Category: Nonfiction

It’s the spookiest time of year again- time for costumes and creepy urban legends and candy and movies using gallons of fake blood. Who doesn’t love a good shiver? After all, for the most part, we modern humans have few of our ancestral fears left. No tiger or lion is going to spring out of the undergrowth at us while we’re waiting in line at the DMV.

In large part, this is because humans have systematically eradicated possible predators from every ecosystem we inhabit. Largely gone are the grey wolves, the cougars, the lions, the tigers, and even the sharks from their ancestral ranges. The amount of territory lost, if you look at it in a visual representation, is stunning.

From Laliberte & Ripple, 2004.

From Panthera.org

From Discover magazine

With these threats (mostly) removed, we humans feel much safer. Perhaps too safe, judging by the amount of money we all spend each year to get scared in haunted houses or amusement park rides.

But by removing top predators, we don’t just ease our own fears. When impala stop seeing, hearing, and smelling evidence of lions and cheetahs, they too breathe a sigh of relief. And what happens next- forgive me- can be a little scary.

Two years ago, I wrote a piece on the current overpopulation of white-tailed deer in the United States. The effect that these deer have on forests cannot be understated: they eat new saplings and demolish the undergrowth, leaving hundreds of other species without food or homes. I argued then that to protect our forests, we need to somehow reduce the numbers of white-tailed deer.

It would be nice if this happened a little less often, too.

I still believe that we have to pull down the population of deer, but there are other factors we overlook that greatly affect how prey species interact with their environment. The number of healthy animals that carnivores actually manage to kill is surprisingly small compared to the number of animals left alone. Disease and famine are much more significant causes of death for most animals then getting snapped up by someone else. (The exception to this is when an invasive carnivore is abruptly introduced to an ecosystem.)

The chance for an individual (healthy) impala to be killed by a lion might statistically be quite low, but they wouldn’t survive as a species if they weren’t driven to change their behavior if they smelled a predator in the area. And that, by and large, is the main effect that predators have on prey, not the part where they eat them.

So how does fear change prey behavior? Numerous studies have examined this by either “muzzling” predators or simply leaving evidence of their existence and watching what the prey animals do. One recent study involved playing dog barks and growls to scare raccoons living on the Gulf Islands in British Columbia. According to the authors, the effects weren’t just immediate- they were large-scale and persisted over a month.

Raccoons used to have more predators on the islands until humans moved in (a common enough story), but now their main predators are domestic dogs. These island raccoons normally spend a lot of their time foraging for crabs along the seashore. However, once the researchers started playing dog calls, there was a dramatic shift: the raccoons started avoiding the shore.

This isn’t actually too surprising, of course. The shore is a very open and exposed place to be if you’re afraid of getting snacked on. What was surprising was how quickly this affected other species along the shoreline. The crabs that the raccoons would normally have preyed upon began to appear in much greater numbers. The crabs ate the food as a species of fish, which began to decrease in number as the crabs increased. And the numbers of the crabs’ own prey, a species of snails, started decreasing in number.

“Diagram illustrating how broadcasting playbacks of large carnivore vocalizations affected multiple lower trophic levels. Green and red arrows represent positive and negative effects, respectively, on foraging, abundance or survival. Solid arrows connect predator and prey; dashed arrows connect species affected, but not directly eaten, by another.” (From Suraci et al, 2016.)

This is what’s known as a ‘trophic cascade,’ meaning it affected multiple levels of the ecosystem. No doubt there were other effects that the researchers didn’t measure, too: for example, perhaps the algae that the snails fed on also increased.

The fascinating thing about all this is that the raccoon population was in no way reduced or restricted. Their own fear was the only thing that changed all of these different animal populations. Scared animals, it turns out, spend less time eating in one spot, and eat less overall. Instead, they spend more time with their heads up, scanning for danger, and are more likely to bolt to a new position at small provocations. They also seek out areas that may not have the best food, but do have good cover, like forests or rocky outcroppings. They may even change their group composition, splitting from large spread-out herds to tight little knots of nervous animals. All this anxiety means that whatever food they eat, plants or crabs, isn’t totally decimated when they leave.

This sort of trophic cascade was exactly what researchers thought they had found in Yellowstone Park in 2004. Perhaps you’ve heard of this one before- there was a popular ‘wolves change the course of rivers’ video that was passed around a lot on social media a while back. Here’s the gist of it:

Like the white-tailed deer, the overpopulated elk in Yellowstone were having a dramatic effect on the growth of saplings, particularly along riverbanks. By removing the saplings, the elk caused greater erosion of the soil at the water’s edge, which caused the rivers to flow wider and slower. The video claims that when wolves returned, the elk immediately began avoiding the exposed riverbanks, clustering inside protected forested areas. The saplings grew back, their roots packing the soil together, and the rivers flowed narrower and faster- changing their course.

Seems very dramatic, but plausible, given the studies discussed earlier. Unfortunately, the effects that the wolves had on the Yellowstone ecosystem were overstated, and the conclusions drawn premature. It wasn’t the wolves’ fault- they were doing their job perfectly well. The fact was that after 70 years without their apex predator, conditions in Yellowstone had changed far too much for the wolves to rescue. It simply isn’t that easy to restore a heavily-eroded river to its former, fast-flowing state just by depending on tree growth.

This is a grim truth we all have to face: even if we return all top predators to their former ranges, we can’t expect them to reverse all the scarring left behind from their absence. And there are, sadly, very big scars. Some examples I pulled from a literature review on the effects of the loss of consumer species (Estes et al., 2011):

• The reduction of lions and leopards in parts of sub-Saharan Africa led to an increase in the number of olive baboons. The baboons also became bolder without predators to fear, and came in increasing contact with humans. This also led to increasing infections by zoonotic diseases and parasites.
• Because of their large size, whales hold on to huge amounts of carbon taken from their planktonic prey. When whale populations were devastated by whaling in the early 20th century, an estimated 105 million tons of carbon were returned to the atmosphere, contributing to global warming.
• The loss of sharks and other large reef predators leads to greater numbers of coral-eating fishes, lower water clarity, and diminished coral reefs.
• When harmful invasive species are introduced to ecosystems, invasions are much, much more successful in the absence of predators.
• And of course, overall diversity is decreased when top predators are lost, because they no longer check the feeding habits of their prey, which can lead to a cascade of effects as described in the raccoon study.

Much of this damage is very hard to reverse. Indeed, since the Pleistocene, human eradication of megafauna (that is, large species of both herbivores and predators) have led to increasingly simplified and fragile ecosystems. The pristine earth we nature-lovers envision never really existed after humans entered the picture. We’re just… really good at changing things up, I guess you could say. In fact, you could argue that all the problems started when we lost our own ecology of fear- when we began crafting tools and weapons that allowed us to strike back at our predators, and became so confident in ourselves. Now we overgraze the planet.

I don’t mean to end this on a hugely sour note. There are some things we cannot ever change, but there are some things we can still fix, or at least begin to patch up. The research on the nonlethal effects of large carnivores is an important step in the process, because it will hopefully lead to more reintroductions like that of wolves in Yellowstone. Ecosystems need their top predators. And I do have hope that we can learn how to live with them- surely with all of our technology and ingenuity we can find a way to do that. Even if we are a little more scared.

One last thought, for this probably-too-serious Halloween post. We have been looking at fear from a very far-seeing ecological perspective, and it is fascinating how much one little emotion can change. Yet we can also zoom in a little more and ask how this fear impacts the lives of the individual animals it affects. In my series of articles on keeping animals in captivity, I mentioned that most researchers consider predation risk a form of acute stress- extreme when it occurs, but not long-lasting. However, when we look at the extreme changes in animal behavior when predators are merely hinted at, perhaps this is the wrong conclusion to draw.

In fact, field research on the effects of predator threat without actual predation (again, by doing things like muzzling, limiting access, or using trained dogs as predators) suggests that even mild exposure can cause chronic stress in prey animals, leading to poorer body condition, lower reproductive rates, and increased susceptibility to disease. This response to a predation threat is actually used to create animal models of PTSD. In other words, face a mouse with a caged cat just one time, and the effects will be traumatic and lingering.

What does this mean? Well, for starters, it could mean that PTSD-like symptoms are far more ‘natural’ than we may assume. Wild animals probably suffer from them all the time, unfortunately. Sheer terror is a very important aspect of animal behavior, with perceived danger perhaps being a much bigger factor than actual danger. But the flip side of this is perhaps by studying the so-called natural PTSD, we can understand how to better treat it in humans and captive animals. After all, even with the terror of predation hovering over them, wild animals still somehow manage to go about their daily lives with success. They still play, socialize, and mate. By studying their resilience, perhaps we can increase our own.

Anyway, here’s a silly video of lots of animals getting scared! Hahahahaha! Happy Halloween kiddos!!

References and further reading:

Clinchy, M., Sheriff, M. J., & Zanette, L. Y. (2013). Predator‐induced stress and the ecology of fear. Functional Ecology, 27(1), 56-65.

Estes, J. A., Terborgh, J., Brashares, J. S., Power, M. E., Berger, J., Bond, W. J., … & Marquis, R. J. (2011). Trophic downgrading of planet Earth. science, 333(6040), 301-306.

Gervasi, V., Nilsen, E. B., Sand, H., Panzacchi, M., Rauset, G. R., Pedersen, H. C., … & Liberg, O. (2012). Predicting the potential demographic impact of predators on their prey: a comparative analysis of two carnivore–ungulate systems in Scandinavia. Journal of Animal Ecology, 81(2), 443-454.

Laliberte, A. S., & Ripple, W. J. (2004). Range contractions of North American carnivores and ungulates. BioScience, 54(2), 123-138.

Marshall, K. N., Hobbs, N. T., & Cooper, D. J. (2013). Stream hydrology limits recovery of riparian ecosystems after wolf reintroduction. Proceedings of the Royal Society of London B: Biological Sciences, 280(1756), 20122977.

Mduma, S. A., Sinclair, A. R. E., & Hilborn, R. (1999). Food regulates the Serengeti wildebeest: A 40‐year record. Journal of Animal Ecology, 68(6), 1101-1122.

Owen-Smith, Norman, Mason, D. R., & Ogutu, J. O. (2005). Correlates of survival rates for 10 African ungulate populations: density, rainfall and predation. Journal of Animal Ecology, 74(4), 774-788.

Ripple, W. J., & Beschta, R. L. (2004). Wolves and the ecology of fear: can predation risk structure ecosystems?. BioScience, 54(8), 755-766.

Salo, P., Korpimäki, E., Banks, P. B., Nordström, M., & Dickman, C. R. (2007). Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society of London B: Biological Sciences, 274(1615), 1237-1243.

Suraci, J. P., Clinchy, M., Dill, L. M., Roberts, D., & Zanette, L. Y. (2016). Fear of large carnivores causes a trophic cascade. Nature communications, 7.

Valeix, M., Hemson, G., Loveridge, A. J., Mills, G., & Macdonald, D. W. (2012). Behavioural adjustments of a large carnivore to access secondary prey in a human‐dominated landscape. Journal of Applied Ecology, 49(1), 73-81.

Heck, it’s just a big flying puppy, right?

This post is the result of several comments I have received- mainly on my tumblr, where I tend to post a lot of videos and photos of the bats I’ve worked with- about people wanting and/or spreading misinformation about pet bats. While I know that comments like “I want one” often aren’t meant seriously, I worry that my cute photos and videos may act as a catalyst for someone to actually seek out a pet bat. I want to explain to everyone who visits this website why that’s a bad idea.

Luckily, as far as I know, bats are not terribly prevalent in the exotic pet trade. I say ‘as far as I know’ because it is extremely difficult to find actual statistics on a business that treads a lot of murky lines between legal and illegal activity, and does much of its business in private, away from outsiders. However, it took only a few seconds of googling for me to find a listing of Egyptian fruit bats for sale in the United States (I won’t link to it and give it any possible publicity). It took just a little more googling for me to find several popular vines from Japan of pet fruit bats of varying species. (Japan in particular is a country with serious issues regarding the import and breeding of exotic pets. Which isn’t to say the US is much better.)

In the U.S. and some other countries, keeping native bats as pets is illegal, but it is legal in many states to import non-native species, particularly fruit bats like straw-colored fruit bats, Egyptian fruit bats, and leaf-nosed bats. As such, this article will focus mainly on the needs of fruit bats rather than insectivorous bats.

It’s not hard for me to see what the appeal of a bat is- I mean, I LOVE bats. And a lot of the fruit-eating species are pretty traditionally cute, with foxy faces and big bug eyes. Chihuahuas of the sky.

I mean, look at this.

But the thing is- and this should be obvious- bats aren’t flying dogs. They are intelligent, social, fascinating creatures, but that doesn’t mean they belong in your living room. And as someone who has worked with these critters, let me give you three solid reasons why.

Reason one: Bats Are Really Gross

Check out this video of a bat… uh, what is he doing? Rubbing something on himself? But what could it be- it’s piss. He’s rubbing piss into his fur. He does this every day, multiple times a day. If you were to touch him, you’d be touching a piss-oiled bat.

‘Urine wash’ behavior, as it’s called, isn’t the only natural behavior of the bat that we humans might find unsavory, but it’s definitely the one I like to bring up to visitors the most. Bats do this as a way to keep themselves fragrant, so to speak, though they also have smelly scent glands on both sides of their neck which they use to mark things as well. Quite liberally. On the corners of the night-houses where these captive bats live, there are black marks where the bats have scent-marked to the point of wearing away the paint. As someone who’s had to scrub the gunk off, that shit is potent. And stubborn.

Scent is a very important sense to a bat, and it’s a large part of how they communicate with one another. So they like to stay stinky. It isn’t so bad when the bats are kept outside, but when you bring a bat inside? Oh, boy. I’ve done a ten-minute drive to the vet with a scared Malayan flying fox in a carrier in the backseat, and the car took a week to recover. Leaving a bat overnight indoors- as was sometimes required with sick or disabled individuals- would greet you with a dense fog of a stench in the morning. Sort of like fermented fruit mixed with skunk. Really good.

It wasn’t just the bat that was stinky. Bats, as the only flying mammals, need to process shit quickly in order to keep their energy up. Which means that they eat a lot and pee a lot and poop a lot. You can’t potty train a bat- it’s just going to come out no matter what. Roughly twenty minutes after a fruit bat has eaten, everything gets processed. We put fresh paper under our isolated bats each night, and every morning that paper would be soaked through with urine, liquid poop, solid poop (it’s normal for them to have both) and spats.

…What are spats, I hear you ask? Let me tell you! You see, when a fruit bat eats fruit, it actually mostly just wants the sugary juice, not any of the hard-to-digest pulp or rind. So when they take a bite, they mash it up against the roof of their mouth, squeezing out as much juice as possible, and then… spit the rest out. So, essentially, any fruit bat enclosure is going to be littered with chunks of masticated fruit.

Spats.

Did you know that bats aren’t the only animals who like fruit? Insects like roaches and fruit flies also like fruit. Do you know what really attracts these insects? Why, chunks of fruit left on the ground, of course! Where there are bat spats, insects follow. It’s great for a native ecosystem, but consider whether or not you want to harbor this ecosystem in the comfort of your home. Along with, you know, having to clean up feces and urine several times a day.

Pooping, peeing, and stinking aren’t the only impolite bodily functions bats do that might be frowned upon in human society. No. I’m talking about public masturbation and sex. Multiple times a day. Not subtle.

Have you ever had to give a tour to a group of kids while a bat autofellated itself in the background? I have.

Have you ever watched a male bat get his erection licked by another male while a third male attempts to mount him from behind? I have.

Have you ever seen a bat engage in so much aggressive anal sex that his partner’s anus is left scarred and bleeding? Thankfully I haven’t, but that was because the bats were permanently separated before I arrived.

Bats… have a lot of sex. And a lot of boners. And even the females will hump, mount, and get cozy with each others’ vulvas. It is impossible to get around it, and even castrated bats still get multiple erections each day, which they proceed to lick and rub their faces against… among other things.

I gave my sister a private tour of the bat facility, and her first glimpse of an erect bat penis caused her to yell. It is truly a startling sight for the uninitiated. I will say that I got so used to it I stopped even noticing the boners a couple weeks in- but think about that. Look at that linked picture and think about it. That happened so much that I stopped noticing it.

Masturbation multiple times a day is normal for a bat. Same-sex behavior is normal for a bat. The employees at Disney’s Wild Kingdom, where they have Malayan flying foxes on display, literally have specific training about how to explain bat erections to children. (Kids react to: bat masturbation!)

Let me close out this section with one final story, told to me by a senior keeper: one day, she was going to feed an older male bat, without realizing he had just masturbated and ejaculated on his own face. He sneezed on her.

Bats are gross.

Reason Two: It’s Expensive and Time-Consuming

Most exotic pets come with a hefty price tag, and I guess if you’re an especially rich person, that’s not an issue for you. But there is no getting around that bats in particular have a lot of special accommodations that they need to be housed appropriately. (And you do want to house your pets appropriately, right?)

The most obvious factor is that bats fly. Flying is a big part of their life. So no matter how small the species is, it is going to need a lot more space than similarly-sized mammals because it needs open space to fly in. If bats aren’t permitted to fly, they often get overweight, or may attempt to fly anyway and end up seriously hurting themselves. They can’t have their wings clipped to prevent long-range flight like birds can, so a bat escaping and flying away is a serious danger.

Essentially, a good bat enclosure is going to be the size of a good bird flight cage. Why not have a nighttime cage and let the bat roam the house during the day, as some people do with birds, you ask? Well, the main answer is that bats naturally seek the highest points in an area to land on. For some small bats with especially adept claws, this will be your ceiling. Or the top of your cabinets. Anywhere inconvenient for you to reach. Small bats are also especially good at slotting themselves into crevices- some species sleep underneath loose tree bark. Imagine trying to find one in a stack of dishes. Large fruit bats are somewhat clumsy fliers and in a variable, closed environment like a house risk seriously hurting themselves crashing into something. Also, unlike birds, they pee and poop in large amounts, separately. The list goes on.

But most importantly, bats are nocturnal and in some cases crepuscular. Unless you’re there at night supervising their outside time, their most active periods would be spent cooped up inside a small cage. Bats need flight cages, preferably outdoor ones, so they don’t stink up your whole house.

Panorama of an appropriately-sized bat enclosure.

Ok, so you’re gonna need a lot of space and building materials to house your bats. And I mean bats plural- almost all bat species are highly social and require companions of their own kind. And I mean require. I spoke about bats kept in solitary for health reasons- it was critical that we at least allow them to spend part of their day in the company of other bats. In fact, they became extraordinarily anxious about it, particularly if they weren’t used to it- I had one, normally calm bat almost jump into my arms due to being so distressed after having to spend the night alone. Other bats, kept isolated each night due to age and the fear that they would fall or get attacked by younger, stronger ones when keepers weren’t around, still desperately wanted to be returned to the group each morning. Even if the group was hell-bent on beating them up.

Bats have a myriad of different social structures, but the fruit bats commonly kept in captivity have social behavior comparable to primates like baboons or macaques. They need large groups- ten or more- to adequately fulfill their social needs. And large groups need large enclosures. Housed in too-small groups, bats become depressed, lethargic, and may stop eating and die. Housed in groups that don’t have adequate living space, bats will most likely fight with one another and end up with injuries.

This leads me to vet bills. Oh, vet bills! You’re going to need to find a vet who’s willing to treat bats in the first place, and then you’re going to pay up a lot of money. And even then, the vet may not know enough about bats to treat one accurately. Bats are physically unique mammals with unique problems- an exotic pet vet may not know, for example, that if a bat is seen ‘cradling’- hanging by both thumbs and feet- it can be a sign of chronic pain or joint problems which may end up leading to the bat needing to be euthanized if not quickly controlled.

Speaking of euthanasia, there’s another serious risk with bats. You see, bats are considered rabies vector species. This means it doesn’t matter if they’re vaccinated (if you can get even ahold of a bat-appropriate vaccine)- if your pet scratches or bites someone and draws blood, and that someone reports it, Animal Services legally have to come in, seize your pet, and euthanize it to test it for rabies. There was a particularly tragic story circulating on tumblr about a blogger’s pet fox, another rabies-vector species, that suffered this fate.

Okay, but say you have built your bats a nice enclosure, with a good-sized colony for them to socialize with, and you even have a vet that knows how bats do. Now you’re going to need to deal with the daily cost of feeding a bat. If it’s a fruit bat, it’s going to need to eat a carefully balanced diet of multiple types of fresh fruit and vegetables* each day, plus vitamin supplements since our commercial fruit has poor nutritional value compared to wild species. Fruit is expensive and spoils quickly, which means a lot of shopping. And it must be fresh fruit- canned fruit is high sugar/low nutrition and there is no such thing as bat kibble, considering they won’t touch food that doesn’t have a high moisture content. I have heard of some zoos having success with canned ZuPreem marmoset diet, which retails between 2-3 dollars per can, in addition to fresh fruit.

(*The diet at the facility I worked at included: apples, pears, kale, sweet potato, carrots, grapes, and bananas, plus the supplement.)

There is also the question of enrichment. You can’t leave a colony of bats alone all day with nothing to do- they are extraordinarily intelligent animals with a penchant for being self-destructive if not adequately entertained. Different, high-quality enrichment should be provided for bats each day, which is a time-consuming process by itself.

Finally, a fact which often surprises people: bats can live for 20-30 years in captivity. You may be feeding them that expensive diet and cleaning that big cage every single day for decades.

Reason Three: You Know, Ethics and Stuff

It is certainly possible for an individual with a great deal of money, space, and time to build an adequate enclosure, provide the appropriate diet, and perform the daily husbandry necessary to humanely keep a small colony of bats under private ownership. But once you get to that point, the bats you own aren’t really your pets the way most people think of pets. Bats kept in a stable social group aren’t going to be interested in socializing with you– you’re not a bat. Maybe you can give them a treat every now and then, and they like that, but overall they’re going to be less stressed if you’re not hanging around them, staring, acting like a predator.

It’d be sort of like having a school of flying, mammalian, tropical fish. For display only.

Most people who want bats as pets do not want this type of pet. They want to be able to reach up and cuddle a bat, carry it around, show it off to their friends. They want to feel a ‘connection,’ a bond, with these adorable animals; they want them to be excited to see them and depend on them.

But to make a bat need you, to want to have contact with you and interact with you in a more-than-superficial manner, you have to do some nasty things. You have to take the baby bat away from its mother and hand-rear it. And I have met some hand-reared bats: many of them are a mess. They may never learn how to fly, they may have nutritional deficiencies (the best formula doesn’t match mom’s milk), and worst of all, they may not learn how to socialize with other bats. To see a bat seek out human contact rather than bat contact is always sad to me, because unlike the other bats, I can’t be there twenty-four hours a day. I can’t sleep beside the bat, groom the bat, or do a myriad of other normal bat behaviors- including sex. Yes, some hand-reared bats will try to have sex with their human caretakers, because that is normal bat behavior. It’s funny- until it’s sad.

By hand-rearing a bat and never giving it the opportunity to socialize with its own kind, you are effectively isolating it. You can’t fill the social need that a whole colony does. Isolated bats often overgroom themselves, bite themselves, stop eating. Bats are already anxious animals, given the number of predators they have- the stress of being constantly handled, moved, or kept in areas that don’t feel safe can literally kill them. Even the best accredited zoo facilities sometimes have this problem with their bats.

Dogs, cats, and other domesticated animals have had thousands of years to temper their anxiety, emotional needs, and physical needs to better match human lifestyles. A dog can be totally dependent on a human caretaker and be happy, healthy, and an excellent pet. If you want an animal to have that kind of relationship with you, please get a dog.

Bats do not make good pets.

Read on: I’ve discussed exotic animal ownership before, in my essay on three considerations to have before adopting an exotic pet. To see other articles I’ve written on topics in biology, head to my nonfiction section!

Bats! They yell at things, sometimes with their noses. What’s up with that? I guess we’ll talk about it and when it started happening. Can you tell I haven’t written an intro to a nonfiction post in a while?

Before we really get started, let’s have a brief primer on what echolocation actually is for those who don’t know. To put it simply, it’s using sound echoes to get information about what’s around you. Sound travels in invisible waves, like ripples on the surface of a pond, which are deflected by the presence of solid objects. A bat screams and then listens for these sound deflections- echoes- and is able to use the way they sound to determine things like the distance, texture, size, and direction of the object, among other things.

When I say the bat ‘screams,’ I’m not being facetious, by the way. The loudness of a bat’s echolocation call, surprisingly, doesn’t have much to do with the size of the bat. Even a tiny bat weighing four grams may be able to emit a shockingly loud 128 decibel sound. For comparison, a jet engine 100 feet away from the listener has a loudness of about 130 db. Many bat species have calls loud enough to damage human hearing- which makes it lucky for us that the frequencies are too high for us to hear.

Bats are able to yell this loud without damaging their own hearing only to a special adaptation that actually causes them to go deaf just before a call is emitted- the muscles in the middle ear actually pull apart the hammer, anvil, and stirrup bones so that sound can’t travel to the cochlea. The muscles relax to allow the bones to reconnect as the sound echoes back.

I wish I could have found a gif of this amazing adaptation, but our imaginations will do. The ossicles- ear bones- comprise of the aforementioned hammer, anvil, and stirrup, which are pulled apart by a muscle contraction to prevent the bat going deaf from its own screams.

Okay, now hoepefully everyone’s up to speed on just what echolocation is. So. The evolution of echolocation in bats is a point of contention among evolutionary biologists. The problem lies largely with a poor fossil record for bats, since their teeny low-calcium bones don’t preserve well. There are few transitional proto-bats in the fossil record, and even fewer fossilized structures that might indicate whether or not an ancient bat was able to navigate via scream. Add to that the fact that there are at least two origins for echolocation in modern bats, and you get a lot of phylogenetic fun.

But let’s start at the beginning. One of the earliest bat fossils ever found is the Eocene bat Onychonycteris. Now, prior to this discovery, there was a lot of debate as to whether bats evolved the ability to fly before the ability to echolocate or vice versa. (Echolocation would presumably still be helpful for a nocturnal gliding mammal, too.) Onychonycteris put that argument to rest because the skull was preserved well enough to show that it lacked some of the specialized hearing anatomy found in echolocating bats. So, as far as we know, flight came first.

Here is the holotype specimen for Onychonycteris. Note the long tail and the claws on the ends of the wingtips, both traits that modern bats have lost.

By the way, while googling for images of this specimen, I stumbled upon the ARK: Survival Evolved profile for this animal, and I’ve probably never been so quietly furious in my entire life. Spot the inaccuracies.

BATS DON’T DESERVE THIS, VIDEO GAME MAKERS.

Anyway, back to the origins of echolocation. So, we can settle at least one debate for the moment- the best evidence we have suggests that bats learned to fly before they learned to scream. But in this case, when did echolocation appear? Here again we have a lot of head-butting, not in the least because the relationships between bat families has traditionally been a massive headache to detangle.

Bats, you see, comprise about one-fifth of all mammal species, with over 1,200 species known, and more constantly being discovered. In that sense, they’re the rodents of the sky, except that they aren’t closely related to rodents at all. At one point it was thought that primates were some of bats’ closest living relatives, based on morphology studies comparing the anatomy of Pteropodids to monkeys. (That belief also assumed that Megabats and Microbats didn’t share a common ancestor, but we’re pretty sure they’re all in the family now.) But the monkey thing is bunk now thanks to genetic studies, which put bats on a different spot in the family tree: as a sister group to Feraeuungulata, a group comprised of all ungulates (hoofed animals, as well as whales) and all carnivores (dogs, cats, bears, etc). Basically, what you should take away here is that bats are a weird group kind of all on their own among the mammals. They’re separated from their closest living relatives by over 60 million years.

Bats and examples of their closest living relatives… really.

So the bat family tree itself took a lot of time to detangle. Even once molecular evidence sorted some things out, there were still more questions. The most recent grouping of bats discards the old terms ‘Megabat’ and ‘Microbat,’ used to refer to big fruit-eating bats and little shouty bats, respectively (though ‘megabat’ is still used to refer to Pteropodids), and adds the new terms Yinpterochiroptera and Yangochiroptera. Yinpterochiroptera, besides being a pain to spell, includes traditional megabats- Pteropodids, the flying foxes- as well as leaf-nosed bats, horseshoe bats, false vampire bats, and a few others, which used to be considered microbats. Yangochiroptera is easier to spell and includes all the rest of the bats traditionally called microbats.

Are you tired yet? I’m very tired.

Now that we have that out of the way, we have to consider which bats in this modern grouping echolocate, and which bats don’t. That should give us a clue as to when the ability evolved- for example, if all bats have it, it must be an ancestral trait; or if one branch of the tree has it, it must have evolved at the beginning of that branch; or if all but one branch has it, it must have been lost in that branch. Easy-peasy, right?

Here’s a phylogeny of bats that can and can’t echolocate, with boxes referring to echolocating groups colored in green.

You’re about to see this poorly-constructed diagram a lot.

Oops! We have a problem. There’s no clean echolocation monophyly here- that is, no easy branches of this tree we can ‘trim’ to collect all the echolocating bats in one group. The big problem seems to be that Rousettus genus up there, which evolved from a group of bats whose other living descendants don’t have echolocation but evolved from another group of bats that do. We’re talking about a gain/loss/regain situation here, which evolutionary biologists absolutely hate. (But it isn’t impossible.)

In fact, there’s another wrinkle to the matter which either clears everything up or throws everything into more chaos, depending on your point of view. The three green groups of bats all have somewhat different ways of echolocating, which I’ll go into more detail about later. This actually led some biologists to suggest that bats evolved echolocation three different times, like so:

Pluses indicate echolocation was gained, minuses indicate that the ability was lost.

But three separate events is a bit much for other evolutionary biologists, who postulate that no, echolocation only evolved twice, damnit, and the common ancestor of all modern bats had the capability. Like so:

Checkmate… ish?

By now you’re probably as sick of looking at that phylogeny as I am, but let me finish up by saying that more evidence points to the second theory than the first, which is nice, because gaining a trait twice is still more parsimonious than gaining it three times, and it lets evolutionary biologists sleep a little better at night. Currently. Probably. Let’s move on.

As I mentioned earlier, the three groups of bats that can echolocate all have slightly different means of doing so, which was the source of some of that phylogenetic kerfuffle. The Yangochiropterans, i.e. the little guys, echolocate using their larynx. They open their itty bitty mouths to do it, like so:

A little brown bat, screaming.

Leaf-nosed bats, horseshoe bats, and other Yinpterochiropteran bats in the Rhinolophoidea superfamily (are you sick of bat phylogeny yet) also echolocate using their larynx to produce sound. However, the sound doesn’t come out of their mouth, but their nose. So, bats in this superfamily have weird, horrible noseleafs specially shaped to shoot out sound. Because they use their noses and not their mouths, they can actually echolocate continuously without having to pause to, say, take a breath or eat an insect.

A horseshoe bat.

One family among Yangochiroptera, the New World leaf-nosed bats (Phyllostomidae), also echolocates through the nose- an ability that evolved separately from that of the Yinpterochiroptera nose-yellers. They have convergently evolved similar noseleaves.

A carefully curated selection of leaf-nosed bats.

Old world vs new world leaf-nosed bats: a lesser false vampire bat (Megaderma spasma) compared with a spectral bat (Vampyrum spectrum). Though they look similar, they are from opposite sides of the bat family tree and evolved their nose-echolocation separately. Confusingly, the spectral bat is also sometimes called the false vampire bat. Neither species drinks blood.

Knowing this, the theory that nose-echolocation in Yinpterochiroptera evolved independently from mouth-echolocation in Yangochirpotera makes more sense, even though that’s probably not what happened. However, we’re fairly certain that the third group of bats, the Rousettus fruit bats, DID evolve their echolocation completely separately from the other two groups. Why? Because they don’t echolocate with their larynx, or throat. They echolocate by clicking their tongues. Hence, their faces aren’t a horror show.

An Egyptian fruit bat (Rousettus aegyptiacus) at the Omaha Zoo.

The particularly interesting thing about Rousettus bats is that they are nested within Pteropodidae. Nearly all Pteropodids are crepuscular fruit-eating bats, who neither need to chase insects nor navigate in the dead of night. Hence, the loss of echolocation in the group. However, despite the fact that they eat fruit, Rousettus bats are nocturnal, and live in caves during the day. This is likely why they regained the ability to echolocate, albeit in a new way.

So: these are the three main ways to echolocate (though there might be a fourth secret way… wait for it). To review the facial adaptations of the bats that use each: bats with large ears and small eyes are probably mouth-echolocators from the superorder Yangochiroptera, while bats with large ears and weird nose ornaments are probably nose-echolocators from the Rhinolophoidea superfamily of Yinpterochiroptera (or Yangochiropteran New World leaf-nosed bats), and bats with large eyes, small ears, and adorable ickle faces either don’t echolocate or happen to be tongue-clicking Rousettus.

Here we see examples of yellers, snootlers, and clickers: Eastern red bats, Honduran white bats, and, uh, Rousettus. Together, they form the most amazing bat musical group you’ve probably never heard of.

Now that we’ve gone over the different forms of evolution, we need to turn to how echolocation is used. The one thing that all bats with echolocation use it for is navigation through dark places, of course, but secondary functions have developed as well. For most echolocating bats, that secondary function is to detect bugs and eat them. Here’s a video with visual representations of how a bat ‘looks’ around an area with sound, comparing echolocation for navigation to echolocation used to chase a target.

The sound a bat makes to echolocate is altered based on almost innumerable factors. The frequency of a bat’s call, for example, corresponds to the size of its prey- smaller insects get higher frequencies. (The reason bats use relatively high wavelengths to hunt for insects is actually because the sound wavelength has to be shorter than the insect’s wing to be effective!) However, in areas with multiple bat species hunting in the same area, each species may stick to a narrow bandwidths of sound to avoid competition, sort of like having their own species-specific radio station. On the other hand, bats who fly in cluttered areas like forests rather than open areas are forced to use broader bandwidths with shorter call lengths in order to be able to differentiate the sound of echoes bouncing off of things like leaves and trees from the echoes returning from insects, in order to both chase prey and not crash into things.

These are just a few examples of how bat calls can differ; in fact, some near-identical species of bat can only be differentiated by listening to their hunting calls. Collecting bat calls is one of the most common ways to survey which species of bat are in an area, other than actually catching them.

Here’s a video of a bat using echolocation to hone in on the location of insect prey. Note how the bursts of sound come faster as the bat draws closer and needs more detailed information. (And listen for the distinct crunching noise of the bat capturing the moth.)

Insects, however, are not passive actors in all this. Indeed, bats and their prey have been involved in a technological arms race for millenia. Most moths and butterflies don’t have ears, and can’t hear. But certain species of moths happen to be the favorite food of certain species of bats, who hunt by echolocation. This drove the moths to evolve- ironically, in multiple different lineages- simple ears, so that they can hear the bats echolocation calls approaching and dodge.

In a surprising twist, moth ears evolved on their waists (thorax), not on their heads. In an even more surprising twist, tiny ear mites have evolved to attack the moth’s tiny ears; however, they only attack one of the moth’s ears so that the moth can still hear enough to save itself and its tiny hitchhikers from being eaten by a bat. That’s cool, I guess.

In response to the appearance of moth ears, some bats have ramped up their echolocation abilities in different ways. For example: some bats have simply changed the frequency of their echolocation to one the moths can’t hear. Other bats have evolved ‘whisper’ echolocation, i.e., echolocation so quiet that the moth’s simple ears can’t detect it. The ear shapes of these bats have changed to better reflect their own teeny cries back to them.

The “just turn your entire face into an ear, just do it” strategy, employed by this barbastelle bat.

The reason for this ghost-faced bat’s bizarre face flaps has not been studied, but it’s possible it evolved for a similar whispery purpose.

Other bats, though they use echolocation to detect the general location of their prey, actually shut up as they get close so the moths can’t detect where they are. Instead, these bats use super-sensitive hearing- even more sensitive than ordinary bat hearing, which is pretty damn sensitive- to pick up the tiny sounds of a moth’s wings moving, or even their feet moving along a surface like a leaf. The bats who use this strategy tend to be the ones with the most ridiculous ears.

Townsend’s big-eared bat. I mean, what else could you say about this guy. Ears.

One can assume that the weirder a bat’s face, the more specialized its insect prey has gotten, with a few exceptions. On the other hand, generalist beetle-eaters (most beetles can’t hear) like this big brown bat get away with relatively normal faces.

And look at those cute beetle-crushing teefers!

Bats that eat fruit or nectar only need to use echolocation for navigational purposes if they use it at all, so their equipment tends to be less specialized as well. However, a lot of herbivorous bats have still managed to evolve bizarre faces. Mainly for sex purposes. Because apparently, there’s nothing sexier than a faceful of horrific flesh flaps.

Wrinkle-faced bats; a rare member of the nose-echolocator group that doesn’t have a noseleaf. Not only do these bats have faces that look like like flesh-colored cottage cheese- possibly having something to do with shaping the sound of mating calls- the males have ‘skin masks’ that they can pull up over their chins, as seen in the photo. Maybe this is to better distribute the musky odor from their chin glands onto their face. Maybe it’s just to distress me. I don’t know.

Male hammerhead bats, which are non-echolocating Pteropodids, have enlarged snouts with weird nose flaps used for producing buzzes and honks that are apparently irresistible to females.

In any case, the ways that the weird faces of bats reflect and shape sound is surprisingly understudied, given how much diversity of form there is among the faces of bats. What we do know is that one of the most important tools for echolocation is a bat’s tragus, which is a fleshy protrusion within the ear. Humans have tragi as well, which some of you may already know if you have a tragus piercing.

Human and bat tragi.

Interestingly, non-echolocating Pteropodids don’t have tragi (see the ears of the hammerhead bat above), and instead rotate their ears to determine sound direction. But echolocating bats (sans Rousettus) keep their ears fixed in position, as seen in the video below.

Humans, too, have mostly immobile ears, which is why we have convergently evolved our own tragii to alter sounds based on the direction they’re coming from relative to our heads. But the variation in the shape of bat tragii- so diverse that a tragus shape can be used to identify differences between species with nearly identical characteristics- suggests that bats use them in much more complex ways than we do.

Diversity among bat tragii. Unfortunately, not much has been studied regarding how tragus shape affects sound.

Humans mainly use their tragii to determine whether a sound is coming from in front or behind us on a horizontal plane- the shape of the tragus causes sounds coming from behind to be slightly delayed. However, bats also use their tragii while echolocating to determine the vertical position of objects that are in front of them, based on the angle the sound bounces back at.

In one study, big brown bats were trained to choose between pairs of marbles suspended at different heights- the pair that was closer together would earn them a reward. However, when their tragii were glued down, the bats had a much harder time determining which pair was the correct one. Other studies have confirmed that altering the tragus makes bats struggle to hunt via sound, though they are surprisingly good at adjusting their behavior.

Other research has determined that wrinkles in the pinna (the rest of the bat’s outer ear) and on other parts of the face help bats detect the general direction of sound, though exact specifications on how all this works aren’t yet well-studied. What has been studied a bit more is how nose-echolocating bats use their noseleafs to shape sound as it comes out. This was discovered, funnily enough, when scientists thought it would be hilarious to cover the noseleaf of a horseshoe bat in petroleum jelly and record changes in the sound quality of its echolocation.

A horseshoe bat, like the one in the study. Side note, please don’t cover bats in jelly. Unless it’s a fruit bat. A fruit bat’d probably enjoy it. They’re kinky.

What the noseleaf appears to do is to split the bat’s echolocation beam into two parts- a broad, general spread that lets the bat have a wide field of sound-based ‘vision,’ as well as a narrow, focused beam that lets the bat focus in on things directly ahead. This enables the bat to retrieve information on the general environment it’s flying through at the same time as it is honing in on insect prey- important for horseshoe bats in particular, since they tend to fly very close to the obstacle-filled ground. Abilities like these are probably why bats with noseleafs are considered among the most sophisticated and skilled echolocators among all bats, able to detect tiny details like changes in the movement of an insect wing through sound.

Also, their echolocation sounds really cool on a bat detector.

There is a lot more stuff that’s been studied regarding echolocation in bats that I could discuss, but we’ve already gone on a bit long here. So let’s close up with a very recent discovery regarding bat echolocation that could possibly shake up the entire field: Pteropodids other than Rousettus species might actually be able to echolocate.

Eh? I can hear you saying. Didn’t I devote a good portion of this article to saying how Pteropodidae can’t echolocate? The fact that they rely on eyesight and are crepuscular, not nocturnal? How can this be a thing that was only recently discovered (in 2014)?

Well, as previously discussed, there are three well-documented ways that bats echolocate: laryngeal echolocation through the mouth, laryngeal echolocation through the nose, and tongue-clicking. Pteropodids definitely don’t use any of these methods. However, they are capable of navigating decently well in complete darkness, albeit not as gracefully as other bats, suggesting that they do have some form of aural navigation.

Like many ‘novel’ animal discoveries, this one came from local knowledge- a man on a bus in Indonesia mentioned to two visiting Israeli scientists that he knew of fruit bats that made clicking sounds with their wings. The scientists, upon trawling the available scientific literature, only found one reference to the behavior in pteropodids from a 1988 paper suggesting one species of bat (the cave nectar bat, a close cousin to Rousettus bats) ‘clapped’ its wings to make clicking sounds, but drew no conclusions as to how those sounds were used.

The scientists tested the cave nectar bat and two other pteropodid species- the lesser short-nosed fruit bat and the long-tongued fruit bat- via recording the sounds they made while flying in a small, completely dark room. Much to their surprise, all three species made audible short click-like sounds as they flew, and were able to avoid large obstacles, though they tended to crash into smaller ones like cables. When tested in light conditions, the bats clicked less than they had in the dark.

Considering the relationship these bats had to Rousettus, the authors wanted to ensure that the bats weren’t producing the sound with their tongues, so they sealed their mouths in some trials and even anesthetized their tongues. The bats still clicked. Video showed that the clicks matched perfectly with the bats’ wingbeats.

The authors were able to prove that this behavior was not, as the earlier study suggested, caused by wing ‘clapping’- when the wingtips of the bats were padded, the clicking sound could still be heard. The exact mechanism of how these clicks are produced is not yet known.

While none of the bats were particularly awesome at using this form of echolocation (they tended to need multiple tries to land using click navigation versus a single try to land using vision) they were definitely able to use it to differentiate between things like a solid block and a soft cloth. Interestingly, these bat species were all from different spots in the Pteropodid family tree, as shown in this figure from the paper:

The authors suggest that this could mean that all pteropodids could feasibly have this rudimentary form of echolocation, which would have evolved after the loss of laryngeal echolocation in this group. Or, some echolocating ability could be so useful for bats that they simply re-evolve it spottily based on their particular behavioral needs. As far as I know, no further studies have been published yet on this remarkable discovery, and the initial study was based only on nineteen different animals, so as yet it all remains up in the air. But it could change- again– the whole paradigm that scientists had finally started to settle on about how echolocation evolved in Chiroptera.

Bats, man.

References and Further Reading

Boonman, A., Bumrungsri, S., & Yovel, Y. (2014). Nonecholocating fruit bats produce biosonar clicks with their wings. Current Biology, 24(24), 2962-2967.

Chiu, C., & Moss, C. F. (2007). The role of the external ear in vertical sound localization in the free flying bat, Eptesicus fuscus. The Journal of the Acoustical Society of America, 121(4), 2227-2235.

Denzinger, A., Siemers, B. M., Schaub, A., & Schnitzler, H. U. (2001). Echolocation by the barbastelle bat, Barbastella barbastellus. Journal of Comparative Physiology A, 187(7), 521-528.

Henson, O. W. (1965). The activity and function of the middle‐ear muscles in echo‐locating bats. The Journal of physiology, 180(4), 871-887.

Houston, R. D., Boonman, A. M., & Jones, G. (2004). Do echolocation signal parameters restrict bats’ choice of prey. Echolocation in bats and dolphins, 339-345.

Jones, G., & Teeling, E. C. (2006). The evolution of echolocation in bats. Trends in Ecology & Evolution, 21(3), 149-156.

Jones, G., & Holderied, M. W. (2007). Bat echolocation calls: adaptation and convergent evolution. Proceedings of the Royal Society of London B: Biological Sciences, 274(1612), 905-912.

Li, G., Wang, J., Rossiter, S. J., Jones, G., Cotton, J. A., & Zhang, S. (2008). The hearing gene Prestin reunites echolocating bats. Proceedings of the National Academy of Sciences, 105(37), 13959-13964.

Müller, R., Lu, H., & Buck, J. R. (2008). Sound-diffracting flap in the ear of a bat generates spatial information. Physical review letters, 100(10), 108701.

Nikaido, M., Harada, M., Cao, Y., Hasegawa, M., & Okada, N. (2000). Monophyletic origin of the order Chiroptera and its phylogenetic position among Mammalia, as inferred from the complete sequence of the mitochondrial DNA of a Japanese megabat, the Ryukyu flying fox (Pteropus dasymallus). Journal of Molecular Evolution, 51(4), 318-328.

Simmons, N. B., Seymour, K. L., Habersetzer, J., & Gunnell, G. F. (2008). Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature, 451(7180), 818-821.

Spangler, H. G. (1988). Moth hearing, defense, and communication. Annual review of entomology, 33(1), 59-81.

Springer, M. S., Teeling, E. C., Madsen, O., Stanhope, M. J., & de Jong, W. W. (2001). Integrated fossil and molecular data reconstruct bat echolocation. Proceedings of the National Academy of Sciences, 98(11), 6241-6246.

Teeling, E. C., Scally, M., Kao, D. J., Romagnoli, M. L., Springer, M. S., & Stanhope, M. J. (2000). Molecular evidence regarding the origin of echolocation and flight in bats. Nature, 403(6766), 188-192.

Tsagkogeorga, G., Parker, J., Stupka, E., Cotton, J. A., & Rossiter, S. J. (2013). Phylogenomic analyses elucidate the evolutionary relationships of bats. Current Biology, 23(22), 2262-2267.

Wotton, J. M., & Simmons, J. A. (2000). Spectral cues and perception of the vertical position of targets by the big brown bat, Eptesicus fuscus. The Journal of the Acoustical Society of America, 107(2), 1034-1041.

Yovel, Y., Geva-Sagiv, M., & Ulanovsky, N. (2011). Click-based echolocation in bats: not so primitive after all. Journal of Comparative Physiology A, 197(5), 515-530.

Zhou, X., Xu, S., Xu, J., Chen, B., Zhou, K., & Yang, G. (2011). Phylogenomic analysis resolves the interordinal relationships and rapid diversification of the Laurasiatherian mammals. Systematic biology, syr089.

Zhuang, Q., & Müller, R. (2006). Noseleaf furrows in a horseshoe bat act as resonance cavities shaping the biosonar beam. Physical review letters, 97(21), 218701.

How Can We Tell When Animal Welfare is Good?

In the previous article, I gave a drawn-out description of some of the theory and history of modern animal enclosure design. But I haven’t much discussed the thing itself. I am, of course, going to– but first we have to lay down a few ground rules.

Remember when I was describing the difficulty I had designing my axolotl tank? Namely, the part about what I thought was aesthetically pleasing being different than what they actually found comfortable to live in. Similarly, it is hard to gauge the quality of an animal’s captive environment by looks alone. In modern husbandry, an animal’s welfare is determined on the basis of three main things, which are often interconnected:

Physical health: the most basic welfare requirement, and the most self-explanatory. Animals should be neither emaciated nor overweight and should not be showing signs of illness or injury. The early “sterile” zoos attempted to achieve this.

Presence of abnormal behaviors: this refers to behaviors such as stereotypies, self-injury, anhedonia, cognitive bias, et cetera, as well as exaggerated negative forms of normal behaviors such as overgrooming. The introduction of enrichment in zoos after the 60s served as a way to try to reduce or eliminate these types of behaviors.

Presence of species-typical behaviors: in other words, the animal performs behaviors that it might have if it lived in the wild. A monkey climbs, a cheetah scent-marks, a bird preens. The presentation of positive behaviors, rather than just the reduction of negative ones, is a relatively new concept to animal welfare, but one that is being implemented in many zoos, labs, and even farms around the world.

Now that I’ve brought up wild behaviors, though, I’d like to emphatically say that the goal of animal enclosure design is not to mimic wild conditions. Firstly, this is impossible even for the best captive situations. Secondly, what ideal wild conditions even are is not something easily defined. Consider, again, the wild axolotl: I am certainly not trying to mimic their polluted, drained wild habitat in my tanks. I am also not introducing their natural predators, parasites, competitors, and et cetera, even though that, too, would be more appropriately wild. The lives of wild and captive animals are very different- arguably, one is not objectively better than the other. Many wild animals have absolutely miserable- and short- lives.

Not, mind you, that many captive animals don’t suffer similarly abysmal fates. It’s simply that the stresses placed on wild and captive animals are very different. The largest of these differences is that most of the stresses placed on wild animals occur in temporary bursts followed by a period of relaxation. For example, a lioness goes hungry for several days, causing her great stress, but then makes a kill and is satiated for a good 48 hours. The impala that the lioness chased, on the other hand, are temporarily highly stressed at her pursuit over the course of those days, but have the opportunity to come down from that anxiety each time she feeds or gives up the hunt.

Neither predator anxiety or hunger should (theoretically) be a major source of stress for a captive animal. Instead of brief bursts of intense stress, captive animals suffer from low, constant levels of chronic stress. For example, the temperature in a reptile enclosure may constantly be just a few degrees colder than the reptile’s ideal climate range. This does not rapidly kill the animal as starvation or predation would, but it does begin to contribute to a gradual decline in health as the reptile’s body struggles, day in and day out, to cope.

One of the biggest concerns in captive animal welfare, then, is actually nearly invisible to us- this is why, again, I frown on short-term visual assessments as a good means of assessing welfare. Chronic stress is hard to measure accurately, especially in non-mammals whose needs and body language are less familiar to us. This is another reason why it is good to look for the presence of positive (i.e., species-typical) behaviors rather than just negative (i.e., abnormal) behaviors when assessing welfare. Animals under constant low levels of stress will often put their energy into vigilance or hiding behaviors- appearing as though they are not doing anything for long stretches of time.

Of course, the caveat to all this is that you need to have some understanding of what constitutes a suite of normal, species-typical behaviors for the animal in question, and in many cases this is difficult to impossible to obtain. In some cases, we are lucky enough to have extensive observations of wild animal behavior. For example: captive lions that spend eighteen to twenty hours each day sleeping or lying down might seem bored or too depressed to do anything else, but this ‘laziness’ is actually species-typical behavior for wild lions (who spend, on average, only three hours each day up on their feet). So this long-term lounging behavior is actually a positive sign for their welfare.

However, more often than not, we don’t have the luxury of these wild accounts, especially for many animals which are extremely difficult to observe in the wild, or simply haven’t warranted enough long-term study from the scientific community. This includes many species of birds, reptiles, fish, and amphibians. Those trying to care for these animals in captivity are then left with guesswork as to what their normal behavioral suite looks like, based on, say, what they might know about the behavior of closely-related animals, or those in similar niches. It is not a perfect solution by any means.

Pet owners, I feel, are some of the worst offenders as far as misunderstanding the wild behavioral suites of their animals go. In many cases they don’t even know the country of origin of their exotic fish or bird, much less its natural lifestyle. You should not buy any animal, ever, without knowing where it came from and what it does to make a living.

With all that said, the best animal enclosures will work to provide opportunities for species-typical behavior while minimizing chronic stressors. Sometimes, surprisingly enough, this can mean substituting temporary stressors instead! One example of this would be veterinary examinations and treatments- usually terribly stressful for the animal at the time, but overall good for preventing injury or disease from causing chronic stress. Think about this the next time you balk at going to the doctor or dentist.

Let’s begin a more detailed discussion on positive enclosure design with a very controversial element: available space.

Space

Space requirements for captive animals is a tricky subject. It is generally easily visible to observers and is often the first thing to be criticized about enclosures by visitors to zoos and other places. But most of these visual assessments are based on the amount of space a similarly-sized human would feel comfortable in, not the actual animal. So how can we assess how much space an animal needs to be free from anxiety and frustration?

At the most basic level, the minimum amount of space an animal needs should allow it to move unrestricted. The animal should be able to stand up, lie down, and turn around unhindered. This minimum is acceptable for very short-term housing such as veterinary cages, in which case limited space is important to prevent the animal from straining itself, as well as providing easy access to the animal so that it can be treated. In some cases, such as when the animals are being transported or treated for serious maladies, even more restrictive housing is acceptable, but again, this should be extremely-short term.

There is some controversy even in this most basic space requirement when it comes to large snakes. Most pet snakes and many zoo snakes are kept in enclosures that are too small to allow them to stretch to their full length. The most common explanation I’ve heard given for this is that the snakes are made more anxious by excess open space, and don’t ever really need to stretch out fully. Indeed, this mindset was so pervasive that I believed it myself for a while. However, research suggests that this explanation serves the snake owner more than the snake itself. To start with, snakes have a single, elongated lung that can take up as much as half their body length which must have room to expand in order for the snake to breathe properly. Also, many wild snakes completely straighten their bodies out in order to resolve digestive issues. Captive snakes in enclosures that are shorter than their total body length are unable to perform this behavior. (Photo from Warwick et al., 2013.)

Another form of short-term housing is a crate or kennel area that is blocked off from the main enclosure (which could be a yard or even your house). Again, this should be a temporary holding area, used for feeding, sleeping, access to the animal, or simply keeping the animal contained while the rest of the enclosure is cleaned. Some animal species may find crates or stalls comfortable and secure spaces to sleep in so long as they are given access to the larger enclosure for the bulk of their active hours.

Many owners practice “crate training” with their dogs in order to secure them during periods of alone time or travel. While this is often successful, there are some caveats to this method. If crating is used as a punishment, or the dog is kept confined while vocalizing or attempting to escape, being crated will become a negative, stressful experience. Likewise, a dog should not be kept crated for more than three active hours (i.e., hours the dog is not spending asleep) each day. (Photo source, CC by SA 3.0)

Temporary confinement can also occasionally be a positive thing for an animal. Briefly restricting access to certain areas of the enclosure increases the amount of anticipation and excitement the animal feels before being allowed back in. Calves and baby goats, for example, spend much more time exploring and playing in a paddock if they are only given access to it for part of the day than if they are given free access to it all the time. Of course, if this restriction goes on too long, anticipation can give way to anxiety and frustration.

Beyond temporary areas, it’s hard to determine how much space an animal needs in its entire enclosure. The size of an animal’s body is not always a good indicator of how much space it needs. A monitor lizard, for example, is much larger than a rat, but spends much less time moving around due to a lower metabolism. So enclosure space isn’t necessarily a function of animal size alone but animal size as a function of animal activity level.

Yet even this is an oversimplification. Say you provide that highly active rat with a bedroom-sized floor space to run around in, with nothing to get in its way. The likely result will be that the rat will only utilize a tiny fraction of that space- namely, the corners and the parts of the floor directly adjacent to the walls. Why is this?

The answer is simple: rats are delicious, and running out into wide-open spaces is an excellent way for them to advertise that deliciousness to, say, a hawk. So that rat is going to avoid spaces where it feels exposed and vulnerable, effectively rendering most of the glorious open space you’ve provided it with useless.

So not only do you have to consider animal size and animal activity level, you also have to consider what activities the animal actually performs. In the case of the rat, you can convert all that useless space into usable space by providing it with a multitude of tunnels, shelters, and other hiding spaces throughout.

A much more suitable use of space for a rat enclosure than the open-field environment (used for testing in the video above). Note how the use of vertical climbing areas increases the amount of space available for use.

Similarly, for some animals, floor space matters little if at all. Perching bird species and arboreal climbers like climbing snakes and monkeys may feel very exposed touching what they perceive as the ground level. So again, that wide-open space you provide them will not work. These animals will need high vertical spaces rather than large floor spaces.

With this in mind, I’d go as far as to say that the amount of space you provide an animal matters much less than how you use that space. And this, again, is entirely based on what the particular species of animal needs.

“Cat shelves” are steadily becoming more popular as a way for cat owners to allow their pets to utilize vertical space.

Animal species is actually not the only factor you need to take into account when considering how an animal will use a space. Male and female animals may be prone to using space in different ways, especially in regards to social and sexual behaviors. And juvenile animals are almost always more active than adult animals, so even though they’re smaller they may need larger spaces than adults of the same species.

When housing more than one animal together, the space needs to increased- but not as much as you might think. Social animals generally don’t spend their time at opposite ends of the enclosure, but rather close together so they can socialize. The caveat, of course, is that socially-housed animals need access to places where they can avoid or hide from their companions in case of fighting or bullying, and that in certain types of social animals, more socially dominant animals may monopolize certain valuable (to them) parts of the enclosure.

An example: aquatic turtles require exposed basking spaces. If there is not enough room for all of the turtles to bask at once, there will be competition over this valuable area, leaving some turtles without access to the appropriate amount of light. This is termed “cryptic overcrowding,” because it can occur in a tank which may, to all appearances, have more than adequate swimming space.

Cryptic overcrowding can be avoided by spreading out resources and preventing “bottleneck” areas where a single animal can blockade or corner others. But in general, the increase in space when adding more animals to an enclosure is not a linear equation. It will depend, again, on the behavior of the species.

Movable dividers like these can help reduce cryptic overcrowding in terms of agonistic behavior. Lower-ranking horses housed in group stalls spent more time lying down when they were out of sight of higher-ranking ones. (Source: thehorse.com)

Aquatic or semiaquatic animals pose a unique challenge when it comes to space. Firstly, movement in water takes less energy than movement on land, so swimming animals need somewhat more space to perform activities with than you would expect for land animals. Secondly, a stable water condition is harder to maintain when there is less water in a system. Dissolved chemicals such as ammonia can be toxic to aquatic animals that breathe through gills or damage their skin, and being in containers with less water means that anything that gets into it will become more concentrated. So the smaller the system, the more dangerous any change in water quality will be.

Betta ‘cubes’ and vases have popped up on the market recently as viable ways to keep these solitary fish. While they can theoretically be kept in such a small space with adequate filtration and heating, the reality is that ammonia waste will build up so rapidly in such a small volume of water that the fish will be in constant stress and indeed life-threatening danger. Ironically, small and micro-aquariums are best left only to the most experienced aquarists.

Some aquariums and other places with large numbers of captive fish will mitigate this issue by keeping the fish in individual tanks connected to a larger flow-through system. In this case, even though the fish may be contained to one area, the amount of water it is living in is actually as large as the entire complex of tanks. In some cases, actual seawater may be cycled through the system via ocean pipes.

Aquatic research or cultivation facilities generally use flow-through water cycling.

Speaking of complexes, there is a way to artificially enlarge an animal’s space: separation and barriers. An open field is not particularly difficult to navigate if one wants to go from one end to the other, but by adding a simple kind of maze, differing topography, or even just visual barriers, the time and energy it takes an animal to traverse the same distance will increase.

One excellent example of this is “Paddock Paradise,” a method of altering horse pastures so that the horses will be motivated to move constantly throughout the day. Ironically, it does this by reducing the total pasture space available by fencing off the center of the pasture so that it becomes a looping track.

Diagram of how to turn existing pasture into ‘paddock paradise.’ More elaborate designs include areas with wading pools, rocky terrain, etc.

This means that the horses will consume the available grass more quickly and be driven to move more often to seek patches to forage in. It also encourages herds to be kept in tighter groups rather than spread out across the pasture, which more closely mimics how they behave in the wild. Early studies suggest that horses kept in Paddock-Paradise style enclosures move about twice as much as those kept in traditional pastures- even though they often have far less available space.

In general, whether or not an animal has adequate space in its enclosure can be assessed by observing where it spends most of its time. “Overutilized” spots, i.e. places where the animal spends a disproportionate amount of time should be replicated or expanded, while places the animal barely or never uses could be eliminated (with the exception that they may provide space for infrequent but still vital behaviors like elimination). I encourage those of you reading along at home to think about the spaces your pet might over- or underutilize within the enclosure you have given it.

So, to sum it all up: while amount of available space is one of the most oft-cited concerns about captive animal welfare, simply adding more space to an enclosure is unlikely to improve an animal’s quality of life unless that space is specifically tailored to the animal’s activities. To this end, there is no hard and fast equation to help one to determine the amount of space an animal will need. Just as a human can be sufficiently entertained in a small apartment with a treadmill and access to the internet, it may be possible to humanely keep an animal in a relatively small space so long as the space is used wisely.

That’s it for part two- next, let’s discuss the importance of climate for captive animals.

(If you missed it, here’s part one of this series on captive animal enclosures!)

References and Further Reading

Carlstead, K., & Shepherdson, D. (2000). Alleviating stress in zoo animals with environmental enrichment. The biology of animal stress: Basic principles and implications for animal welfare, 337-354.

Clark, J. D., Baldwin, R. L., Bayne, K. A., Brown, M. J., Gebhart, G. F., Gonder, J. C., … & VandeBer, J. L. (1996). Guide for the care and use of laboratory animals. Washington, DC: Institute of Laboratory Animal Resources, National Research Council, 125.

Cornetto, T., & Estevez, I. (2001). Influence of vertical panels on use of space by domestic fowl. Applied Animal Behaviour Science, 71(2), 141-153.

Hunter, S. C., Gusset, M., Miller, L. J., & Somers, M. J. (2014). Space use as an indicator of enclosure appropriateness in African wild dogs (Lycaon pictus). Journal of applied animal welfare science: JAAWS, 17(2), 98.

Imfeld-Mueller, S., & Hillmann, E. (2012). Anticipation of a food ball increases short-term activity levels in growing pigs. Applied Animal Behaviour Science, 137(1), 23-29.

Jackson, J. (2006). Paddock Paradise: A Guide to Natural Horse Boarding. Star Ridge Publishing.

Leone, E. H., & Estevez, I. (2008). Use of space in the domestic fowl: separating the effects of enclosure size, group size and density. Animal Behaviour, 76(5), 1673-1682.

Mason, G. J. (2010). Species differences in responses to captivity: stress, welfare and the comparative method. Trends in Ecology & Evolution, 25(12), 713-721.

Morgan, K. N., & Tromborg, C. T. (2007). Sources of stress in captivity. Applied Animal Behaviour Science, 102(3), 262-302.

Reinhardt, V. I. K. T. O. R. (1992). Space utilization by captive rhesus macaques. Animal Technology, 43(1), 11-17.

Roberts, M., & Cunningham, B. (1986). Space and substrate use in captive western tarsiers, Tarsius bancanus. International journal of primatology, 7(2), 113-130.

Ross, S. R., Schapiro, S. J., Hau, J., & Lukas, K. E. (2009). Space use as an indicator of enclosure appropriateness: A novel measure of captive animal welfare. Applied Animal Behaviour Science, 121(1), 42-50.

Ross, S. R., & Lukas, K. E. (2006). Use of space in a non-naturalistic environment by chimpanzees (Pan troglodytes) and lowland gorillas (Gorilla gorilla gorilla). Applied Animal Behaviour Science, 96(1), 143-152.

Warwick, C., Arena, P., Lindley, S., Jessop, M., & Steedman, C. (2013). Assessing reptile welfare using behavioural criteria. In Practice, 35(3), 123-131.

Watters, J. V. (2014). Searching for behavioral indicators of welfare in zoos: Uncovering anticipatory behavior. Zoo biology, 33(4), 251-256.

Young, R. J. (2013). Environmental enrichment for captive animals. John Wiley & Sons.

The Background and History of Captive Animal Enclosure Design

Sharks view some captive humans. This is an example of an inadequate enclosure design. (Photo source. CC BY-SA 2.0.)

So, let’s say you’ve got this animal, and you’ve got to take care of it.

In the vast majority of cases, ‘taking care’ of the animal includes enclosing it in some way, whether it be in a tiny box or a giant fenced park. In general, in order to care for an animal’s needs, you need to have access to that animal, and to be able to control what it can encounter. For example: oxygen, food, and water are three things you probably want any animal under your care to encounter. Predators and pathogens are two things you might want to keep out.

But of course, these are the most basic needs an animal has, and what I’m describing is the bare minimum of animal care. In other words, animals can live with their basic needs provided but not thrive. The distinction between the two is a rather recent discovery as far as animal care goes, and even as far as human care goes, as we shall see.

In any case, enclosure design is one of the most important animal welfare concerns of the day, and current captive animals are kept much differently than they used to be- hopefully, to their benefit and ours. In this first post on the topic, I’d like to go over, briefly, the history and the science behind what we know about keeping captive animals comfortable and engaged.

This is not meant to be a guide to keeping any species in captivity, just to clarify. But it will, hopefully, help you consider the needs of any animals under your care in new ways.

Is There Value to Captivity?

Speaking of caring for animals, I keep four axolotls as pets. If you don’t know what an axolotl is, it’s essentially a large weird salamander.

Pictured: weird salamanders doing weird salamander things. (Photo source: me.)

A bit of background knowledge on axolotls: their habitat in the wild is restricted to a single set of canals in Mexico, and their population is in rapid decline. By now, they may even be entirely extinct in the wild. Yet they have a huge captive population. It isn’t as though axolotls are difficult to breed, feed, or exquisitely sensitive to certain water parameters- rather, they are resilient and hardy critters who will eat most anything that fits in their mouths and make salamander love willy-nilly. The problem is that in the wild, they have nowhere left to go.

As I mentioned, the axolotl’s habitat is a single set of canals in Mexico. If this seems bizarrely restricted, that’s because it is: the canals used to be a vast lake, Lake Xochimilco, which was part of a system of five lakes: the other four have vanished. The cause is, as expected, human activity. Pre-Hispanic cultures farmed crops by piling mud and decaying vegetable matter in the shallow lakes to form floating patches called chinampas. Over time, as the population grew, massive numbers of people were living on the lakes themselves- Mexico City is, in fact, built on these former lakes. Much of the water was drained away in modern times to prevent flooding. So the axolotl is left with a few canals that run through one of the most densely populated urban centers of the world.

Pictured: what the axolotl has left. (Photo source. CC BY-SA 2.0.)

I bring up the axolotl’s wild habitat because it presents an interesting challenge to what the word “wild” really means. Is an axolotl in a manmade canal in the center of the city still really wild? If so, are the polluted, refuse-choked waters really the best place for axolotls to be- if there are even any left?

Even if the axolotl is extinct in the wild, it is in no danger of actually going extinct. There is a huge captive population of axolotls, split between laboratory animals, pets like mine, and a few in zoos as well. As I said, they are not difficult to keep or propagate. And I would be remiss if I did not acknowledge the efforts of groups such as the Durell Institute and the Mexican government to conserve and protect the wild axolotl.

But for the most part, there is no longer really such a thing as a wild axolotl- the species is maintained by artificial human life support. If we stopped, there would be none left. And the axolotl isn’t the only animal with this issue. It is oft-repeated that there are roughly 7,000 tigers in captivity versus 2,000 in the wild- though few realize that about 4,000 of the captive tigers reside on Chinese breeding farms, where they are raised for use in traditional medicine.

Factory farming of tigers in row after row of enclosures at the Guilin Xiongsen Bear & Tiger Farm, South West China. (Image by IFAW/Sinopix.)

Like the axolotl, the tiger has no trouble breeding in captivity: the problem is that it has fewer and fewer wild places to go. It is also important to realize that the vast majority of tiger and axolotl populations are effectively null for use in rewilding efforts. Why? Bad breeding. The pet trade’s fascination for rare color morphs and disregard for things like subspecies and natural behavior has led to highly inbred captive individuals that lack the survival skills to propagate without human assistance. Albino axolotls and white tigers would not and will never survive in the wild, yet people love to see them and hence, here they are.

This white tiger, while ‘appealing’ to look at, is not capable of surviving without human help. (Photo source. CC BY-SA 2.0)

Accredited zoos are perhaps the only groups heavily invested in maintaining rewild-able genes in their captive populations, and even then, they are still confronted with the issue of not having enough habitat to put their animals back into. Further complicating this is the sheer difficulty of introducing a captive population back into the wild, especially in a habitat where the species has largely been absent for some time. Successful reintroduction attempts, such as the black-footed ferret (which was bred from 18 remaining captive individuals) are still relatively rare.

What, then, is the value of a permanently captive species?

This is actually a very interesting question, because we are forgetting certain groups of animals which are very valuable to us. There was once a large, bison-like animal called an aurochs, which roamed from North Africa through South Asia and most of Europe in the thousands. Now the aurochs is extinct… in the wild. But it lives on in the form of domesticated cattle, in populations far larger than their wild cousins ever had. Most would agree that in terms of sheer monetary value, cows are fairly important to us.

Indeed, this is the story of nearly all of our domesticated animals, from dogs to horses. If a wild population even remains, it is small and dwindling, but captive populations are incredibly robust. We humans have a habit of multiplying what we like about an animal and tossing the rest.

So there is certainly value in captive animals for humans- but not necessarily for their wild relatives. In many cases, having huge captive populations of an animal can actually hurt conservation efforts more than help. If we consider at the aurochs, the wild cattle were largely edged out of existence by domestics whose herders shot grazing competitors. In many other cases, making an animal popular as a pet or in the public consciousness only fuels the black market trade for members of the species, whole or in pieces. Have you seen the cute video of a slow loris being ‘tickled’? So have several million others, and a good chunk of them want to buy one.

As cute as it seems, this slow loris is actually exhibiting a defensive posture.

At this point, you may be thinking that captivity is the doom of all wild species. But that isn’t quite the case. If you look at the comments on any “pet” slow loris video now you will see a stream of comments angrily denouncing the owner for animal cruelty. The popularity of that original video was what prompted a large-scale effort by scientists and animal lovers to educate the public about the ethical mire of issues behind keeping these primates as pets. With education comes larger-scale funding towards combating the black market trade, which is a large cause of the wild species’ decline.

The slow loris species probably gained net harm from the release of that video, but for other species, it may have helped by making people naturally more suspicious of ‘cute’ exotic pet videos. If widespread exposure of an animal leads to proper education about that animal, there is a conservation benefit to captivity.

Indeed, education itself is one of the largest values- in terms of conservation- of keeping captive animals. And enclosure design has much to do with this. The more people see animals in naturalized rather than humanized environments, the more likely they are to express interest in the animal’s conservation. Likewise, though successful wild reintroductions are rare, they are slowly becoming more feasible as conservation science advances, making captive populations function as better genetic repositories. Indeed, with non-habitat-size-related threats such as disease or parasites- chytrid fungus in amphibians is a good example- healthy captive populations may be a very good thing for wild species.

Chytrid fungus may eventually be responsible for the extinction of many amphibian species. If we can preserve some members of these species in captivity until we find a cure, shouldn’t we? (Photo source. CC BY-SA 2.5.)

Of course, all of this has sidestepped the very large question of the welfare of the individual animals in captivity because we have been focusing on things at the species level. It may not help (or harm) the species as a whole for some animals to be kept in captivity: certainly for many domesticated animals, captivity is their whole existence, plain and simple. But from the perspective of the individual animal rather than the species, the questions become very different. Rather than just general survival, we begin to consider an animal’s psychological well-being. More and more, modern zoos and pet owners are changing the question from “Is it healthy?” to “Is it thriving and experiencing pleasure?”

We’ll discuss the difference between these two states in a little while, but first, let’s delve into a little more background.

Good Intentions, Bad Care: A History

I’m going to bring up my axolotls again, and I swear it’s not just because I like talking about them.

I acquired my first two weird salamanders while taking a college course on developmental biology. The axolotl is a much-prized laboratory organism for its ability to regenerate nearly any part of its body via the conversion of adult cells back into a form of stem cells. For a vertebrate, this ability is a Big Deal.

In any case, during the course we were given the opportunity to see the axolotl’s regeneration skills for ourselves, and afterwards I took pity on my two test subjects and adopted them. (Initially, I thought they were both female, which is why I now have four instead of two.)

The lab, it should be noted, kept their salamanders in highly scientific tupperware containers, with just about enough room to turn around for each axolotl. They were not kept in plain water, but rather a specialized mixture of salts added to water called “Holtfreter’s solution.” This solution was changed every other day. The largest axolotls might also have bubblers added to their containers, but otherwise, that was about the extent of their habitat.

Hi-tech lab conditions. (Photo source: me. This axolotl is now five years old and lives in a 55-gallon tank. You’re welcome, Wooper.)

Naturally, to me, this seemed a bit heinous: at the time I didn’t know very much about salamander behavior, but I did figure that the animals would want at least enough room to move around in. My TA informed me that all I would need to keep them was a plastic bin and a bubbler, but I wanted something different: a lovely, interestingly decorated tank, where my axolotls would frolic and rejoice for their improved lives.

Poor, naive me.

If you have owned aquatic animals for more than, say, a year or two, you will realize that it is bizarre that they are marketed as “beginner’s pets.” Nearly every aquatic creature you can purchase as a pet might be qualified with the advice that it “dies easily,” but it isn’t that the animal dies easily- it’s that we humans barely understand the intricacies of water quality for those who breathe it. Imagine being trapped in a sealed room, surrounded by water, and your life depends on a school of confused fish. You have to hope they remember to change your air frequently enough for you to not suffocate on your own exhaled carbon dioxide, that they remember to remove your waste, which is piled in the corners and stinking up the room, and that when they do give you fresh air it’s composed of the precise gaseous mixture that humans evolved to breathe.

When we keep non-aquatic animals we usually don’t have to worry about that thing they breath, but fish are another matter. Captive fish were not commonly kept in tanks (well, for long, at least) until the 1850s or so, because a bewildering number of factors have to be managed in order to keep a tank healthy. The issue is the disconnect from a larger ecosystem. Just like we would rapidly experience dramatic changes in air quality staying in a sealed room, so do fish in water separated from larger bodies, with all the associated bacteria, soil, plants, and others in play.

In this sense, it would be nearly impossible for a laboratory to keep axolotls in large numbers in cycled aquaria, because the micromanagement is so intensive. The spartan environments my axolotls were once kept in were not necessarily derived from sheer cruelty or greed. Holtfreter’s solution maintains a water quality that is stable and helps the axolotl resist disease or fungi, so long as it is regularly changed. Compared to cycled freshwater aquaria, it may be actually less stressful for an axolotl to be kept in a regularly-changed, uncycled, one-gallon container of Holtfreter’s solution. (This is not only due to finnicky water quality but the fact that any sort of current in a tank can stress an axolotl out.)

I am not saying that axolotls do not benefit from increased space to move around in, variable habitat to explore, or the presence of others of their own kind (so long as everybody is an adult). However, the nicest, most enriched aquarium in the world could still be considered a welfare concern if the water quality was not up to par. To be quite blunt: the welfare of many captive axolotls in extremely nice-looking tanks is worse than the ones in the one-gallon lab containers simply because their first and most essential need is not being addressed properly. You, in that sealed room, would not care how nice it all looked and how much stuff there was to play with if you were choking on your own emissions.

Things you should know if you want to keep a fish (alive): the nitrogen cycle.

I discuss the difficulty of housing axolotls and other aquatic animals properly because it speaks to a larger issue of humans poorly understanding animal needs. You cannot assume that any animal will thrive in an environment that appeals to our sensibilities only. Furthermore, many animals that aren’t as familiar to us- I’m talking animals that aren’t mammals here- display signs of stress in ways we can’t see or read. A fish that “died easily” was likely shouting its problems in a language its caretaker was unable to understand.

Some of the earliest steps in improving the lives of captive animals revolved around limiting and simplifying their enclosures in order to better serve their basic needs. It’s true that a lion enclosure looks nice with a little grass, but grass hides urine and feces, which need to be cleaned up fast to decrease the risk of disease (plus, it stinks). So concrete is better, because it can just be hosed off quickly each night. Complex environments also offer more opportunities for an animal to hurt itself, by getting stuck, or breaking something and getting cut on a sharp edge, or simply by leaping and running around. Better keep it as simple and manageable as possible. In fact, having any other animals around is a risk too- a risk of getting hurt in a fight. So keep them all alone.

To our modern sensibilities, this “hard architecture” sounds like an atrocious way to design an enclosure, but for the early zoos, it was the best way to keep animals alive. Without a background in what the psychological value of enrichment, exercise, or social interaction was, in the 1930s and later zoos focused on merely keeping their animals as clean and injury-free as possible.

(Footage of the Berlin Zoo in the 1930s.)

The focus on “sterile” enclosures was actually something of a change from even earlier animal collections, which were city park zoos. The latter did focus on displaying animals in naturalistic conditions, as they were usually replacing the more traditional city parks where people went to walk around and feel the virtues of nature. These parks often attempted cage-free enclosure designs with moats and inclines rather than bars. But they also had very high animal turnover due to poor sanitary conditions. Most animal collectors in this era relied on a steady stream of animals coming in to replace the ones, to coin a phrase, that “died easily.”

So naturalistic gave way to sterile in the later 1900s. (Actually, before city park zoos, even EARLIER zoos were rich person’s menageries which were also pretty non-naturalistic, so the pattern has really gone back and forth over time.) Zoo animals were not the only ones that the new, cleaner mindset affected: as human populations became more dense and industrialized, farms were increasingly expected to maintain larger groups of animals on less land. The pasture, barn, and then the feedlot emerged during this time period. Disease and injury became a major threat in these conditions, so animals were kept in more and more isolate and easy-to-clean conditions. Things like farrowing crates for pregnant sows were a natural result of this mindset: they stop the sow from being able to get up and potentially crush her piglets.

Sows in gestation crates, where they will stay for the four-month duration of their pregnancies. (Photo by HSUS. CC BY-SA 3.0.)

Since then, zoos have changed more rapidly than farms towards a more psychological welfare-focused design, largely because zoos rely on public visitation and farms rely on production. But even for zoos, the changes came slowly at first. From the 30s onwards, ‘modern’ science dictated that bodily health was the only health that mattered, and that concepts like ‘play’ and ‘affection’ were mere artifacts of the romantic minds of uneducated people. It wasn’t just animals that were kept sterile- in the increasingly dense population centers of mankind, humans were being treated in a similar manner, particularly those in hospitals or orphanages.

The fear of disease was understandable: it was everywhere. City orphanages limited social contact with their charges for fear of infecting them or spreading already-present sickness. The prevailing theory of what ‘love’ was at the time was that it emerged in infants when they were fed by their mothers (thanks, Freud), so all the caretakers needed to do was make sure the orphans were kept fed… right?

However, a new disorder began to emerge in isolated infant patients and orphans. Termed anaclitic depression or ‘hospitalism,’ it could lead to a weakened immune system, mental retardation, and even death. No germ or disease was the cause.

The research of Austrian-American psychoanalyst René Spitz was among the first to address this syndrome, and what he found was probably unsurprising to those of us in the world of today: limited contact with infants by caretakers was what was causing them to literally waste away. In contrary to most recommendations to mothers at the time, Spitz argued that physical contact and affection between mother and infant was not only healthy, it was necessary for proper development.

American orphanage circa 1890.

Harry Harlow’s experiments with monkeys took this idea even further. To determine whether “love” emerged from feeding or physical contact, he removed infant macaques from their mothers and provided them with two surrogates: a wire one with a bottle stuck inside it, and a cloth one without any food. The monkeys ate from the first, but spent the rest of their time cuddling with the second. Harlow coined the concept of “dependency” for infants from this experiment: infants look to their mothers for more than simply nourishment. This seems obvious to us now… but it was a massive revolution then.

Of course, these revelations later flipped into the rather problematic concept that a child’s biological mother should be the one and only person to raise them, but that is a different article altogether. The reason I bring up this change in childcare because the public shift against sterile childhood environments was what also bled over into criticism of sterile animal environments. Harlow’s experiments in particular proved that being reared in deprivation has serious effects on both humans and animals.

Around the 60s, there was a bit of a zoo revolution. Presenting barren, sterile enclosures to the public was no longer acceptable. More and more research on animal mental disorders stemming from lack of enrichment led to a shift in animal husbandry practices not only in zoos but in laboratories and eventually farms as well.

Living Versus Thriving

So zoos began to shift their focus from strictly physical needs to a more enlightened view of both physical and mental health. Initially, the focus was on reducing or eliminating disordered behaviors in their charges. The most well-known of these, of course, are stereotypies: that is, repetition of simple locomotor behaviors such as spinning, pacing, jumping, or swaying. Others include compulsive behaviors such as fur or feather-picking, nose rubbing, and self-injury.

Beyond eliminating these openly unpleasant behaviors, zoos were motivated to keep their animals from seeming ‘bored,’ or, for the guests’ benefit, boring.

This was easier said than done, because the zoos weren’t exactly starting from scratch. Even the best of enclosures cannot make up for long periods of deprivation, as research by Harlow and others showed. An animal raised alone in a small concrete enclosure would balk at the sight of an open, grassy one, and display fearful or downright antisocial behaviors to others of its own species (and get knocked about roughly in return). Further complicating it all was that no single set of enrichment or habitat modifications could hope to hover the vast range of species kept in zoos.

Enrichment, by the way, refers to a number of things. It can be as simple as providing more than one type of food to eat, or as complex as providing multi-member social groups. Essentially, anything in an animal’s environment that engages the animal’s interest can be considered enrichment.

Enrichment studies with laboratory animals presented some solutions to these troubles. Animal labs in general are invested in maintaining large populations of animals at some sort of “baseline” physio-psychological state in a small space for a low cost, so naturally the greatest push for reform would come from them. Consumers not be able to (directly) taste the stress in a farm chicken, but in a lab rat extra stress can affect test results to a great extent.

Of course, that is not to say that scientists doing animal research always understood this fact, and the keeping of laboratory animals, like that of keeping animals in zoos, farms, and even as pets, has changed a great deal over time. Indeed, it has changed so much that a great deal of research done in the past is barely appropriate to compare to modern research, considering the differences in the way the animal subjects were housed. However, many of these changes are invisible to the public due to the secrecy with which much lab animal research is carried out in today.

The secrecy surrounding lab animals has the unfortunate side effect of concealing how much better their care has gotten over time. For example, this photo shows the enriched environment provided to many lab mice today. (Photo source.)

While Harlow’s monkey studies are probably the most famous animal enrichment studies, and certainly a landmark in the shift towards providing more socially enriched environments for captive animals, there were others that came even earlier. In 1947, Dondald Hebb compared rats raised in cages without social contact to those raised as pets, and found that the pet rats were better at solving problems than the caged rats. This led him to develop a theory of brain plasticity- that is, a theory that an animal’s cognitive abilities can be shaped by experience as well as genetics. This was a big boat-rocker in the 1940s scientific community. It suggested that brains, much like muscles, could be strengthened by frequent use.

Further studies showed the tremendous differences between the brains of animals growing up in enriched vs barren environments: namely, they had more synapses and dendritic connections- a physical manifestation of the power of enrichment. René Spitz also observed this phenomenon in a more outward form in his studies of orphans: those that grew up in orphanages were more likely to show cognitive impairments than those who grew up with their families.

But from the standpoint of animal welfare, does having more neurons and connections in the brain really improve an animal’s life? The answer seems to be yes, for the most part. Having more complex neural networks can serve as protection against mental disorders of old age such as dementia and Alzheimer’s. It can also stave off the presentation of harmful behaviors such as self-injury and anorexia (yes, animals can have anorexia too, though it isn’t related to their self-esteem).

In a more general sense, though, enrichment helps an animal physically as well as psychologically. Animals with more complex environments have reduced levels of stress and stronger immune systems then those without. The brain and the body, after all, are not exactly two entirely separate systems. So, as much as a lack of food or water makes an animal deprived, so does a lack of enrichment. Boredom can literally kill- slowly, but surely.

So as animal caretakers, our aim should be to give our charges the best lives we can provide. This means that we have to think about more than just their physical needs. In modern society, the animals who provide us with food, clothing, and medical advances should be housed in a way that enriches their lives. And as wild spaces become smaller and smaller and active wildlife management begins to blur the lines between wildlife and captivity, it is imperative we learn how to help animals thrive- because in an increasing number of cases, we will have to provide the environments they live in.

This wraps up my article on the background of keeping animals in captivity. In the ensuing parts of this series, we’ll discuss how to take all this background and history and use it to create captive environments that allow animals not just to live, but to thrive.

Click here to continue reading part two of this series, Stress and Space!

Read on: If you’d like to learn more about how mental disorders manifest in animals, I wrote a post about it here. I also wrote a post discussing my criteria for when keeping an exotic pet is ethical here. And to learn more about the blurring of wild and human spaces, I wrote about the white-tailed deer population problem in the US here. To view a list of all my nonfiction work, click here!

References and Further Reading

Ainsworth, M. D., Andry, R. G., Harlow, R. G., Lebovici, S., Mead, M., Prugh, D. G., & Wootton, B. (1962). Deprivation of maternal care: A reassessment of its effects. In Public Health Papers (WHO) (No. 14). World Health Organization.

Armstrong, D. P., & Seddon, P. J. (2008). Directions in reintroduction biology. Trends in Ecology & Evolution, 23(1), 20-25.

Bowkett, A. E. (2009). Recent Captive‐Breeding Proposals and the Return of the Ark Concept to Global Species Conservation. Conservation Biology, 23(3), 773-776.

De Courcy, C. (1990). Evolution of a zoo: a history of the Melbourne Zoological Gardens, 1857-1900.

Duhon, S. (2015). Short Guide to Axolotl Husbandry. Ambystoma.org <http://www.ambystoma.org/education/guide-to-axolotl-husbandry>

Gewin, V. (2008). Riders of a modern-day Ark. PLoS biology, 6(1), e24-e24.

Griffiths, R.A., Graue, V. and Bride, I.G. 2003. The axolotls of Lake Xochimilco: the evolution of a conservation programme. Axolotl News 30: 12-18.

Harlow, H. F. (1958). The nature of love. American psychologist, 13(12), 673.

Hayes, M. P., Jennings, M. R., & Mellen, J. D. (1998). Environmental enrichment for amphibians and reptiles. In Second nature: Environmental enrichment for captive animals (pp. 205-235).

Hoage, R. J., & Deiss, W. A. (Eds.). (1996). New worlds, new animals: from menagerie to zoological park in the nineteenth century. JHU Press.

Hutchins, M., & Smith, B. (2003). Characteristics of a world‐class zoo or aquarium in the 21st century. International Zoo Yearbook, 38(1), 130-141.

Jones, C. 2002. Water quality model for the reintroduction of the axolotl (Ambystoma mexicanum) into the canals of Xochimilco, Mexico City. Undergraduate Honours theses, Trent University Peterborough, Canada.

Maas, P.H.J. (2014). Aurochs – Bos primigenius. In: TSEW (2015). The Sixth Extinction Website. <http://www.petermaas.nl/extinct>. Downloaded on 28 August 2015.

Miller, B., Biggins, D., Hanebury, L., & Vargas, A. (1994). Reintroduction of the black-footed ferret (Mustela nigripes). In Creative conservation (pp. 455-464). Springer Netherlands.

Nekaris, K. A. I., Campbell, N., Coggins, T. G., Rode, E. J., & Nijman, V. (2013). Tickled to death: analysing public perceptions of ‘cute’ videos of threatened species (slow lorises–Nycticebus spp.) on web 2.0 Sites. PloS one, 8(7), e69215.

Nekaris, K. A. I., Shepherd, C. R., Starr, C. R., & Nijman, V. (2010). Exploring cultural drivers for wildlife trade via an ethnoprimatological approach: a case study of slender and slow lorises (Loris and Nycticebus) in South and Southeast Asia. American Journal of Primatology, 72(10), 877-886.

Nowell, K., & Xu, L. (2007). Taming the tiger trade: China’s markets for wild and captive tiger products since the 1993 domestic trade ban. TRAFFIC East Asia.

Rumbaugh, D. M. (1997). The psychology of Harry F. Harlow: A bridge from radical to rational behaviorism. Philosophical Psychology, 10(2), 197-210.

Spitz, R. A. (1945). Hospitalism; an inquiry into the genesis of psychiatric conditions in early childhood. The psychoanalytic study of the child, 1, 53.

Stamps, J. A., & Swaisgood, R. R. (2007). Someplace like home: experience, habitat selection and conservation biology. Applied Animal Behaviour Science, 102(3), 392-409.

Teton, J. (1988). “Archives de l’Aquariophilie: L’aquariophilie a-t-elle évoluée considérablement depuis des décennies ?”, Revue Aquarama.

(This article is part of a series on spider behavior- if you haven’t read my Introduction to Spiders yet, find it here!)

Yup, it’s happening. We are going to learn all about the twisted, terrifying, and occasionally quite kinky world of spider sex.

You would think that I could not fill up a whole article on the topic of spider sex- after all, sex is sex, right? Tab A into slot B, and bam, done: that’s sex. Not for spiders, though. Not only have they added a whole extra step to the basic mechanics to the act, but even getting a chance to mate can be an extreme challenge. I’m sure right about now you’re all considering the use of “widow” in the name black widow, but sexual cannibalism is actually only a small part of the spider sex story.

Yeah. The spider sex story.

THE SPIDER SEX STORY

It all begins when the male spider ejaculates.

Does that seem a little late for a starting point? Actually, for spiders, the act of ejaculation long precedes the actual act of fertilization. No female is even close to the male when this occurs, and he probably won’t meet one for a long while.

You see, male spiders have no penises with which to transfer sperm to females. In place of any abdominal genitalia, they have a simple hole called the gonophore on the underside of their abdomen. When the spider ejaculates, sperm simply falls out of this hole. This would make mating rather difficult, because as I mentioned before, the male spider ejaculates before a female is even present- actually, he ejaculates pretty much as soon as he is physically capable of doing so. (I’m sure some of my readers can relate.)

To prevent the sperm from just falling on the ground, the male spider spins a little web underneath his abdomen, kind of like a spider-diaper, to catch the sperm when it falls. He then contorts himself so that he can suck up the sperm into needle-like appendages within his pedipalps. This is often referred to as “charging” the palps.

Is this making you uncomfortable? I’ll try to go into a bit more detail.

I discussed spider pedipalps in the previous article: they’re two appendages on either side of the spider’s mouth that look like small legs. On males, the tips are usually enlarged… for reasons.

A handsome striped lynx spider showing off his enlarged pedipalps.

If you flip the spider over, it quickly becomes apparent that those fuzzy things aren’t just used for dusting. Underneath the palp lies a coiled organ called a palpal bulb, containing a sperm duct and ending in a needle-like point called an embolus. This organ works like a turkey baster. It can suck sperm up… and when needed, it will spit it out again.

A close-up of the pedipalp of a goblin spider. This is an example of a simple male pedipalp; others can get ridiculously complex, with tubes and frills everywhere. (From Izquierdo & Rubio, 2011.)

So, when the male spider does finally meet a female and get with the doin’, it is these pedipalps he inserts into the female spider’s paired spermatheca (i.e., sperm storage organs). We’ll get to the female half of things in a moment, but first, let’s talk about those pedipalps. Because it’s weird, right? Why transfer sperm in such a complicated way when so many other creatures manage to make the process so easy?

The story- the theorized story, anyway- is perhaps more interesting than you might think. First, we have to remember that while intravaginal sex seems pretty normal to us, it evolved long, long after our lineage split with the arthropods, the group that includes insects and arachnids. In fact, the arthropods that do practice a form of sex that we’d consider more “traditional” (abdominal genital inside other abdominal genital) actually evolved the practice entirely separately from us.

What happened before internal fertilization, then? Well, we still see it today in many of our aquatic cousins, the fish: the male simply sprays his sperm over the female’s eggs. Easy-peasy. The earliest arthropods, which were also aquatic, did the same thing.

But when arthropods and vertebrates both started to leave the water, a change had to occur. Sperm evolved to swim through liquid to get to eggs, so if a male ejaculated on dry land, the sperm would obviously not make it. Similarly, eggs released without some kind of waterproof covering- like an eggshell- would just dry out. This is why amphibians must fertilize their eggs in the water.

Contrary to what you might think, there is nothing internal going on here. (Photo source.)

But for other animals, some major mechanical changes had to take place.

Most land vertebrates engineered the “butt bump” style of mating: they got one hole to connect to the other, somehow, so that the sperm wouldn’t dry out and could get to the egg before it took on its protective covering. And some arthropods stumbled upon this strategy as well. However, as far as arachnids (as well as many insects) go, there was an even better solution: sperm packaging, in the form of spermatophores.

I won’t delve too deeply into spermatophores, since we have a lot of other things to cover today. However, most spiders do not use spermatophores, which are literal packages of sperm that a male gives to a female. Instead, it’s assumed that this was probably an ancestral trait of theirs, since almost all other arachnids do use them. From spermatophores, presumably, rose the spider habit of gently maneuvering the sperm packages into the female with one’s pedipalps, until eventually male pedipalps evolved into a specialized organ for this exact purpose. To put it another way, spiders converged on an extremely roundabout route to sex that looks similar to ours… if male humans had their penises on their faces.

It looks a little like this:

Glorious, glorious spider sex. (Photo source.)

There are both drawbacks and advantages to transferring sperm in this way. The drawback is that it takes a male spider a lot of time and energy to get ready for copulation, more than it would for, say, a male mammal. However, in some species, the male spider makes up for this by ensuring his paternity. He may, after inserting his sperm, deposit a special plug to prevent the female from mating with anyone else. Or, in more extreme cases, the male spider may actually break off his pedipalps, in an act the literature unfacetiously calls “genital mutilation,” in order to keep them lodged eternally within the female.

Just super great stuff.

But we’ve been focusing on the males way too much. It’s not as if the females just passively sit around and wait to be fertilized, after all. The process of laying eggs is far too costly (sometimes it costs her life!) to just take in any old sperm. It had better be the best sperm available, or consequences may be dire.

As I mentioned before, female spiders have paired spermatheca organs for the male to insert his pedipalps into. These organs can just hang onto sperm until the female ovulates, in which case the sperm kind of gets shot through a loop so that it passes over and fertilizes the descending eggs before the spider lays them. In most female spiders, there are actually three reproductive tracts: two for the male to insert his pedipalps into, and one in the center where the eggs come out.

Sadly I could not find a good (fair use) photo of female spider genitalia. I know you all are extremely disappointed.

Here is Spiderman’s abdomen instead.

The advantages to storing sperm like this means that female spiders can actually pick and choose which sperm get to fertilize their eggs by only allowing males to inseminate one out of two spermatheca- thus enabling them to remember whose sperm went where. They can also choose to eject the sperm entirely if necessary. So if they hang on to the sperm of a questionable male and nobody better comes by, well, better to have crappy genes than none at all. Otherwise, if Mr. Spider Right comes by, that old sperm gets tossed out like used cat litter.

The length of the tubes connecting the spermatheca to the oviduct is variable between different species- some have barely any separation at all, while some are fantastically elongated and looped multiple times. The reason for these differences is possibly due to an evolutionary arms race between male and female genitalia: the emboli of male palps grow longer in order to bypass female mate choice by directly depositing the sperm in the oviduct, whereas the female spermatheca grow longer to prevent this. I am not kidding about the looped and longer parts- in some diagrams, female copulatory ducts look like a child’s scribbles with all their twists and turns.

Like this one, comparing the reproductive tracts of two different species. The two circles are the spermatheca, the squiggly bits are the ducts leading into them. (From Eberhard & Huber, 2010.)

You can see why some male spiders might try to take other, more drastic measures to give their genes a fighting chance.

What about these measures, then? Thus far, we’ve mostly talked about the mechanics of spider sex in general terms. Sperm meets egg, etc. But as with many animals, there is more to the story than that: not only do spiders have to make things mechanically complicated, they have to make things behaviorally complicated, too.

Let’s delve into the questionably kinky world of spider mating rituals.

SPIDER FLIRTATION PART ONE: THE PEACOCKS

The gif I posted up at the very top of this article is of a peacock spider (Maratus sp.), and it is part of a spider group rapidly becoming familiar to the internet consciousness. It’s not hard to see why: as a subset of jumping spiders, peacock spiders are mandatorily adorable, and the flashy displays of the males just push this genus over the edge.

Here is footage of one species of peacock spider (Maratus speciosus) performing his courtship dance.

See? Doesn’t that make up for all those horrifying descriptions of spider genitals from earlier? …No?

Ok, well, anyhow, as you may have guessed, the male spider uses his colorful “fan” in the same way that the spider’s namesake, the peacock, uses his. (The spider’s fan is actually an upraised abdomen with outstretched abdominal flaps, but we won’t quibble here.) It is used as a means to get the female’s attention and probably proves something about that particular male’s genetic quality.

As to what that might be… nobody really knows. The study of this particular group is relatively new to science, as new species are still being discovered, each with its own particular display patterns and dance moves.

To help explain how something so flashy could go unnoticed for so long, I am providing this helpful size comparison. (Photo by Jurgen Otto.)

By the way, the visual display is only a part of what the male spider is trying to impress with- the other part we just aren’t sensitive enough to feel. But female peacock spiders, bless their single-chambered hearts, are just sensitive enough. During courtship, the male peacock spider stridulates his abdomen, sending out specialized little vibrations for the female to pick up with her legs. He also drums with his forelegs, occasionally on the female’s head. Do you understand yet how sexy he is, lady?

Like the visual displays, these acoustic displays vary by species, and by situation. In fact, the spiders seem to mix and match visual and acoustic displays depending on the environment they meet the female in. If she’s far away and out of sight, acoustic displays will get her attention; if she’s close up, add the visual component to the mix.

Even without adding variations based on the environment, you might have noticed in the video above that the dance of the peacock spider can be quite long and complex. Not only does the male display and vibrate his abdomen, he also raises his third pair of legs (which are also modified with species-specific fringes and colors) and waves them in all different directions. Many species add in even more moves, like flapping their abdominal flaps and pedipalp waving (equivalent to a male human whirling his junk around). About the only thing all the dances of all the different species of peacock spider seem to have in common, in fact, is the very end of the dance: the male will stretch his first and third pairs of legs over the body of the female. If he’s lucky, she’ll allow him to mate with her after that.

Peacock spider dance moves shown in what may be my favorite scientific figure of all time.(From Wearing et al, 2014.)

It really does beg the question as to why these dances need to be so complex, and again, the answer is that nobody yet has a clue. Certainly there might be some evolutionary pressure to differentiate one species’ moves from another, but that can’t explain everything- many spiders already have evolved a good, non-flashy system for this in their pedipalps and spermatheca: the pedipalps of one species generally only fit into the spermatheca of the same kind, like a lock and key.

Perhaps some of the answer might lie in a crucial difference between the behavior of an animal like a peacock compared to its spider namesake: when a peahen doesn’t like how a peacock is dancing, she doesn’t usually turn around and eat him.

But female peacock spiders will, if they aren’t fond of the male’s display- or even if he’s not even displaying. Like most spider species, they aren’t above a little cannibalism now and then. It’s hard for evolution to maintain perfect hair-trigger attack behaviors if you’re supposed to slow down and try to have sex with potential prey once and a while. Perhaps this is what helped speed the evolution of the extraordinarily flashy and increasingly desperate displays of male peacock spiders: they can’t even get close to a female otherwise!

Interestingly, a number of other insects have taken advantage of this with other species of jumping spiders- there are a handful of flies and moths that mimic spider courtship and territorial behavior in an effort to trick their predators into not eating them. If there are peacock spider mimics like these out there, that would certainly prompt the evolution of harder-to-mimic displays on the part of the real males.

A moth (Brenthia hexaselena) mimics a jumping spider predator (Phiale formosa). From Rota and Wagner, 2006.

It is certainly a topic that deserves more study. However, we can’t just talk about peacock spider courtship when we discuss spider sex, as interesting as it is. This form of courtship- with flashy, exaggerated visual displays- is actually fairly rare among spiders. Jumping spiders and other spiders that hunt actively have very good eyesight, as I discussed in the previous article. However, most spiders that spin webs do not, and rely much more heavily on detecting vibrations and chemoreception. For males of these species, other tactics are necessary if they hope to have a chance at giving the female their sperm.

SPIDER FLIRTATION PART TWO: THE TEENY SNEAKY SEXERS

Female peacock spiders are noticeably larger than males, which emphasizes some of the danger males are put into during courtship, but in terms of spiders the size difference is trivial. If you want to see a real size difference, you should observe the male and female orb weaver spiders.

A mama spider and her baby? I hope not, because these two spiders are engaged in the act of mating. (Photo source.)

Golden orb weaver spiders show the most extreme version of sexual dimorphism, with the female spider being roughly 1000 times heavier than the tiny male. In fact, in many species of web-spinning spiders, males and females were at first assumed to be separate species; in others, the males have not yet even been discovered!

Size differences are most pronounced in spiders that have a sessile lifestyle, including those that hunt from webs and others like the well-camouflaged crab spiders. Why the difference, though? Initially it was assumed that it was due to the danger of being eaten by the female- could smaller males sneak a mating in undetected? But this seems not to be the case, as it is actually the larger males that have more mating success. Further compounding this theory is the fact that based on phylogenetic data, in most species with pronounced size dimorphism it is the females who have gotten bigger, not the males that have gotten smaller- selection was acting on her, not him. But why?

A giant female orb weaver hangs out with her posse of tiny males. (Photo source.)

The difference may not have to do much with sex, but rather with the lifestyles of these spiders. If the size difference evolved along with the web-spinning lifestyle, females- which are generally the ones that spin the webs- could afford to get bigger, while males- which lead a migratory lifestyle to seek out the sessile females- needed to stay small.

Paradoxically, though, there are some species in which the males did get smaller, notably the males of the tangle-web spiders (Tidarren sp.). Actually, these males get so much smaller that they have to tear off one of their pedipalps before they fully mature because it would be impossible for the spider to function with both. The remaining pedipalp also gets ripped off during copulation- almost immediately- but luckily can continue transferring sperm by itself into the female for roughly four hours.

You use what you got.

Even in spiders with female gigantism rather than male dwarfism, the males’ genitals have to get bigger, because obviously they have to be able to penetrate the female enough to deposit sperm. This has led to a few species of spiders with emboli (the organs at the tips of their palps) that inflate to three or four times the length of their own bodies. Impressive!

I don’t know what to caption this with.

These itty-bitty males have to achieve a monumental task: they have to get close enough to the female spider to mate with her without being eaten on the spot. This is difficult when the females in question are nearly blind: no peacock spider-style ornamentation will help here.

Most males declare their intentions up front via vibrations, love taps, and chemical signals. They pluck the strands of the female’s webs for dances that can go on for literal hours. They have to- if the dance isn’t long enough and the female isn’t impressed, well… you only get to put in one application.

Some spiders in the genus Pisaura move beyond mere strutting and actually offer their potential mates valuable gifts in the form of pre-killed prey items. When offered these gifts, the females grab and eat them, giving the males a chance to swoop in and do the deed.

To be fair, some species- like this giant wood spider- use the wait-until-she’s-eating strategy as their main tactic without providing the food themselves. (Photo source)

However, this gift-giving behavior isn’t always as generous as it first appears. While some males are honest, others use a sneaky ploy: gift-wrapping. By wrapping up their present in silk, they make sure the female takes longer to eagerly unwrap it- giving them more time to copulate while she’s distracted. Some males take this ploy to be outright jerks: they wrap up small inedible items, like seeds or dried insect shells, to give to the female. Needless to say, they have to copulate fast to use this strategy and be prepared to run when the female discovers the deception.

Not many Pisaura males go so far to trick the females this way, though- the risks usually run a little too high. (Though some are actually bold enough to try to snatch the meal back after they’re finished mating!) However, for other male spiders, no risk is too high to ensure their seed is sown. In fact, what would seem a drawback for other males can actually work in their favor.

Sexual cannibalism is usually considered an accident, or just a side effect of having to mate with something like a mantis or spider: if the male gets away, great; if he doesn’t, well… them’s the breaks. But some male spiders have evolved to use sexual cannibalism as an actual asset to their breeding. Not only do they not resist it, some males, like redback spiders, will actually flip their abdomens onto the female’s fangs during mating to encourage her to get eating.

It might seem a little counterproductive to the survival of the fittest to willingly off yourself, but remember, evolution doesn’t necessarily favor the long-lived: it favors the ones that pass on their genes. And surprisingly, letting the females eat them helps the males: as with the gifts from the Pisaura spiders, a distracted female mates for longer, even if what she’s distracted with is eating her partner.

Letting yourself get eaten, of course, means that you won’t be able to mate with any other females, so the males that tend to allow or encourage sexual cannibalism tend to come from those that have very high mortality rates prior to finding their mates. Once they leave their mothers’ webs, their only mission that single instance of sex- they don’t even eat. Most of these males also have fragile pedipalps that break after a single mating episode, so there isn’t much point in them trying to find other mates anyway!

Once the female spider has finished eating her first mate she’s less likely to accept another- she’s full now. So there’s yet another advantage for the redback spider male, who watches serenely from spider heaven: ensured paternity.

(By the way, the more-likely-to-mate-when-she’s-full behavior occurs in most female spiders, not just redbacks. At times, a free lunch may be more valuable than a clutch of eggs, no matter how well he dances.)

Here is a video of a male redback spider performing the death flip:

It may seem like things are pretty rough for male spiders in general (though I’m sure if you were to ask them, they wouldn’t care a whit). However, we need to spare a few thoughts for the difficulty on the ladies’ end. Yes, they may eat the males who don’t please him, but it’s not just out of hunger or genetic snobbery. Having small males hanging out in your web can alert prey items to its presence and make it harder for you to catch dinner. Furthermore, they can even attract predators- and furthermore, they sometimes even steal the female’s food!

And sometimes the male spider is the one who makes sex scary for the female.

For some species, it’s as simple as the male tying up the female with silk to ensure she doesn’t snack on him during mating. Ironically, in the literature, this technique is called a ‘bridal veil.’ Some so-called bridal veils contain a chemical compound that makes the female woozy and docile during mating, while other species concentrate on just tying her up completely.

Maybe a little light spider bondage isn’t too bad; certainly some scientists think that the females might find the chemicals and the experience sexually stimulating. But for some species, the females have it much rougher, and not really in a sexy way. The males of diving bell spiders, i.e., the only fully aquatic spiders, are actually larger than the females. And unlike practically every other spider species, it’s the male diving bell spiders that might cannibalize the females. Researchers only noticed this when they saw females running away from large males- even though larger males are actually the ones they prefer to mate with!

(This preference is possible to observe because even though the males are larger than the females, she still has to twist her abdomen up to allow him to inseminate her. Nonconsensual sex is nearly impossible if you’re a spider.)

The size switch was likely prompted initially by the environment: female spiders, who spin underwater webs to fit inside, can do this more easily while small, while males, who again rove in search of mates, can do this more easily underwater while big. Spider cannibalism is less driven by the sex of the individual than it is by the size. Big eats small.

But while females preferred big male mates, things get dangerous when they get too big. So while males remain larger than females due to the environment and the females’ own preferences, they can’t evolve much bigger- else they’ll never be able to catch a mate.

Male and female diving bell spiders. (Photo source.)

Don’t feel too bad for all these nervous spiderfolk, though. We’ve learned all about the process of courtship, so now it’s time to delve back in to the deed itself. Because there is more to it to just sticking in a thing and shooting out sperm- and it’s all for the ladies.

IT’S ALL FOR HER: INSENSITIVE MALES MAKE THE BEST LOVERS

Interestingly, and uniquely amongst nearly every other animal, the male sperm transfer organs of spiders (the palpal bulbs) have no nerves and therefore no sensory capabilities. Even insects have innervated phalluses (when they have them at all) but not spiders. As humans we may find this rather disappointing, but there are some other, worse consequences to being numb, as one writer eloquently points out:

Because of the lack of nerves in the palpal bulb, the challenges faced by a male spider attempting to copulate can be likened to those of a person attempting to adjust a complex, delicate mechanism in the dark, using an elongate, elaborately formed fingernail. (From Eberhardt and Huber, 2010)

Apparently, this isn’t just conjecture: male spiders have a lot of what the scientific community refers to as “slips” and “flubs” while trying to inseminate females. This whole business gets even more ridiculous when you look at the mazes some of those spiders have to traverse with their emboli.

Let me bring this image back.

Female spiders also have a curious lack of sensory organs, at least on the external portions of their genitalia (i.e., the area immediately surrounding their epigyne, technically called a spider vulva). Researchers are less sure about how sensitive the interior of the copulatory ducts and the spermatheca is- think of the size of the last spider you saw and try to imagine how tiny all these organs must be. It’s amazing they’ve figured out as much as they have.

Still, the female has got to have some sensitivity somewhere- a lot of spider behavior hinges on it. Lots of males prepare their palps by coating them with saliva to soften them, and then scraping areas on the female’s underside, perhaps to further signal his intent, or to stimulate her. Most continue to actively stridulate and stroke during sex, with one palp inserted and the other tapping rhythmically. The passion of some of these spiders often literally shakes the web.

(Please start playing this song in the background while watching this next video.)

But oh, we’re not done. The rather humble sounding short-bodied cellar spiders are among some of the most intense lovers of all, and the females tell them about it. Most spiders make little audible noise at all- it’s all sent via vibrations. But the female cellar spider actually squeaks by rubbing ridges on her chelicerae (fangs) and palps together. Researchers describe it as a sound similar to leather creaking, whatever that means.

This squeak is a negative one- it’s used in two contexts: when the female is chasing the male away because she doesn’t want to mate, and when she’s not happy with how things are going during sex. You see, the male short-bodied cellar spider has specialized, muscular palps. During copulation, he presses these palps up against his chelicerae so that the female’s epigyne is pinched, and then rotates his palps rhythmically for up to 40 minutes.

Spiderman digs it.

Apparently all this canoodling and doodling is a very good thing: more pinching and twisting seems to lead to larger clutch sizes when the female lays eggs. However, if he squeezes too hard, the female lets him know with a series of angry little squeaks until he desists. This, too, leads to higher fecundity; it pays to listen to her.

Bring back the sensual music as you read these excerpts from a scientific paper describing the sex between cellar spiders:

 Very early in copulation each inward twist lasted for only about 2 s… Later the inward twists became longer and lasted for many seconds before the next outward twist… Still later the single outward twists were replaced by short bursts of twisting… Abdomen vibration was much more rapid during copulation… The strongest vibrations caused the male’s entire body to vibrate… (From Huber & Eberhard, 1997)

Whew, it’s getting a little warm in here, might want to open a window or something. These spiders might very well be too sexy for science.

Spider porn aside, most authors seem to agree that all these movements seem to be for one thing and one thing only: to stimulate the female. There aren’t many definitive answers as to how or why, but there’s a good chance that the female has stretch receptors inside her copulatory ducts and spermatheca so that she can feel when things are being pressed a certain way. The scientists claim that this is some measure of how the females can discern male fitness, but I’m fairly sure that the male spiders just like to treat a lady to a good time. You know, to thank her for not eating them.

…Though she might eat them afterwards anyway.

As long as the sex happened, he’s ok with it.

Previously: An Introduction to Spiders. Next: Social spiders!

To read about other weird animal sex things like masturbation and bird yaoi, here is the full list of all my articles.

References

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Andrade, M. C. (2003). Risky mate search and male self-sacrifice in redback spiders. Behavioral Ecology, 14(4), 531-538.

Breene, R. G., & Sweet, M. H. (1985). Evidence of insemination of multiple females by the male black widow spider, Latrodectus mactans (Araneae, Theridiidae). Journal of Arachnology, 331-335.

Eberhard, W. G., & Huber, B. A. (2010). Spider genitalia. The evolution of primary sexual characters in animals. Oxford University Press, New York, 249-284.

Forster, L. M. (1992). The Stereotyped Behavior of Sexual Cannibalism in Latrodectus-Hasselti Thorell (Araneae, Theridiidae), the Australian Redback Spider. Australian Journal of Zoology, 40(1), 1-11.

Girard, M. B., Kasumovic, M. M., & Elias, D. O. (2011). Multi-modal courtship in the peacock spider, Maratus volans (OP-Cambridge, 1874). PloS one, 6(9), e25390.

Hebets, E. A., Stafstrom, J. A., Rodriguez, R. L., & Wilgers, D. J. (2011). Enigmatic ornamentation eases male reliance on courtship performance for mating success. Animal Behaviour, 81(5), 963-972.

Herberstein, M. E., Wignall, A. E., Hebets, E. A., & Schneider, J. M. (2014). Dangerous mating systems: Signal complexity, signal content and neural capacity in spiders. Neuroscience & Biobehavioral Reviews, 46, 509-518.

Herberstein, M., Schneider, J., & Elgar, M. (2002). Costs of courtship and mating in a sexually cannibalistic orb-web spider: female mating strategies and their consequences for males. Behavioral Ecology and Sociobiology, 51(5), 440-446.

Hormiga, G., Scharff, N., & Coddington, J. A. (2000). The phylogenetic basis of sexual size dimorphism in orb-weaving spiders (Araneae, Orbiculariae). Systematic Biology, 49(3), 435-462.

Huber, B. A., & Eberhard, W. G. (1997). Courtship, copulation, and genital mechanics in Physocyclus globosus (Araneae, Pholcidae). Canadian Journal of Zoology, 75(6), 905-918.

Izquierdo, M. A., & Rubio, G. D. (2011). Male genital mutilation in the high-mountain goblin spider, Unicorn catleyi. Journal of Insect Science, 11(1), 118.

Knoflach, B., & Van Harten, A. (2001). Tidarren argo sp. nov.(Araneae: Theridiidae) and its exceptional copulatory behaviour: emasculation, male palpal organ as a mating plug and sexual cannibalism. Journal of Zoology, 254(04), 449-459.

Li, D., Oh, J., Kralj-Fišer, S., & Kuntner, M. (2012). Remote copulation: male adaptation to female cannibalism. Biology letters, 8(4), 512-515.

Peretti, A., Eberhard, W. G., & Briceño, R. D. (2006). Copulatory dialogue: female spiders sing during copulation to influence male genitalic movements. Animal Behaviour, 72(2), 413-421.

Rota, J., & Wagner, D. L. (2006). Predator mimicry: metalmark moths mimic their jumping spider predators. PloS one, 1(1), e45.

Rutledge, J. M., Miller, A., & Uetz, G. W. (2010). Exposure to multiple sensory cues as a juvenile affects adult female mate preferences in wolf spiders. Animal Behaviour, 80(3), 419-426.

Schütz, D., & Taborsky, M. (2005). Mate choice and sexual conflict in the size dimorphic water spider Argyroneta aquatica (Araneae, Argyronetidae). Journal of Arachnology, 33(3), 767-775.

Uhl, G., & Vollrath, F. (2000). Extreme body size variability in the golden silk spider (Nephila edulis) does not extend to genitalia. Journal of Zoology, 251(1), 7-14.

Vahed, K. (2007). All that glisters is not gold: sensory bias, sexual conflict and nuptial feeding in insects and spiders. Ethology, 113(2), 105-127.

Vollrath, F., & Parker, G. A. (1992). Sexual dimorphism and distorted sex ratios in spiders. Nature, 360(6400), 156-159.

Wearing, O. H., Delneri, D., & Gilman, R. T. (2014). Limb Displays of Male Saitis barbipes (Simon, 1868)(Araneae: Salticidae). Arachnology, 16(6), 219-224.

Whitman, D. W., Orsak, L., & Greene, E. (1988). Spider mimicry in fruit flies (Diptera: Tephritidae): further experiments on the deterrence of jumping spiders (Araneae: Salticidae) by Zonosemata vittigera (Coquillett). Annals of the Entomological Society of America, 81(3), 532-536.

Zolnerowich, G. (1992). A unique Amycle nymph (Homoptera: Fulgoridae) that mimics jumping spiders (Araneae: Salticidae). Journal of the New York Entomological Society, 498-502.