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Monday, June 18, 2012

Snake-eating beetles


So little is known about the parasites of snakes that we tend to discount them all together, but the ecological  and evolutionary interactions between hosts and their parasites can be very strong. This is a story about how two enterprising snake biologists solved a mystery that had been puzzling entomologists for decades.

Burying beetles (genus Nicrophorus) conceal small vertebrate carcasses underground and prepare them for consumption by their young by excavating a crypt up to 60 cm deep, removing fur or feathers from the carcass, and covering it in anal secretions to prevent fungal growth. The two parents slowly eat the carcass, defending it from other carrion eaters, and feed regurgitated bits of it to their altricial larvae, which hatch from eggs they lay in the walls of the crypt and beg to be fed like baby birds. Although feeding your babies poop-coated vomit sounds like the plot of a gruesome horror movie, it has been a successful evolutionary strategy for the burying beetles. Their complex social behavior, including biparental care and communal breeding, is unusual among insects. The whole process takes about two weeks.

Nicrophorus pustulatus
Of the nearly 75 species of burying beetle, distributed throughout the Northern Hemisphere, one in particular stands out for its unusual natural history. Entomologists studying the group use dead mice to bait traps, but one species, Nicrophorus pustulatus, never seemed attracted to the carrion. In addition, they are able to produce very large broods (up to 190 vs. 30-45 for most other species of burying beetle) of large offspring on carcasses in the laboratory. Usually, a large brood size comes hand-in-hand with a decrease in individual offspring size, but not in this species apparently. Why not?

Theories ranged from that N. pustulatus used larger carcasses, such as rabbits, without burying them, to that  it was an interspecific brood parasite, like a brown-headed cowbird, laying its eggs in the nests of other burying beetles. But in 2000, a paper in the journal Ecoscience by two snake biologists, Gabriel Blouin-Demers and Patrick Weatherhead, then of Carleton University in Ontario, revealed a surprising discovery. They were studying the nesting ecology of black ratsnakes (Pantherophis obsoletus, formerly Elaphe obsoleta) in Canada by radio-tracking adult female ratsnakes to their oviposition sites. Their purpose was to document the use of communal nests by these snakes and to collect information on clutch size and juvenile survival. When they examined the ratsnake nests they found, they discovered that many of them contained adult and larval  N. pustulatus.

Ratsnake eggs parasitized by carrion beetles
Blouin-Demers and Weatherhead found evidence of beetles in six of the seven nests they looked at. In some nests, only old eggshells with small holes evidenced the beetles' presence, but in others 100% of the eggs were destroyed by the beetles and their larvae. Because black ratsnakes nest communally in this part of the world, up to 111 eggs can constitute a nest, even though the average clutch size is only 11-15 eggs per female. The ratsnakes use the same communal nesting sites year after year, which can be highly beneficial because of increased nest temperature and shorter development time. At such northern latitudes, female ratsnakes do not lay eggs until June or July, and the babies must hatch by late August in order to avoid being killed by an early frost. A mother ratsnake's only parental care is her nest site choice, and research has shown that eggs laid in communal nests hatch earlier, grow larger in their first year, and can even swim faster than those incubated with just their clutchmates. However, the probability of a beetle infection probably increases with increasing nest size, because it only takes one infected egg to spread the beetles to the whole nest. This is why N. pustulatus is so fecund compared to other carrion beetles - because it can raise enormous numbers of larvae on large snake nests, full of nutritious eggs and already hidden away in sites with ideal thermal and humidity.

Black Ratsnake (Pantherophis obsoletus)
Based on their findings, Blouin-Demers and Weatherhead characterized N. pustulatus as a parasitoid of snakes. A parasitoid is different from a parasite because they are parasitic only as larvae (although in this case, with a little help from their parents), and they always kill their host. However, they are also different from predators, because each parasitoid larva only kills a single host individual instead of many. Blouin-Demers and Weatherhead suggested that theirs was the first example of a vertebrate being host to an arthropod parasitoid, and so far they are correct.

The full mystery is far from solved, though. Did N. pustulatus evolve this behavior by first exploiting snake eggs that failed to hatch? How do the beetles find reptile eggs? Are communal nests easier for the beetles to find, or do they simply prefer them because of their higher concentration of resources? How has parasitism by this beetle influenced ratsnake evolution? Do any other species of Nircophorus also parasitize reptile eggs? Does N. pustulatus beetles also parasitize the eggs of other species of snake? Observations of fox snake (Pantherophis vulpinus) nests in Illinois have also yielded beetle larvae. The range of N. pustulatus extends farther north than that of any oviparous snake species (snakes at high latitudes tend to be viviparous, because the females can more precisely control the temperature of their developing offspring if they carry them around). What do they use for rearing their young up there? Could it be turtle eggs, or do they use small animal carcasses like their ancestors?

Nicrophorus pustulatus with phoretic mites
From the beetle's perspective, it has arrived at a very successful reproductive strategy by shifting hosts. By moving away from nesting in carcasses, for which they must compete with flies, ants, fungi, bacteria, and scavenging vertebrates such as skunks and raccoons, it has secured an apparently unique niche. As a defense against carcass competitors, some Nicrophorus species carry phoretic mites that eat fly eggs, but lab experiments have shown that the mites sometimes eat the beetles' eggs too, so the benefit is not without risk. Additionally, not having to move or bury snake eggs saves the parent beetles a lot of energy prior to laying their eggs. Experiments have shown that N. pustulatus females oviposit rapidly in house snake (Lamprophis) eggs, and that male beetles elevate their sex pheromone emission in response to snake eggs. Other beetles in the genus Nicrophorus did not show the same response. While N. pustulatus will use mouse carcasses to rear their young in the lab, no one has ever found them doing so in the field. The entomologists who performed these lab tests also found that N. pustulatus adjusted its fecundity to the available mass of snake eggs.

As a driver of evolution in oviparous snake nesting strategies, Nicrophorus pustulatus may play an important role. Could they potentially pose a threat to egg-laying snake species that are of conservation concern, such as the Eastern Indigo Snake (Drymarchon couperi)? What might happen if they were introduced to a continent whose snakes had not evolved with parasitic beetles eating their eggs? There is still so much we don't understand about snake behavior, reproduction, ecology, and evolution, especially in the wild. Thanks to the observations of a few scientists who thought they were studying something else entirely, we are one step closer.


ACKNOWLEDGMENTS

Thanks to Joyce Gross, Loren Padelford, and Gabriel Blouin-Demers for allowing me to use their photographs.

REFERENCES

Blouin-Demers G, Weatherhead PJ (2000) A novel association between a beetle and a snake: parasitism of Elaphe obsoleta by Nicrophorus pustulatus. Ecoscience 7:395-397 <link>

Blouin-Demers G, Weatherhead PJ, Row JR (2004) Phenotypic consequences of nest-site selection in black rat snakes (Elaphe obsoleta). Canadian Journal of Zoology 82:449-456 <link>

Ikeda H, Kubota K, Kagaya T, Abe T (2006) Niche differentiation of burying beetles (Coleoptera: Silphidae: Nicrophorinae) in carcass use in relation to body size: estimation from stable isotope analysis. Applied Entomology and Zoology 41:561-564 <link>

Robertson IC (1992) Relative abundance of Nicrophorus pustulatus (Coleoptera: Silphidae) in a burying beetle community, with notes on its reproductive behavior. Psyche 99:189-198 <link>

Scott MP (1998) The ecology and behavior of burying beetles. Annual Review of Entomology 43:595-618 <link>

Smith G, Trumbo S, Sikes D, Scott M, Smith R (2007) Host shift by the burying beetle, Nicrophorus pustulatus, a parasitoid of snake eggs. Journal of Evolutionary Biology 20:2389-2399 <link

Trumbo ST (2007) Defending young biparentally: female risk-taking with and without a male in the burying beetle, Nicrophorus pustulatus. Behavioral Ecology and Sociobiology 61:1717-1723 <link>

Creative Commons License

Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

6 comments:

Ember Lynne said...

"poop-coated vomit" Wordsmith extraordinaire, Mr. Durso.

But I wanted to ask how the hell you test the sex pheromone emissions of male beetles? I have this image in my head of a huddle of scientists intently trying to sample the "aura" of a little beetle caught in pincers or something. Please tell me I'm wrong...?

Andrew Durso said...

The article says they could tell just by looking at their posture - they looked 8 times over 4 hours, and scored each male as either releasing or not. More boring than your image, and also less quantitative...

Ember Lynne said...

not what I expected! but now I just have more questions. How do you first find out this posture is releasing and that posture isn't? This is what always happens with science! You get one little piece of information and it makes you curious. Then, if you're Durso, a few decades later, you get a PhD.

Andrew Durso said...

I suppose it was already known from other behavioral studies of this beetle genus. A quick search reveals this paper:

http://www.jstor.org/stable/10.2307/4534795

the first sentences of which are:

"Pheromone emission in male burying beetles was first described by Pukowski (1933) who had observed a conspicuous behaviour of males that had remained alone on a carcass: They climb an elevated place and
adopt a 'typical, very surprising posture' (translation by the authors) with the head held down and the extremely extended abdomen pointing up. This posture
is maintained for several hours, and only the tip of the abdomen is moved slightly up and down or in circles."

So in this case, the behavior was so conspicuous that it was described before its true function was known.

Sam said...

That's not the only invertebrate parasitoid of vertebrates. There are helminths that kill fish, parasitic flies that kill toads and lizards, and even large animals like deer, sheep, and humans can be killed by heavy infestations of screwworms.

Andrew Durso said...

Thanks for your insightful comment Sam. I'm not overly familiar with the parasitoid literature. My statement above was relaying what Blouin-Demers and Weatherhead wrote in their paper, and at the time I couldn't think of any other examples. Your third example sounds like a parasite that can be lethal at high levels, which I don't think is quite the same as a parasitoid (because individual screwworms don't kill their hosts). A quick search revealed that most fish-infecting helminths are referred to as 'parasites', but I didn't get to delve into their natural history yet. On the other hand, calliphorid flies are definite parasitoids of toads I'm surprised that Blouin-Demers and Weatherhead overlooked this, since it seems to have been known for a long time. I'd love to see some more literature on other cases; can you post some links?