Deceit in Nature

As a species, we can be quite hard on ourselves. Nature is often separated from Homo sapiens and put on a pedestal of purity and goodness while we lament our species’ wickedness. I’m not going to touch that philosophical debate with double-layered lab gloves on, but I’m here to tell you that, as humans, we’re hardly the pioneers of deceit and cruel treachery. I’ll save war, murder, and rape for another post (with triple-layered gloves), but today I want to show you some of the fascinating ways nature has us beat with how underhand and brilliantly sneaky it can be.

The fundamentals of life come down to survival and reproduction. If you survive long enough to reproduce, you pass your genes on. If you don’t, you’re an evolutionary dead end…literally. Consequently, any adaptations that increase the ability of organisms to survive (avoid predators, catch prey, save energy, etc) and reproduce (avoid angry rival males, kill angry rival males, woo females, efficiently invest energy into making and raising babies, not accidentally kill your babies, etc) are selected for and propagated. There are no morals or rules of conduct in nature, so this leads to a wide array of ridiculous behaviors that would certainly be frowned upon in human society.

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Defensive: The Quest To Avoid Being Dinner

Self-defense is the most socially-acceptable deceitful behavior. It’s hard to criticize anything done to avoid ending up on someone’s dinner plate, although we (hopefully) don’t encounter too many cannibals or human predators. In nature, however, the risk of being eaten is probably one of the most significant pressures animals face. Richard Dawkins and John Krebs proposed the Life-Dinner Principle, which describes the relationship between predator and prey: if a predator fails to catch prey, it misses dinner; if prey fails to avoid a predator, it dies. Consequently, we would expect prey animals have a far wider range of defensive adaptations than predators have corresponding techniques to capture prey. I won’t be covering all the possible types of defensive deceit here (there are quite literally books on the subject), but sharing a few of my favorite examples to give you a taste of the vast variety.

Stevens M 2014Camouflage is one of the most widespread defensive strategies. These disguises can be visual and remarkably versatile; in a single species of shore crabs, each crab can have a unique pattern and coloring based on its environment[10]. Cephalopods (octopus, squids, etc) are also masters of camouflage. While this gives them an advantage as a hunter, it is also a remarkable defensive technique. Cephalopods have special cells called chromatophores, which contain collections of pigments. Muscles attached to these cells are controlled by nerves and allow the creatures to instantly change the expansion, contraction, color, darkness, contrast, and distribution of markings on their bodies. Sharks are hardly going to chow down on what they think is a piece of coral when they’re looking for a tender and juicy octopus!

Auditory camouflage is less well known than visual, likely as there are far fewer well-studied examples. This phenomenon has been recognized in moths and has evolved as a defense against one of their primary hunters: bats. Bats use echolocation to hunt, and moths have evolved remarkable behaviors as a response. Some moths produce ultrasonic signals to warn bats of toxicity or startle them and allow the moth to escape. Others would turn the air force green with envy with their ability to use sonar jamming; the moth species Bertholdia trigona have organs on their thoraxes called tymbals, which are controlled by muscles to produce an ultrasonic burst of sound that disrupts the brown bat Eptesicus fuscus from being able to process the echos and locate the moths[2].

defenseUpping the deceit-scale, some harmless animals have evolved to pretend to be a different, harmful species. This sheep-in-wolf’s clothing technique is known as Batesian mimicry and can only exist if the cost to predators from eating the harmful species outweighs the benefit from eating the mimicking species. That is to say, if prey is scarce and a little snake is mimicking another snake that has an annoying, but not deadly, bite… well, the predator is going to be eating them both. But, if food is bountiful or the venomous snake is deadly, the predator is more likely to avoid both the actual dangerous snake and any mimic that passes for it. Luckily for Batesian mimics, predators that have a negative experience with a model harmful species tend to avoid anything that looks similar for a long time, and do not often re-sample the population. The Amazonian bird known as the Cinereous mourner (Laniocera hypopyrra, if you want it to sound more optimistic but less pronounceable) hatches chicks that look like someone applied an electric shock to a neon orange guinea pig. As it turns out, they’re mimicking toxic caterpillars of the family Megalopyge, even down to bobbing their heads to mimic the caterpillar’s movements[8].

Another remarkable example is the collection of ant-mimicking jumping spiders. It turns out that these arachnids are on the menu of many creatures, including other jumping spiders! By mimicking the appearance of ants, they not only gain access to ant nests so they can have a feast, but they gain protection because ants are infamously disgusting prey. On top of the fact that ants bite and sting, they also produce chemicals such as formic acid that make them taste terrible and are often found in groups which means you have to battle a littleant mimic2 army of them. There are at least 2000 known species of ant mimics for these reasons, and jumping spiders make up a good number of those. One genus of jumping spiders, the Myrmarachne, is entirely composed of ant mimics. Some Myrmarachne species even mimic the group behavior of ants and travel in clusters of 50 to hundreds of members[6].

Aggressive: The Quest to Catch Dinner

On the opposite side, we have the hungry. We all need to eat, one way or another, and sometimes that means using deception to entice victims. All living creatures have to balance their energy budget while determining if the risks, time, and energy required to attain a meal is worth it. Some predators disguise themselves as either harmless or desirable to lure in the unsuspecting. This is a little like the phenomenon of clowns in the horror genre, where clowns were trusted to be harmless and funny and then all of a sudden they start walloping people with giant hammers and appearing in bedrooms at ungodly hours. We have wised up to the fact clowns are actually the epitome of evil, which nicely demonstrates the importance of predatory efficiency: if the disguise results in high rates of successful kills, future prey will not learn to avoid it. Simultaneously, predators need a disguise to be enticing enough to outweigh the prey’s sense of caution.

sharkThe cookiecutter shark, Isistius brasiliensis, feeds by latching onto creatures and using its round mouth and serrated teeth to chomp out circular clumps of flesh (like how a cookie cutter shapes cookie dough, only less pleasant). Their bites aren’t generally fatal, but to avoid the risk of approaching large prey directly and to attract things to chomp on, cookiecutter jawsthey’ve evolved to utilize bioluminescence on their underside. The green bioluminescent signals are often used by ocean species as “counter-illumination” to mimic light shining into the water and camouflage themselves completely, but the cookiecutter shark actually uses it to create a smaller silhouette; an illusion of a harmless, and tasty, prey fish [12]. When a larger fish or mammal investigates the potential meal, the shark does a rapid dine-and-dash.

Spiders are also masters of deceit, with the golden orb weaver Nephila clavipes spinning golden webs and displaying unique body patterns. While studies have shown that bees actually learn to avoid white or other colored webs, they do not learn to associate the yellow webs with danger. This is likely because yellow is strongly associated with nectar-bearing flowers and therefore potentially too valuable to the bees for them to avoid. If that was not enough to lure in unsuspecting bees, the patterns on the spiders actually attract prey, perhaps mimicking those found on flowers[11]. The silver argiope Argiope argentata spider also uses their webs to lure in prey, but these weave patterns into the web that mimic those appearing on many flowers in UV light as nectar guides. The orchid mantis also mimics flowers to attract pollinators; this little killer looks like a beautiful pink and white flower, drawing in unsuspecting bees and other insects. Interestingly, studies suggest that this insect does not actually mimic a specific flower, but exploits the general preference of pollinators for certain colored objects. This type of deceit is known as sensory exploitation, rather than mimicry.

Perhaps the only thing more effective than mimicking food is to mimic a sexually receptive female. We may make jokes about men being single minded about their needs, but the drive to go forth and multiply is so strong that many predators have evolved to take advantage of it in spectacularly terrible ways. Sometimes the deceit is based on straightforward mimicry; female fireflies of the Photuris genus mimic the light signals flashed by receptive females of the genus Photinus, attracting males from several different genera and then unceremoniously eat them[7]. Similarly, the spotted predatory katydid mimics species-specific clicks of sexually receptive cicadas females, luring males close enough to capture and devour.

bolas spiderIn other cases, the deceit is more specific and complex. The bolas spider, Mastophora, is found throughout the Americas. They’re chubby little arachnids who spend the daylight hours hiding by camouflaging themselves as bird poop. At night, they relinquish their disguise and become hunting tightrope walkers. Balancing on a thread of web, they make a sticky ball attached to a strand and proceed to fling it at moths, reeling in their delicious catches. This rather unique hunting strategy is aided by complex chemical mimicry; the spiders produce chemical compounds in the exact ratio of the key compounds in female moth’s sexual pheromones[4,9]. Thus, male moths come fluttering by to check out what they think is a sexy lady, only to be assaulted by a ball of goop and eaten. The drawback to this strategy is the cost of specificity: the spider’s pheromone mimic is specific to only one or two species of moth, which means that if anything happened to those populations the spiders would be in trouble.

For our final example, we’ll return to jumping spiders. The Australian (go figure) Portia fimbriata species of jumping spider is cannibalistic, with its main prey being jumping spiders of the genus Euryattus. Not only does P. fimbriata have amazing spider-hunting skills (they walk onto webs of small spiders and create vibrations to mimic caught prey, but with larger spiders they create ambiguous vibrations that cause the resident spider to move to the center of the web and approach slowly, allowing the jumping spider to stalk it safely. For all prey sizes, they finish with a burst of vibrations mimicking a disturbance like wind or a leaf hitting the web to hide their movements as they attack), but they also trick females by pretending to be suitors. Euryattus females create nests inside rolled up leaves and males will approach and perform a little mating dance on the leaf. P. fimbriata has learned to mimic the vibrations of this dance, tricking the females into coming out and being eaten. Interestingly, this behavior is only seen in the spiders whose territory overlaps with Euryattus, and yet if you breed those spiders in a laboratory setting with no exposure to Euryattus, they will still exhibit the hunting behavior, suggesting this is actually an innate, genetically encoded behavior[5]!

Parasitic: The Quest to Have Someone Else Do Your Work

cuckooWe can all relate to trying to avoid work. Laziness might have a negative connotation and even be classified as one of the seven deadly sins, but it can be an efficient strategy to conserve energy and time (“Work smart, not hard” – I remember wanting to throw a textbook at people who said that in college). What would be frowned upon in human society (bullying someone else to do your homework, tricking couples into raising your children, enslaving people to work for you…you know, the normal types of laziness) are widespread strategies in nature. Why invest precious resources into something when you can get someone else to do it with just a little trickery?

I’ve previously covered some fascinating, mind-altering parasites, but parasitism extends far beyond those. Many times, like those in my previous post, parasites are looking to manipulate something’s behavior in order to reproduce or spread. The nematode Myrmeconema neotropicum infects ants and actually causes the ant to change color, turning its host into a mimic of the ripe fruit of Hyeronima alchorneoides. It also makes the ant raise its gaster, increasing its chance to be noticed and eaten by birds that proceed to spread the parasite. Sometimes, pheromone mimicry plays a role as well; larvae of Meloe beetles emit a mimic pheromone of its host species of bee. When the male bee arrives, it attempts to mate with the undulating mass of larvae, which attach themselves to his abdomen. The male bee then goes on to encounter a real female and the larvae switch hosts, ride the female to the hive, and then proceed to feast on the bee larvae and grow within the hive. Why try to hunt food when you can be delivered straight to it?

cuckoo eggsCuckoos are a fantastic example of brood parasitism and kleptoparasitism. While 60% of cuckoo species raise their own young, some species have their offspring raised by completely different birds in order to shrug off the demands of parental investment. Females will lay a single egg in the nest of another species, and when the chick hatches it will eject all of the host’s own eggs or chicks, allowing it to monopolize the parental care. Naturally, this has resulted in an evolutionary Cuckoo chicksarms race in which the host species has evolved defenses such as the ability to recognize and reject parasitic eggs, subsequently causing selection of cuckoos whose eggs mimic the color and pattern of host eggs. Those cuckoos that target a specific species evolved to lay eggs that mimic the size, pattern, and color of host eggs. Not only that, but as cuckoos tend to be larger than the host species, the chicks evolved techniques to manipulate the host parents into bringing them more food than normal. Horsfield’s hawk-cuckoo chicks have vivid yellow underwings. When the host parents come to the nest, the chick flashes its wings, mimicking the open beaks of multiple hungry chicks and causing the parents to deliver extra food. Cuckoos also have more intense begging displays – sound analysis has shown that the chicks vocalize at similar rates and intensity to an entire brood of chicks instead of just one[3]. An important factor in the ability of cuckoos to successfully parasitize is passing on the genes encoding species-specific egg patterns and behaviors. Consequently, some cuckoos have accents to their songs based on what species raised them. When they look for a mate as an adult they match accents, ensuring that they maintain the specific traits that allowed them to successfully hoodwink their host parents!

The alcon blue butterfly, Maculinea alcon, also manipulates species to care for their young. The female butterflies lay their eggs on plants, and when the baby caterpillars hatch they drop to the ground and are discovered by Myrmica ants. The caterpillars produce chemicals that mimic those used by the ants to recognize workers and brood, resulting in the ants actually carrying the caterpillars back to their nest. Once there, the caterpillars refine their chemical mimicry and the unwitting ants proceed to feed them, and, if food is scarce, will even kill their own brood and feed them to the growing caterpillars. The method is so efficient that they have a 90% success rate at ending up in a nest, at which point they are fed and protected by the ants for 1-2 years until they are ready to pupate[1]!

Sometimes ants are instigators rather than victims; the European slave-maker ant, Harpagoxenus sublaevis, has earned its name by creating slave empires to do all of their colony labor. A queen ant will invade the nest of a different colony and murder the current queen and all the adult workers. This leaves the colony’s developing brood, which hatches and imprints on the new queen and performs the colony tasks for her. Meanwhile, the queen’s own brood hatch and, rather than be bogged down by menial tasks, they go on raids and replenish the slave force by capturing other broods.

Reproductive: The Quest to Get Laid

Sure, deception allows you to dodge being eaten, guarantees a meal, or even allows you to shrug off your adult duties – but the real question is: can it get you laid? If we take a look at nature, the answer is a resounding yes – although I’d like to interject with a disclaimer that I do not recommend using these strategies for finding a human partner.

orchidOn the slightly less scandalous end of the spectrum, plants often use mimicry to trick insects into pollinating them. Nectar is pricey to make, so it saves energy and resources if plants can just trick insects into getting coated in pollen instead of bribing them with nectar. Some plants use Bakerian mimicry; female flowers will mimic male flowers of the same species in order to cheat pollinators out of any reward. Others use Dobsonian mimicry and imitate a nectar-producing species of flower but do not produce any actual nectar reward, leaving expectant pollinators empty handed and, one assumes, quite miffed. Perhaps even more impressive is Pouyannian mimicry, where flowers will mimic other organisms, such as female insects, in order to cause pseudocopulation: hoodwinked males will attempt to mate with the flower and, consequently, end up coated in pollen and go on to fertilize other flowers while thinking it’s actually getting laid. Poor guys. Orchids are one of the most famous examples of this: over 10,000 species have intricate flowers matching the size, color, posture, and even pheromones of female insects.The Australian hammer orchid targets male Thynnid wasps. Female wasps typically wait on top of a plant for males to find, so the orchids have evolved flowers to not only mimic the wasps’ body shape while waiting, but also her pheromones. While the disguise is impressive, if males are given the option of a real female wasp or a flower they manage to recognize the deceit. Consequently, these orchid flowers have evolved to bloom in periods when female wasps are not yet posing for males. A key component to the successful mimicry is not only the visual mastery, but the chemicals emitted to complete the deception. Sometimes it’s generic sexual pheromones, species specific, or it doesn’t have to do with sex at all: Epipactis veratrifolia is a flower pollinated by several species of hoverfly. Rather than hoodwink them with sex pheromones, the plants have taken advantage of the fact that hoverfly larvae eat aphids, and the females make sure to lay their eggs on plants with signs of aphid population. Most of these cues are chemicals both from the affected plants and the aphids. E. veratrifolia plants mimic not only the appearance of aphids, but also the chemicals aphids secrete as alarm signals when under attack. These signals are general, allowing the flowers to fool multiple species of hoverflies into landing to lay their eggs and picking up pollen in the process.

Animals take a slightly more active role when using sexual mimicry. The parasitic wasp, Cotesia rubecula, participates in a common practice called mate-guarding wherein the male mates with a female, and then guards her to prevent any other males mating with her. For these wasps, females attract males with pheromones and then males induce mating behavior through vibrations, causing the female to assume a receptive position to initiate sex. After having sex, the female only continues to be receptive for a brief time. During this time, if a second male appears the first will attempt to distract him by mimicking the female’s sexually receptive pose. If the second male is distracted for long enough by the fake-female, the real female will become unreceptive to any further advances, ensuring that the first male’s genes are passed on (I’m a little skeptical that this would fly in our own species).

Mimicking females is a pretty solid strategy for some underdog males to achieve sex. In many species of fish, there are multiple types of males: a larger male that typically mate-guards and a sneaker male that physically resembles the female gender. This allows the sneaker male to bypass the large male’s security, approach a harem of females or nest of eggs undetected, and then ninja fertilize the eggs or have a quickie with some of the ladies. Cuttlefish are also guilty of this; fierce competition during mating season leads to up to 11 males fighting over a single female. The winner guards the female fiercely, but some males who aren’t up to fighting temporarily disguise themselves by turning mottled, hiding some of their arms, and altering their overall body shape in order to appear female and sneak under the guard’s nose!

Overall, humans are a bit more restrained in our use of deceit, if only due to social pressures and our attempted adherence to moral and ethical codes. We can see some of it in hunting, war, and the bizarre (and mildly concerning) lengths people are willing to go to get laid. As we’ve reduced evolutionary pressure on ourselves in first world countries (food is generally easy to come by, we don’t have to strive to avoid being eaten, and dating apps exist), our deceits focus more on personal social, economical, and sexual gain…not to mention the brilliant strategies concocted by students to avoid doing as much work as possible, such as writing a blog post instead of analyzing data.

References

[1] Akino, T., Knapp, J.J., Thomas, J.A., and Elmes, G.W. (1999) ‘Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies’. Proceedings of the Royal Society B: Biological Sciences 266: 1419–26.

[2] Corcoran, A.J., Barber, J.R., and Conner, W.E. (2009) ‘Tiger moth jams bat sonar’. Science 325: 325–7; and Corcoran, A.J., Barber, J.R., Hristov, N.I., and Conner, W.E. (2011) ‘How do tiger moths jam bat sonar?’ Journal of Experimental Biology 214: 2416–25.

[3] Davies, N.B., Kilner, R.M., and Noble, D.G. (1998) ‘Nestling cuckoos, Cuculus canorus, exploit hosts with begging calls that mimic a brood’. Proceedings of the Royal Society of London B: Biological Sciences 265: 673–8.

[4] Gemeno C, Yeargan KV, and Haynes KF. 2000. Aggressive chemical mimicry by the bolas spider Mastophora hutchinsoni: identification and quantification of a major prey’s sex pheromone components in the spider’s volatile emissions. Journal of Chemical Ecology. 26: 1235–43.

[5] Jackson RR and Wilcox RS. 1990. Aggressive Mimicry, Prey-Specific Predatory Behavior and Predator-Recognition in the Predator-Prey Interactions of Portia fimbriata and Euryattus sp., Jumping Spiders from Queensland. Behavioral Ecology and Sociobiology. 26(2): 111-119.

[6] Jackson RR, Nelson XJ, and Salm K. 2008. The Natural Distory of Myrmarachne melanotarsa, a Social Ant-Mimicking Jumping Spider. New Zealand Journal of Zoology. 35: 225–235.

[7] Lloyd JE. 1965. Aggressive Mimicry in Photuris: Firefly Femmes Fatales. Science. 149(3684): 653-654.

[8] Londoño, GA, García, DA, Martínez, MA. 2014. Morphological and Behavioral Evidence of Batesian Mimicry in Nestlings of a Lowland Amazonian Bird. The American Naturalist. 185: 135–141.

[9] Stowe M.K., Tumlinson J.H., and Heath R.R. (1987) ‘Chemical mimicry: bolas spiders emit components of moth prey species pheromones’. Science 236: 964–6.

[10] Stevens M, Lown A, and Wood L. (2014). Camouflage and Individual Variation in Shore Crabs (Carcinus maenas) from Different Habitats. PLoS ONE. 9. e115586. 10.1371/journal.pone.0115586.

[11] Tso, I.-M., Liao, C.-P., Huang, R.-P., and Yang, E.-C. (2006) ‘Function of being colorful in web spiders: attracting prey or camouflaging oneself?’ Behavioral Ecology 17: 606–13.

[12] Widder, E.A. (1998) ‘A predatory use of counterillumination by the squaloid shark, Isistius brasiliensis’. Environmental Biology of Fishes 53: 267–73.

As an overall reference:

Stevens, M. (2016). Cheats and deceits: How animals and plants exploit and mislead.

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