The occasional behavior by female mantises of eating their male suitors has attracted a great deal of interest, and has been used as an example of how ruthless and alien nature (and even the female gender) can be. However Dr Beetle thinks that on the contrary, it provides a good lesson on how humans influence their results and yet still believe they are witnessing 'natural behavior'.
Animals will often make little sense when observed under artificial conditions, because animals adapt to wild conditions where a much wider range of environmental cues occur. These cues may be too subtle to replicate in the laboratory. Under artificial and confined conditions, animals can do a variety of odd things because they lack the cues that normally switch their behavior. For example, a fox that kills all the hens in a coop is often used as proof of the ruthlessness of a 'killer instinct'. (more beetle). But really it only shows that instincts can go wrong under artificial and confined conditions. In nature, most birds and hens would escape, with the effect of altering the fox's behavior before carnage can begin.
But the glee of humans in being able to discredit nature does not stop at their claims of cannibalism in so many species. Further bizarre claims made by humans are that the female mantis intentionally bites off the male's head to increase reproductive prowess, because in its death throws, the decapitated male continues to attempt mating 'with no inhibition', or to increase sperm output. But this behavior is about as natural in mating as a chook running around a yard after its head is lopped, or the involuntary shuddering or excretion that takes hold of some animals upon death.
Refreshingly, a study by Liske and Davis in 1987 threw the first human light on the importance of the natural environment to behavior in mantises. The Chinese mantis Tenodera aridifolia sinensis was among those wrongly accused of sexual cannibalism during mating in several previous studies. However Liske and Davis, although still stuck in the laboratory, made some concessions to the mantis. They fed the mantises regularly, turned the bright observer lights down, and left the room to replace a fidgeting human observer with a stationary video camera. Surprise surprise, no cannibalism occurred! In fact, a whole courtship behavior by the male and female mantises, new to science, was observed!
I think the study by Liske and Davis suggests that mantises will naturally follow their instinct to pounce on any small moving object, especially when hungry. They need a 'one tracked mind' with fast reflexes to obtain prey - they don't have a web to help them and they cannot fly swiftly after their prey. Under natural conditions, it would seem sensible for them to evolve a courtship behavior that then allows their own kind to turn off the 'pounce and eat' instinct from a safe distance. Such an instinct would be difficult to turn off when hungry or starved under artificial laboratory conditions, but under natural conditions the courtship would allow non-violent mating to occur. A further part of the courtship behavior might be that if the female does not participate in the courtship display, the male would know not to approach. If however the male is 'desperate' or confined in the laboratory, it may have no choice but to try and approach the female, if it really wants to mate. It could not fly off to try another female. It would have to approach the unresponsive female, but this time cautiously, because it senses the risk of being mistaken as food. Using these simple and sensible principles, it may be possible to explain all human observations on mantis mating behavior.
An attempt to regain the 'evil manta' was made by Lawrence in his 1992 paper. He studied Mantis religiosa, the bastion species most renowned for its cannibalism. Lawrence studied religiosa under the same favorable laboratory conditions as the Chinese mantis, but did not observe courtship behavior. Instead, he observed cannibalism and a cautious (= scared?) approach by the male. Surely therefore, cannibalism by religiosa is not an artifact. However, Dr Beetle thinks that even here, a courtship behavior may still be found in religiosa by more sensitive study. Perhaps religiosa is even fussier than the Chinese mantis about its surroundings, before it will act naturally. Just because the observed religiosa males approach their females cautiously, does not mean this is its natural or evolved approach to mating. Perhaps the male is cautious because it knows that no natural courtship behavior is possible under the human imposed conditions. Then the only alternative it may have when mating is to be cautious.
One behavior noted by Lawrence was 'juddering', a dance by males apparently made as a warning to other males. This is the first time such behavior was observed, even though this species has been studied by biologists for over a century. It makes you wonder what other hidden behaviours will be discovered in mantises upon more careful observation. I would suggest that unless a courtship is noted in mantises, then the biologist is probably not studying the mantis under suitably natural conditions. Natural behavior may be far more cryptic to the human observer than previously realised, and until they are found, no claims on knowing the natural behavior of the mantis can be made.
Lawrence observed that in the laboratory, the process of mating took 4 to 5 hours, while under more natural conditions outside it took two hours. Surely this fact alone would suggest to a human that something is going wrong in their laboratory. Unnatural complications in the laboratory are making the mating behavior prolonged and strained.
A rapid drop in male compared to female population was suggested as further proof that males were being cannibalised. However, such alteration to the sex ratio is common in insects. Males often disperse more than females. Dispersal brings with it a greater range of hazards. The flying male may be blown into inhospitable terrain. It moves more often so will be noticed more often by predators. The energy expended in dispersal will also sap the male's strength and leave it more vulnerable to a wider range of fates. For example, many leafhoppers (which suck sap, and have no hint of being cannibals - so far) also have dispersing males. Their sex ratio drops rapidly in favor of females through their adult season, simply because of dispersal. The fact that female mantises produce pheromones to attract males suggests that males come to females rather than females to males - a sure sign that greater dispersal occurs naturally in males.
The other suggestion is that cannibalism increases near the end of a season as the prey quality decreases. The evidence of 'starvation' in the wild was that females fed ad libitum in the laboratory were fatter than their wild counterparts. However, this is not evidence that wild mantises are in a naturally deprived state of hunger. It may just be that if food is offered to you on a plate, you will eat more than perhaps you should and put on more weight. Most animals I can think of will overeat if fed constantly. In the wild they would eat only to the extent that strikes up a balance between hunger and the effort required for getting food. The natural state of most wild animals is that they are fit and healthy.
The paper then described mantises in the 'wild' in Portugal, where the vegetation was predominantly grassland of two species of thistle, and a few types of shrub. Under these conditions, some cannibalism was still observed. However, this landscape sounds to me not wild, as a wild place should have much more variety of plant species. Greater plant variety, to which the mantis evolved, would bring with it a greater variety of prey species. The prey would therefore be available over a longer period of time due to their variety in life cycles. The more cyclic condition of food abundance and shortage for the mantis in Portugal may not be the condition to which religiosa originally evolved. What do I mean? Well, a similar example is that Christmas beetles in Australia often kill gum trees through overgrazing. Even though this occurs in the 'wild', it is not a natural result that the beetles evolved to do. The problem arises because the Christmas beetle now lives in a highly modified landscape where its natural cues and balances have gone. The beetle larvae feed underground on grass roots, a food source now highly abundant due to land cleared by humans for pasture. Beetle larvae enjoy an unprecedented survival rate. However, from larvae emerge numerous adult beetles whose diet is gum leaves. The few scattered trees remaining in 'the wild' therefore succumb to overgrazing, whereas once the trees would have survived in numbers.
Some of the evidence for cannibalism in the wild was that females reared and fed in the laboratory were taken from their cage and placed on a bush. They were allowed to settle for ten minutes, and then males added to the bush. However, this experiment cannot be counted as proof that cannibalism is natural in the wild. It should not be surprising that a mantis kept under artificial conditions will continue to display its restricted behaviors, even if placed temporarily in the 'wild'.
In other observations of 'wild matings' Lawrence simply noted the behavior of wild specimens whenever they were encountered. On 31% of occasions the male was cannibalised. However, the start of these courtships involving cannibalism was never actually observed! It seems to me an assumption that mating was being observed, whereas perhaps the females had simply ambushed unsuspecting males for food. Females produce a pheromone to attract males; however, after mating they no longer produce the pheromone. Therefore one of the cues males use to become aware of females in their vicinity is lost if the female had mated previously. The males being cannibalized may have simply and unknowingly strayed near a previously mated female (no pheromone produced for them to know) that ambushed them in the same way that it tackles any other small moving object. To test this theory, the females could have been captured and tested for pheromone production.
The confusion surrounding mantises can probably be transferred to other creatures such as spiders as well. Cannibalism during mating may well occur naturally for some species. However, it is probably much rarer than biologists currently suggest, and occurs more often when cues go wrong rather than as an adaptive imperative or evolutionary advantage.
There is some additional information that suggests that cannibalism of the male arthropod is not the norm. In some spiders, the male is far smaller than the female, which has been cited as an adaptation for overcoming the risk of being eaten. Spiders have the choice of evolving an elaborate courtship that will turn off the female's instinct to pounce, or more rarely, of forgetting about courtship and adapting the male to become so small that it can creep in and mate without even being noticed by the larger female! For example, the female mangrove golden orb weaving spider (Nephila plumipes) has a body about 20 mm long, while small males are about 5 mm long and rarely noticed. This strategy requires a happy medium. Too small and the other males at the edge of the web can tell you to butt out. But if you get too big and bossy, the female might notice you as dinner instead. (Posted August 2001)
