Mimicry is a recurring subject on this site, mainly because I’m fascinated by the precision with which natural selection can mold animals and plants to look like things they’re not. We’ve also seen examples of plants mimicking animals before, as in the orchids that mimic bees and wasps, fooling randy insect males into trying to copulate with the flowers (this deception promotes pollen transfer). But I think the following example is unique, for it involves plants whose seeds mimic animal feces. And the mimicry involves both the shape, size, and odor of the seeds.
What does the plant gain from this mimicry? It fools dung beetles, who apparently mistake the seeds for antelope dung. And dung beetles, as we all know, roll the dung balls away, bury them, and lay eggs in them, providing sustenance for their larvae. By fooling the beetles, the plant gets insects to not only disperse the seeds, but bury them, hiding them from seed predators and destructive fires, giving them a head start in germination.
This fascinating mimicry is described in a new article in Nature Plants (reference below, free access at link) written by a team of investigators from the Universities of Cape Town and of KwaZulu Natal in South Africa. Here’s the duplicitous plant, Ceratocaryum argenteum, a rush-like angiosperm native to Cape Province, South Africa (photo from Rosa Rubicondior).
The plant is unusual in having large rough seeds (nuts), which, as you can see in figures a-c below, are about 1.5 cm (0.6 inches) across. They’re not only large, but, to the investigators, smelled distinctly like animal feces.
While studying what animals might eat these seeds, the team discovered that while de-husked seeds were eaten by the area’s main mammalian seed-eater, the striped field mouse (Rhabdomys pumilio), those mice avoided whole, husked seeds and didn’t cache or bury them. But in the course of these observations, the authors realized something else: hard seeds like these often have no odor, and in fact hard seed coats may have evolved in part to protect predators from smelling the inner seed and eating it. Thus the pungent fecal odor of C. argenteum suggested that maybe the odor was adaptive for the plant.
Sure enough, they observed individuals of the dung beetle Epirinus flagellatus treating the seeds exactly as if they were spherical pieces of animal dung: the beetle rolled away the seeds and buried them. Here’s the beetle; it’s a small one, about 1 cm. long:
Here, from Science News, is a video of the hapless beetle rolling and burying a C. argenteum seed. This is the Sisyphus of the animal world, laboriously rolling a heavy object to no avail.
To see how many of these seeds got buried, the authors put out 195 of them in 31 locations. They found that 27% of the seeds were buried whole (presumably by dung beetles) within a day, under what they call “optimal moist conditions.” That’s a pretty good way to get your seeds moved to new habitat where they don’t have to compete with other seeds, and even planted underground. One can see how a plant tricking a beetle in this way could substantially increase the spread of the plant’s genes.
When they dug up the seeds, they found no beetles or eggs associated with them (beetles tend to go underground with their dung balls, laying eggs in them and nomming some of the dung). This suggests that the beetles discover their mistake only after rolling away the seeds and burying them. I guess they just give up and return aboveground, searching for real dung.
What are the seeds’ adaptations to facilitate beetle dispersal? First, their shape. As the authors note:
C. argenteum seeds look similar in size, shape and dark brownish colouration to the dung of local small antelope (Fig. 1g). [JAC: this is feces from the bontebok, Damaliscus pygargus]. Seeds are remarkably circular (ratio of widest to narrowest seed dimension = 1.02; Fig. 1a,b) whereas scatterhoarded nuts tend to be flattened (L. sessileratio = 1.86; Fig. 1h, i). This circularity would facilitate rolling. Seeds of most of the other Ceratocaryum and closely related Cannomois species are unscented, smaller, smooth, black and have elaiosomes for ant dispersal (Fig. 1j).
Here are the figures (a and b are above; note similarity of bontebok feces in shape and size to the plant seed).
Finally, the mimicry involves, as noted above, not just size and shape but odor as well. Using gas chromatography and mass spectrometry, the authors compared the amount and composition of volatile chemicals emitted by both old and fresh C. argenteum seeds with those of other seeds in the family, and also with the dung of elands, elephants, gemsboks, impalas, and bonteboks. (The main antelopes in the area are elands and bonteboks.)
C. argenteum seeds emitted a tremendously higher amount of volatiles than did other seeds in the family (a 300-fold difference). Further, as you can see from the figure below, the chemical composition of C. argenteum seeds resembled that of dung, while related but non-rolled seeds did not. As the authors note:
Compounds emitted from the seeds that are also emitted by eland and/or bontebok dung include various acids, the benzenoid compounds acetophenone, phenol, p-cresol and 4-ethyl-phenol, as well as the sulphur compound dimethyl sulphone (Supplementary Tables 2 and 3). Most of these compounds are well known as components of the scent of herbivore dung (see also Supplementary Table 3). Similarity in scent is not due to bontebok feeding on C. argenteum as this plant is unpalatable and bontebok feed instead on various grasses (Poaceae).
One final point: the habitat of C. argenteum is one swept regularly by fire, and, unlike many plants, this species can’t re-sprout after a fire. Thus, the ability to get its seeds buried away from the flames is highly adaptive!
This is a very nice paper that reveals a heretofore unknown kind of mimicry. And the mimicry involves not just shape and size, but odor.
The resemblance of C. argenteum seed odor to that of animal dung was obvious to the investigators, but of course what matters is the resemblance of the smells to beetles. And we can’t say that the dung smells the same to humans as it does to beetles: all we can say is that beetles and humans probably detect the same chemicals. The perception of odor, after all, is subjective.
There are probably many other cases of animal and plant mimicry that also involve odor, but aren’t so easy to detect because the odors are perceptible to insects or other beasts whose odor receptors differ from ours. After all, it was discovered only recently that the bee-and-wasp-resembling orchids have also evolved a scent resembling the mating pheromones of bees. There must be many aspects of mimicry that—as humans whose range of senses differs from that of many creatures who are duped—we simply cannot yet detect.
CODA: I was a young graduate student when I took my first trip to the tropics: a two month Organization for Tropical Studies course in ecology in Costa Rica. (It was a fantastic experience.) Before I went, one of my naturalist friends, the late Ken Miyata, gave me some advice. If you want to learn some biology, he said, go out in the forest by yourself and defecate. Then just sit near your leavings and watch them for a while. So I did it, and sat nearby for over an hour. Within a matter of five minutes, all manner of insects had descended on the pile, and soon the dung beetles came, rolling bits of scat into balls and trundling them away. Within an hour the pile was completely gone—eaten or sequestered by all kinds of beasts. Dung is a rich resource, and the rapidity of its disappearance shows not only its value to many species, but how well adapted they are at finding a small lump of excrement in the deep forest. In the tropics, nothing edible goes uneaten.
h/t: Kevin H.
____________
Midgley, J. J., White, J. D. M., Johnson, S. D. and G. N. Bronner. 2015. Faecal mimicry by plants found in seeds that fool dung beetles. Nature Plants 1, Article number: 15141 doi:10.1038/nplants.2015.141 (summary given on Phys Org).
sub
Perhaps the beetles discover the mistake when they try to lay eggs in the seeds – I imagine observing beetles egg-laying habits would confirm that?
Very interesting.
PS I have ner watched my own poo – to give the proper scientific term 😉 but have lain on the ground photographing animal poo to observe insects at work. Trouble is that in farmed land pesticides in dung can affect insects that eat it eg
http://onlinelibrary.wiley.com/doi/10.1111/j.1751-0813.1998.tb10159.x/abstract;jsessionid=E4371D2D4A24C299CF9C70FF9FAB18A1.f01t03
Very interesting!
Interesting.
“all we can say is that beetles and humans probably detect the same chemicals.”
Could this not be studied in the lab fairly easily? Expose the beetles to various compounds and observe their reactions.
Use artificial dung balls with the right color vs the wrong color. The right texture vs the wrong texture, and the right smell vs the wrong smell.
I found this to be a fantastic paper. It illustrates so many impressive aspects about what is life and how evolution solves physical problems to help preserve information.
This plant has utilized information (chemical and physical properties of its seeds) in order to minimize the energy required to help reproduce. Amazing.
Information, or knowledge in the case of humans who are aware of the information, is paramount to life being able to control and persist in nature. Give a chunk of uranium to someone who has no idea what atoms are and they will almost certainly die. Place the same chunk in a reactor and it can produce energy for thousands of people for decades. Science, or the process of gaining knowledge, always extends evolutionary advantages.
Sub
This so feeds me head. I tried to go to a medical genetics meeting this morning, hoping that the few others who hadn’t flown to Baltimore for a conference would show up. I left the cold, locked room, with a wistful longing for mental content. This satisfied it. Thanks!!
I greatly enjoyed the phrase “duplicitous plant.” The word randy was new to me and so well placed: I got quite an image.
In addition, nom is a word that was new until I started reading WEIT. I look forward to using nom in my speech, but for now, I just nommed a quiche.
Love the CODA. Both the deployment of the CODA and the content. It reminded me that I had what might be an anti-naturalist experience by comparison, when, in 1999 I’d traveled to Papua New Guinea to practice Tok Pisin. I have vivid memories of defecating in the bush. But, unlike you, I was trying desperately not to be creeped out by the creepy crawlies. Various villagers would construct ol haus pekpek (outhouses) to provide visitors some privacy, but they were crawling with insects. Spiders everywhere. It was much more comfortable to dispense with dignity and just go en plain air. I’m afraid the wonder of the insects was lost on me, though I do recall people saying that the spiders ate the birds.
I found the following information in a quick web search:
Restoniaceae is a monocot family widely distributed in the southern hemisphere of the Old World. One species occurs in South America (Chile); seeds may have floated there from New Zealand.
In the species of this plant family the sexes are separate (dioecious) and individual plants of the same species often differ markedly in appearance depending upon its sex!! This may or may not apply to Ceratocaryum. Sexual dimorphism may result from adaptations in male and female plants for growth in different habitats. Could it be (I shamelessly speculate) that male plants are adapted to, say, drier or less stony soils and dung beetles have been duped to roll some seeds to where males (and dung beetles) do best?
Good study that makes you want to learn more.
Trying to reverse-engineer free software to help other teams visualize HIV outbreaks in Athens & Odessa (and Chicago, though those dynamics are readily apparent)… excruciating stuff. (so was having to “pill” Butter, who may be getting an arthritic hip)
What a fascinating and welcome break from this tedious stuff. I want to be a population biologist when I grow up.
In a sense, this may qualify as shitty advice. But only on one interpretation.
If only faith were as fecund as feces!
b&
The Greatest Show on Earth!
Thanks for the CODA, that was some interesting shit.
Odd that the beetle would discover the deception after expending the energy to roll away and bury the seeds. I could understand if the beetles did not discover the deception at all. But a beetle that discovers the deception sooner should have a big advantage under the current scheme.
That surprised me, too. Sooner discovery may be the next step in the coevolutionary dance.
What this says is that the beetle lacks the capacity for foresightful planning. Instead, it operates off a program instilled by natural selection, with specific triggers for each step. When confronted with one of those triggers (e.g. a round ball of apparent dung), it executes the corresponding step (rolling it away and burying it). If a trigger is absent, that step does not get performed.
On this view the beetle doesn’t “discover the deception”; it just finds itself in a state with no appropriate triggers, and reverts to some default behavior (such as wandering off in search of dung).
Just a little over a week ago I was watching a pair of dung beetles in South Africa via a live webcam. In this species, the female rides the dung ball while the male rolls it to a suitable site (so sayeth the tour guides). The two were discovered at the edge of a dirt road and the male was trying to roll the ball up a small–but daunting to him–bank at road’s edge.
It was almost painful to watch, as several times he’d almost make it over the lip of the berm, only to lose control and have the ball carom back down into the road whilst he was frequently thrown onto his back. Meanwhile sweetie just clung serenely to the ball, waiting for him to recover his composure and begin the effort all over again.
In retrospect it seemed very much as you describe, programmed behavior with specific triggers. I was reminded of watching a hermit crab switching shells, going through a strict sequence of steps, returning to step one whenever the process was interrupted.
Some screen shots:
http://imageshack.com/a/img912/6979/46OaAz.png
Dung beetle rolling ball with female upon it
http://imageshack.com/a/img911/4425/bZpKni.png
Ball slips and male knocked to ground
I take it for granted that the beetle does not have the capacity of foresight and operates using a behavioral algorithm. But natural selection does not require such foresight.
So then your question comes down to: why don’t the trigger criteria for step N include the trigger criteria of step N+1, in order to detect errors sooner and avoid wasted effort?
Presumably the answer, as W.Benson notes below, has to do with the cost/benefit ratio of more complex triggers. Given the beetle’s limited cognitive capacity, maybe there’s an advantage to postponing trigger tests until they’re actually relevant, rather than front-loading the entire program with all the tests needed by all the steps.
Yet we still don’t really know if the relationship will remain static or change in the future… 🙂
I see what you’re saying, though.
Beetles get loads of poo each day all year long. Deceptive seeds will be few in number and only available a few days each year during the fruiting season. For a dung beetle, taking the time to discriminate may not compensate the time lost when examining the real thing. If the female does not roll the dung off quickly before competitors arrive, all may be lost.
Ah, makes sense.
If the seeds were to fall all year round, surely the little beetles would benefit from evolved strategies which discriminate better. The plant has done well for itself to only promote ‘in the noise’ loss of effort onto the beetle.
That probably answers my question, ‘could one expect beetles to evolve that try a nibble on the seed (/dung) _before_ rolling it away?’
It seems the answer is ‘not necessarily’.
cr
Perhaps there is some advantage to the beetle to bury the seeds? Maybe they act as decoys for some some parasitic wasp that goes after beetle larvae?
This is incredibly fascinating. Thank you for the article. When I first started reading and commenting on WEIT I struggled greatly with the science articles, but I now find them largely fascinating. While I could never become a scientist I am more scientifically aware than ever before, thanks to WEIT.
Holy sh*t, I just realized that Gingko seeds are also round, and as everyone who has teh pleasure of stepping on them knows they smell like poo. So maybe this is another example?
Hey, that’s right!
Turns out you get a lot of hits when you Google “why do Gingko seeds smell?” Unfortunately, the “why” turns out to be more of a “how”–they smell because of butyric acid–than an evolutionary explanation. (They also have allergenic compounds–alkylphenols–that are related to those in cashew shells and poison ivy, which makes one wonder if the chemical warfare is simply for discouraging seed predators.)
Also, most sites describe the odor as like vomit. My son & I know from experience that at least one tarantula is attracted to cat vomit–though we suspected at the time that it was the moisture the spider was after. 😀
Finally found an interview with a botanist who does relate the smell to seed dispersal:
http://e360.yale.edu/feature/peter_crane_history_of_ginkgo_earths_oldest_tree/2646/
…And brings up Dan Janzen’s suggestion that some extant plants may have adapted to dispersal by animal species that have since gone extinct.
A more diligent search would probably turn up more info; I only looked at a few hits, nor did I try Google scholar.
At any rate, fascinating!
Thanks for the info. It seems a reasonable hypothesis that lll those pungent secondary plant compounds made by Gingkos are there for some reason.
Absolutely! You can tell that I got excited by your musing. 😀
This kind of adaptation is so utterly fascinating to me. I can’t help by think about how many mutations and how many generations it took for these adaptations to manifest themselves in this way. I also am fascinated by the manner and the varying ways in which evolution can incorporate other species into the process. Sure, parasites abound but there are examples of symbiosis as well and in this case, without the presence of dung beetles there would have been no such adaptation, just some individuals of C. Argenteum with mutated smelly seeds.
I just happened to see a very determined Rainbow Scarab (Phanaeus vindex) amongst some composting horse manure in my garden the other day, so I looked up information about the beetles on the Texas A&M Agrilife Extension website. According to this resource, dung beetles are responsible for removing up to 80% of cattle droppings in some areas of Texas. I think that’s a load of bullsh*t, myself. 😉
This also demonstrates something interesting about this case of mimicry, and by extension about mimicry in general: mimicry need not be perfect, and indeed may be more adaptive when it’s deliberately imperfect.
In this case the plant wants the beetle to roll the seed away and bury it, so the mimicry must be accurate enough to trigger that portion of the beetle’s behavioral program. But the plant does not want the beetle to eat the seed or lay eggs in it, so its mimicry must not include the triggers of those behaviors.
More generally, the ideal mimic need not be a perfect mimic, indistinguishable from the thing being mimicked; rather, we should expect its mimicry to be narrowly targeted to a specific adaptive purpose.
In Nimoy’s voice : “Fascinating!”
“Dung is a rich resource, and the rapidity of its disappearance shows not only its value …”
Could this explain why a MacDonald’s burger gets eaten?
We all know what the beetles are thinking:
“Oh, no shit!”
A clear demonstration of why punctuation is important even to dung beetles!
b&
Does anyone know how a seed signalling that it is dung impacts on seed predation by organisms other than the local field mice? I know that in some ecosystems rodents target seeds in mammalian dung (from e.g. work by Andresen and Levey in the Amazon). But could it be that in this environment smelling like dung reduces seed predation by say ants, or by other beetles[1]? Maybe there is more than one advantage to this for Ceratocaryum argenteum.
[1] These are major seed predators in semi-arid sclerophyllous scrub in Australia. I don’t know if it’s true for the Cape’s fynbos, about which I know very little, but it seems likely.
Are there any smells C. argenteum cannot fabricate in its seed? Banana? Witch hazel? Pop corn? There must be virtually infinite smells that are possible. Is our plant, or any plant, capable of generating them all? If “yes,” how could our plant be so lucky as to evolve the dung smell? A P of 1/almost infinity (hopefully, you get the idea) is infinitesimal. It’s not gonna happen. And this line of reasoning? applies to the other characteristics in our present story, shape and size, and maybe to characteristics in general.
If our plant is limited in the present sense, why is it so limited? What constrains variation? I find it hard to believe that the right mutation can be “found” in general in each individual case, or maybe in any case, because of its high improbability. I am partial to the notion of constraint of variation, which means biased, rather than random, variation.
On occasion, popular press writers, like Ken Miller broach the topic of constraint. But the treatment, in my opinion, is desultory. For writers like Coyne and Dawkins, there is no issue. For writers like and Kirschner and Gerhart(The Plausibility of Life), constraint is huge.
Sorry to have changed the subject.
Every single Creationist example of the statistical likelihood of some trait arising is a most spectacular example of bad math.
And most presume that the particular outcome we observe was the goal of the process.
First, when you consider the number of offspring produced over the span of millions of years and the number of mutations per offspring and the number of variations possible simply within the plasticity of the genome coupled with sexual selection…it’d be a miracle if there weren’t any novel solutions found with such an exhaustive search.
And, second, it is not the case that this particular smell is the outcome that was being aimed for. Lots of other plants use entirely different reproductive strategies. Indeed, when you examine all the various successful reproductive strategies, it becomes quite apparent that successful reproductive strategies are a dime a dozen, and it’s just a matter of chance which species will stumble upon which strategy — and innumerable more successful strategies won’t be stumbled upon by any species.
Cheers,
b&
Thank you, Ben, really. But I do have a reply.
First, I don’t understand why Darwinists become irritated when someone wonders about the probability or improbability of the events subsumed under evolution. Besides the math there is, more importantly, a substantive issue. Excuse this next mini rant: Scientists deplore the public’s ignorance of evolution, but get irritated when someone raises a question that should occur to any half awake person. Scientists want people to accept unquestioningly what is put before them by scientists.
So why wouldn’t anyone wonder about the plausibility of several mutations occurring simultaneously? I know science’s answer to Behe’s concern. But Behe’s concern is reasonable, even though it turns out he was wrong. The math is not easy in the present general regard, and I doubt that anyone understands it. I mentioned Kirschner and Gerhart’s “The Plausibility of Life.” The book is really about the plausibility of natural selection and should have been so named. These scientist’s solution for making Darwin plausible is constrained or biased variation.
So cut people some slack; we are dealing with a
hard subject matter. Encourage questions and stop being defensive.
I have used up my time and have not addressed your substantive objections, Ben. Maybe later.
Sorry for the rant. Love and kisses.
David
Would you be irritated if a Flat Earther wondered why people in Australia don’t fall down into the Void?
If I have the statistics right, a typical human has roughly 50 novel base pair mutations out of a bit over three billion base pairs total — which simultaneously works out not merely to several simultaneous mutations but dozens…but merely 0.0000006% of the genome being mutated. At the same time, there are several billion humans on the planet, meaning, in total, there’re a third of a trillion mutations spread out amongst the entire human gene pool.
Each typical human is host to tens of trillions of bacteria of a great many different species. Each bacterium has its own genome with some fraction of mutations. And, rather than a generational time on the order of decades for humans, bacterial generational times can be on the order of hours or even minutes.
Humans are a tiny fraction of the life on Earth.
Here I am, just talking about humans and one subset of the organisms we carry around, and we’re already reaching into using terms like “trillions of quadrillions” to describe the number of mutations represented — and that’s before we even move on to the billions of years over which all this has been going on.
So, yeah. Gets damned frustrating damned quick when somebody who clearly has a problem with arithmetic as basic as I’ve just put forward above starts tossing around big numbers as some sort of reason why all this is impossible or even implausible.
Cheers,
b&
Nonetheless, you’ve responded quite helpfully; I hope Dave sees it.