no UV exposure (like what you have in Maine in November) to high UV exposure (South Africa in their summer). And the way my body responds to this perceived insult is to burst into hives. Heat and humidity (both available in sizeable quantities in South Africa at that time of year) exacerbate the condition, as does more sun exposure. For me the issue is most pronounced on my hands, which are hard to keep covered out in the open grasslands. And once the hives are out, they do not like to be stuffed into a pair of gloves or any other covering. Unfortunately for my hives, one of the sites we worked at once or twice a week was a recently cleared section of pine plantation that was transitioning into a giant bramble thicket, and a good pair of gloves was critical for wading through the sea of thorns. This site was called Hilton, but it quickly became Hell-ton, and I dreaded our trips there.
Aside from these few annoyances, the field season passed quickly, and for the most part, enjoyably. Before we headed up to Tanzania (via Egypt) for the next leg of the field project, we had a few weeks of adventure travel to enjoy. I’ve already touched on one of the elephant encounters, but in the next post we’ll visit with rhinos, hippos, and a huffing honey badger.
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About the author:
Loren grew up in the wilds of Boston, Massachusetts, and honed his natural history skills in the urban backyard. He attended Cornell University for his undergraduate degree in Natural Resources, and received his PhD in Ecology from the University of California, Santa Barbara. He has traveled extensively, and in the past few years has developed an affliction for wildlife photography.