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I'm currently supervising a graduate student who's writing a review of the literature on tool use in wild chimpanzees. This has become a most enjoyable interaction: it's a topic I've been interested in for quite a while now, so the supervision role is an excuse to extend my own knowledge, and it's great helping the student to enhance their own skills in relation to academic research and writing. 

Anyway, a couple of days ago I came across a new paper (Boesch et al., 2016) on an intriguing aspect of chimpanzee behaviour, and my student and I had a stimulating discussion about it at our regular weekly meeting this morning. (There's a general summary of the findings and the project which generated them here.) I'd previously heard of (& shared with her) what appeared to be an isolated incident of 'fishing' by an orangoutan, but this new paper documents wild common chimpanzees, Pan troglodytes, using a new technique to obtain freshwater algae. (Of interest in the orangoutan example were the claims that the image of the animal in action were faked, claims discussed here and dismissed as false.)

It seems that it's unusual for primates to eat aquatic plants, although they may eat fish and invertebrates when available. Both bonobos (Pan paniscus) and gorillas eat plants growing in swampy areas. Common chimpanzees do the same, but have also been reported eating algae - something that's really unusual in animals apart from marine species. And it's highly unusual in chimps too: 

despite decades of chimpanzee research, there are only a few observations of algae harvesting, suggesting that this behavior is indeed rare

and in most of these observations the chimps used their hands, rather than tools, to scoop algae from the water. It's possible, of course, that the local ecology of other well-studied chimpanzee groups just don't favour consumption of aquatic algae. But this behaviour could also be due to cultural evolution in a few small social groups.

So, Boesch and his team set up a research station at Bakoun, in Guinea (not far south of the equator), as part of a continent-wide attempt to 

contribute to a fuller understanding of the extent of chimpanzee behavioral variation and flexibility

in order to help get a handle on the actual level of behavioural diversity in wild chimps, and to answer questions around the relative effects of ecological diversity and cultural evolution on differences in behaviour shown by different groups of animals.

The chimps in the study area at Bakoun hadn't been studied before, and to minimise the potential impacts of interaction with humans, all observations were made using 'remote video camera traps', triggered to begin recording on detecting movement. These cameras were set up at sites where there was other evidence of chimp activity, such as remains of tools. Obviously they captured much more than chimpanzee activity, but of the 1,473 video clips that showed chimps, 486 (from 11 different sites), showed the animals 'fishing' for algae (Spirogyra sp.). Most of these events happened during the dry season, when water levels were lower, peaking in the 'hot dry' season when chimps returned repeatedly to the same sites over several days. 


The chimpanzees were observed to fish for algae at sites where the algae occurred in large accumulations at the bottom of the river bed.We rarely observed free floating, surface algae being targeted... [and we] observed all age and sex classes perform and succeed in fishing for algae from deep ponds or river shores.

Interestingly, the researchers found that every single animal used a tool to collect algae, even those only 2 or 3 years old - and they tended to use the same hand each time they fished. They fished by holding one end of a long stick, reaching it down to the bottom of the water, and then twirling the stick so that strings of algae were wound onto it. They then withdrew the stick and pulled the algae off with their lips. And, when algae fishing, the chimps usually avoided getting wet as much as possible. 

To see how successful this was as a food-gathering strategy, two of the research team used a discarded chimp tool - they managed to collect 400g of Spirogyra in just 10 minutes. Since individual chimps were seen fishing for an hour at a time, algae fishing could make quite a contribution to their seasonal diet:

chimpanzees may be fulfilling substantial dietary requirements [for protein, carbohydrates, and lipids, plus antioxidants and minerals] by ingesting large amounts of Spirogyra algae during the dry season

And just what were these tools? Mostly woody branches, modified by stripping off smaller branches and fraying one of both ends; some of these branches were up to 4m long, allowing access to algae that was otherwise unreachable in deeper parts of the river. In around 20% of events chimps arrived at their fishing sites already prepared ie bringing tools with them.

As I commented to my student, research like that described by Boesch and his colleagues goes well beyond simply documenting the activities of our close cousins. This is because, while it's likely our own hominin ancestors used a variety of plant-based tools, these aren't the sort of thing that's likely to be found by palaeontologists, and so 

research on primates can illuminate the potential repertoire of tool use behaviors that may reasonably be assumed to have been present in our last common ancestor (Boesch et al. 2016).

For example:

we suggest that in Bakoun, tool use permits a more efficient access to a rarely available but highly preferred resource, such as algae, that permits chimpanzees to flourish in an environment otherwise more limited in food and water. It is therefore probable that our last common ancestor would have similarly made and used tools to also engage in rudimentary fishing, to collect and consume rich aquatic fauna, and perhaps flora too (ibid.).

And

This [research] demonstrates the flexibility in [chimpanzee] technical skills and how this helps them to obtain access to valuable resources in a drier habitat and new context. Such technological skills have been suggested to be present in our human ancestors when they invaded drier, savanna habitat during the course of human evolution (ibid.).

C.Boesch, A.K.Kalan, A.Agbor, M.Arandjelovic, P.Dieguez, V.Lapeyre, and H.S.Kuhl (2016) Chimpanzees routinely fish for algae with tools during the dry season in Bakoun, Guinea. American Journal of Primatology 78(12), published on-line 3 November 2016. DOI: 10.1002/ajp.22613

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I mean, really - have you ever seen something like this before?
 

Melibe engeli is a type of sea slug, and a most unusual one. Its body is partly translucent, and has projections called cerata, themselves covered with smaller projections called papillae, down both sides. The animal is an active hunter - but what a hunter. It lacks the toothy radula seen in most gastropods, & instead has that amazing, extendible, 'hood' around its mouth. Tiny, highly-sensitive hairs detect prey & trigger the animal to close the hood; the prey animal is engulfed whole, to die during the digestive process.

I don't think sci-fi could come up with anything stranger than this!

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There's a lovely, life-size bronze sculpture of a Powelliphanta land snail sitting on my china cabinet. I love it because a friend made it for us - and because snails in this genus are rather special, for they are all carnivorous.

Now, I 'knew' this fact, but I'd never actually seen one feeding. Snails being normally rather slow, sedate creatures, it was hard to imagine how they'd ever catch anything other than even slower prey. That was until I saw this video

Every earthworm's nightmare!

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The semester's begun, teaching has started, admin isn't letting up any time soon, & there are days when I feel like a zombie by home-time. So it seems entirely appropriate to revivify a post I wrote 3 years ago, on that very subject.

Honestly, sometimes I think the zombie apocalypse is already here. Certainly zombies seem to be flavour of the month (& whatever friends say, I still can't bring myself to watch Walking Dead). And I've written about them myself: well, the insect variety, anyway.

But our developing understanding of how parasites 'zombify' their hosts has been developing since well before the latest iteration of human zombies grabbed the popular imagination. I was reminded of this when I saw the video below (in all its over-the-top hyperbolic glory), for I was first introduced to the concept of zombie snails years & years ago by one of David Attenborough's TV programs**. (According to my aging memory, it would have been an episode of Life on Earth.) 

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So, last night I was asked how hedgehogs mate. 

The obvious answer was, carefully! My interlocutor suggested that perhaps face-to-face was most likely, but as far as I know, very few species (& that short list includes our own) do that. It turns out that care is indeed needed, for the male approaches the female from behind, & she must adopt what's coyly called a 'special posture' and flatten her spines so that the sensitive portion of his anatomy doesn't take on the appearance of a kebab.

The question was actually part of a wider discussion around the architecture of sexual reproduction: the mechanics of how the bits fit. If you'd like to hear the entire thing, it's here on the RadioLive site.) Entomologists, in particular, seem to spend quite a bit of time studying this architecture, not least because these details may help them distinguish between species that are otherwise pretty much identical in their appearance. (There's a lovely story about Michael May's work on dragonflies here, complete with etchings illustrations.)

In many cases the structures - which can be quite bizarre - are driven by competition. Competition between the males, but also between males and females. So in those dragonflies, for example, the males' penes have all sorts of features that are related to sperm competition - they allow a male to scoop out, scrape out, or otherwise displace semen deposited by another male, and replace it with their own. And in mallard ducks, which are highly promiscuous, a sort of male/female arms race has driven the evolution of extremely complex genital anatomy in both males & females, discussed here by Ed Yong. Incidentally, that link also includes a video - perhaps not for the faint-hearted! - of the rather explosive uncoiling of & ejaculation from the drake's corkscrew penis.

Some of these structures can be rather large: we're talking a metre long for male African elephants, for example (according to wikipedia), around 2.7m in right whales, and up to 3m in Blue whales (the largest animals alive). And as one might expect, this has been attracting human attention for a long, long time. Sadly, some of that attention has been seriously harmful to the survival of some species - witness the aphrodisiac claims made for the sex organs of tigers by Traditional Chinese Medicine, for example. But there's also the point-&-wink sort of interest, shown in a painting of a dead sperm whale dating from 1606 and described by Menno Schilthuizen in the excellent book, Nature's Nether Regions:

On an otherwise nondescript Dutch beach likes the Leviathan, its beak agape, its limp tongue touching the sand. A smattering of well-dressed seventeeth-century Dutchmen stand around the beast. Prominently located, and closest to the dead whale, stand a gentleman and his lady. With a lewd smile, face turned towards his companion, he points at the two-metre-long penis of the whale that sticks out obscenely from the corpse. Centuries of smoke-tanned varnish cannot conceal the look of bewilderment in her eyes.

These few square feet of canvas ... [exemplify]... the unassailable fact (supported by millenia of bathroom graffiti, centuries of suggestive postcards, and decades of internet images) that humans find genitals endlessly fascinating.

However, it's only relatively recently that this fascination has really been reflected by scientific interest: interest in the structures, their function, and their evolutionary history. But, as Brian Switek points out in his book My Beloved Brontosaurus (which is also an excellent read), we still have no idea how dinosaurs - especially the big ones - actually mananged to mate. Particularly the big spiny ones. This may well remain one of life's not-so-little mysteries. 

 

It has occurred to me that the search history on my computer will look really, really odd as a result of doing a spot of research for this post!

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Demodex mites are tiny little creatures that live in mammals' hair follicles. I first heard about them years ago, when I watched a documentary with my science class back at PN Girls' High. It was about animals that are parasitic on humans, and after the segment on eyelash mites, I don't know about the girls but I felt itchy for days!

For eyelash mites live where the name suggests, in the follicles of our eyelashes. (There are 2 species: Demodex folliculorum and D. brevis.) The common name gives an idea of just how small they are: adult length is 0.3 to 0.4 mm. They spend a lot of time inside the eyelash follicles, snacking on the sebum and dead cells (or maybe the bacteria) that accumulate there. But at night... at night, they come out and wander across our faces as we sleep, achieving a speed of 10cm/hr or more. Which doesn't sound much, but when you remember how small they are, that's quite an achievement. Presumably that's also when they mate, which they do where an eyelash follicle opens to the skin's surface. 

I was surprised to discover that these mites lack an anus. This sounds somewhat problematic, but the eyelash mites have survived, with their human hosts, for at least tens of thousands of years, so they obviously cope somehow. And when they die, their little bodies degrade and release their contents. On your face. Or in the follicles where they spent most of their lives.

Though demodex mites are tiny, there are an awful lot of them. There may be only one or two per hair follicle (they don't restrict themselves to the eyelashes), but an individual human has around 5,000,000 hairs on their body (Thoemmes et al., 2014), so that's an awful lot of available places for a mite to set up home in.

Thoemmes & her co-workers were interested in the genetic diversity of these mites. They predicted there'd be geographically-distinct lineages, because the tiny animals are very closely associated with their hosts and don't seem to be particularly mobile between hosts. However,

if Demodex lack strong geographic structure, it suggests the movement of mites among humans must occur very frequently (perhaps even with social greeting rituals) and across large geographic distances.

To test this hypothesis, the team examined adults (from a single North American population) visually, but also tested skin scrapings for the presence of mite DNA. The results showed that despite being able to see mites on only 23% of their sample population, 16S rDNA sequencing indicated that 100% of those sampled actually had mites present. The latter matched other research showing that 100% of dead bodies tested positive for the presence of Demodex.

Figure 2 from Thoemmes et al. (2014): Maximum likelihood (ML) phylogeny of mites based on 18S rDNA sequences.

While the results of their phylogenetic analysis of the mite DNA are based on samples from only 29 people, they're interesting nonetheless. It appears from that analysis that the 2 species, D.folliculorum & D.brevis, probably colonised humans at different times. Because D.brevis' DNA indicates that their nearest living relatives are mites living on dogs, then the researchers suggest that we acquired this species from our doggy friends, perhaps as recently as 11,000 years ago but possibly as many as 40,000 years ago. There does appear to be some regional variation (based on a comparison of the US data with earlier sequencing results from Chinese populations), but there's also quite a bit of variation within populations, due perhaps to individual humans picking up different mites on different occasions as individual humans came into close physical contact.

And after reading all this & watching a few videos, I feel itchy again!

Thoemmes MS, Fergus DJ, Urban J, Trautwein M, Dunn RR (2014) Ubiquity and Diversity of Human-Associated Demodex Mites. PLoS ONE 9(8): e106265. doi:10.1371/journal.pone.0106265

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Once upon a time, I wrote about traumatic insemination in bedbugs. (Those of my friends who are still traumatised by learning about the reproductive habits of various slug species may not wish to follow that link.) Now, two papers just published in Nature Communications describe the results of sequencing & examining the genome of the common bedbug, Cimex lectularius

Bedbugs have probably been with us since humans first lived in caves, where the bugs jumped (possibly literally) from bats to Homo. They're now a widespread human ectoparasite (found on every continent apart from Antarctica) and have developed resistance to the pesticides once used to control their populations. In introducing their paper on their analysis of the C.lectularius genome, Rosenfeld & his colleagues (2016) comment that

There is a limited molecular understanding of the biology of the bed bug before, during and after feeding on human blood, which is essential to their life cycle since bed bugs are temporary ectoparasites, whereby they access their hosts for blood feeding and then seek the refuge of the indoor environment for digestion, waste production and mating.

To increase our understanding of the bugs' life cycle, Rosenfeld's team looked not only at the genome sequence but at changes in gene expression, finding the most pronounced changes occurred after the insect had sucked its fill of human blood. They also found that these changes in expression 

included genes from the Wolbachia endosymbiont, which shows a simultaneous and coordinated host/commensal response to haematophagous activity. 

In other words, gene expression in both host and parasite changes in a synchronous way after the bug has fed. (Just as an aside, Wolbachia is a bacterium that has a significant impact on the reproductive lives of its host.) In the bugs the change could be described as huge: "20% of all stage-regulated genes" showed differential changes in expression after a blood meal.

As you'd expect, the bugs have a number of genes with anticoagulant activity - after all, having blood coagulate in their needle-like mouthparts while feeding would really gum things up - plus other genes associated with blood-feeding. The research team also identified a number of mutations that confer resistance to pesticides such as pyrethroids & cyclodienes, plus others that may underlie metabolic changes that speed up detoxification. Genes that have an impact on the thickness of the bugs' cuticle also have an impact on resistance (also noted by Benoit et al. 2016). 

In the second paper, Benoit and his colleagues (2016) also analysed the common bedbug genome to produce

a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host–symbiont interactions, and several mechanisms of insecticide resistance.

Traumatic insemination involves male bugs stabbing their sexual partners pretty much anywhere on their bodies with a sharp, pointy, penis. It's a habit that can lead to the females picking up a range of pathogens, and unsurprisingly natural selection has driven the evolution of a range of adaptations minimising the physical harm and risk of infection. 

Because the bugs are obligate blood-feeders (haematophagous), their chemosensory system has evolved to allow them to find their particular hosts (ie us). The team observed that the genes involved in this system differed between C.lectularius & the related species that feeds on bat blood, as the 2 species have specialised on different hosts. They identified a total of 102 genes involved in chemosensory pathways, well down on the number found in related bugs (hemipterans) that feed on a range of plant species. (On the other hand, they have a much-expanded repertoire of salivary enzymes, compared to the plant-sucking bugs.)

The bedbugs' specialisation on human blood as their sole food source did have some potential pitfalls, as apparently vertebrate blood lacks some of the micronutrients that arthropods require. And that's where Wolbachia comes back into the story: 

such specialization also drives obligate associations with symbionts, including Wolbachia, that generate critical micronutrients that are deficient in vertebrate blood (Benoit et al., 2016).

Wolbachia does this by providing its host with 

a cocktail of specific B vitamins that are critical for reproduction and development

The research team also found genes encoding proteins (aquaporins) that allow the bugs to rapidly shed the excess water imbibed in a blood meal, and concluded that differential expression of aquaporin genes (and others) allow the bugs to survive periods of starvation and dehydration in between hosts.

In their conclusion, Benoit et al. comment that the wealth of information uncovered by these genomic studies may allow us to move towards an answer to a pressing question: 

What triggered the current bed bug resurgence?

To which harassed travellers would probably add, and how can we bring them back under control?

J.B.Benoit, Z.N.Adelman, K.Reinhardt, A.Dolan, M.Poelchau, E.C.Jennings, E.M.Szuter, R.W.Hagan, H,Gujar, J.N.Shukla, F,Zhu, M.Mohan, D.R.Nelson, A.J.Rosendale, C.Derst, V.Resnik, S.Wernig, P.Menegazzi, C.Wegener, N.Peschel et al. (2016) Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nature Communications 7 Article number 10165 doi:10.1038/ncomms10165

J.A.Rosenfeld,D.Reeves, M.R.Brugler, A.Narechania, S.Simon, R.Durrett ,J.Foox, K.Shianna, M.C.Schatz, J.Gandara, E.Afshinnekoo, E.T.Lam, A.R.Hastie, S.Chan, H.Cao, M. Saghbini, A.Kentsis, P.J.Planet, V.Kholodovych, M.Tessler et al. (2016) Genome assembly and geospatial phylogenomics of the bed bug Cimex lectularius.  Nature Communications 7 Article number: 10164 doi:10.1038/ncomms10164

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By now many of you have probably seen images of green-glowing zebrafish, or pigs whose snout & trotters glow in the dark. In both cases the animals are genetically modified and are expressing a fluorescent protein originally sourced from a jellyfish. (The body form of a jellyfish is a medusa, while that of sea anemones & their freshwater relative, Hydra, is called a polyp.) There are a range of these proteins, which collectively belong to a group called the Green Fluorescent Proteins (what else?), and while a wide range of jellyfish produce them1 there are only occasional reports of glowing polyps.

However, in a paper just published in the open-access journal PLoS ONE, Andrey Prudkovsky & his colleagues describe finding tiny (~1.5 mm) fluorescent polyps living in the Red Sea. More specifically, growing in colonies on the shells of small gastropods, a relationship described as epibiotic. The snails are active at night on the sandy seabed, and the researchers noted that the little gastropods buried themselves in the sand when a torch shone on them. They also noticed that the snails, as they moved about in the moonlight, were covered with tiny pinpoints of green light.

Where fluorescence has been described in other polyps, it's mostly been in the 'stalks' of the little animals, but in all the polyps Prudkovsky's team studied, the intense green glow came from a region known as the hypostome - the region around the animal's mouth & encircled by its tentacles. Because both the intensity and the site at which the proteins are expressed is so unusual, the researchers suggest that this could be a useful taxonomic characteristic, given that it's hard to tell one colonial polyp species from another.

They also speculate on the adaptive significance of a polyp having a green glow around its mouth, suggesting that 

[f]luorescence in the hypostome of Cytaeis sp. has probable ecological significance as prey are likely to be attracted to the tentacles and mouth of the polyps

although I do feel that until there's actual observational evidence of this happening, it's a little like an evolutionary just-so story. But isn't the combination of little snails and glowing polyps rather beautiful?

Fig 3.  Hydroid polyps of Cytaeis sp. from the Saudi Arabian Red Sea, scale bar 2 mm; (A) fluorescence of living polyps on the shell of the gastropod Nassarius margaritifer; (B) polyps on the shell of a N. margaritifer specimen, scale bar 2 mm; (C) close-up of polyps, scale bar 0.5 mm.

Fig 3 From Prudkovsky et al., 2016: Hydroid polyps of Cytaeis sp. from the Saudi Arabian Red Sea, scale bar 2mm; (A) fluorescence of living polyps on the shell of the gastropod Nassarius margaritifer; (B) polyps on the shell of a N.margaritifer specimen, scale bar 2mm; (C) close-up of polyps, scale bar 0.5mm. doi:10.1371/journal.pone.0146861.g003

1 And also in comb jellies, marine arthropods, and cephalopods cephalochordates (thanks to herr doktor bimler for picking up the evidence of my brainfade).

Prudkovsky AA, Ivanenko VN, Nikitin MA, Lukyanov KA, Belousova A, Reimer JD, et al. (2016) Green Fluorescence of Cytaeis Hydroids Living in Association with Nassarius Gastropods in the Red Sea. PLoS ONE 11(2): e0146861. doi:10.1371/journal.pone.0146861

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Following on from the private lives of snails, I bring you: slugs! (The first part of this post is largely a repost of something I wrote back in 2009.)

 

Leopard slugs, like other terrestrial slugs & snails, are hermaphrodites. They produce both eggs & sperm, but must exchange sperm with another slug in order to fertilise their eggs. (This reproductive strategy means that an amorous snail or slug doesn't have to find a partner of the opposite sex, it needs only to meet another snail. Or slug. Of the same species, of course.) Actual copulation is preceded by a range of somewhat slimy courtship & precopulatory displays - in garden snails this involves (among other things) piercing one's partner with crystalline darts... Sounds painful, I know, but this part of the ritual apparently enhances uptake of the piercer's sperm by its partner.

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This morning when I went out to feed the goldfish, I encountered a pair of snails in flagrante delicto. I resisted the urge to step on them :)

However, I was reminded of a post that I wrote several years ago, on the sexual habits of snails, and thought it was worth a repost. So here goes:

Copulation in garden snails is generally preceded by (among other things) pushing 'darts' into each other's bodies. There've been various explanations for this odd behaviour (I mean, it sounds painful!), including the suggestion that the dart acts as some sort of 'wedding present' (nuptial gift), which might make the pierced partner more inclined to mating. Or that it indicates how ready the dart-shooting snail is to mate. But data from a 2001 study (Pomiankowski& Reguera) suggests another reason for this behaviour.

Snails have quite intimate, elaborate courtship rituals that involve a lot of close physical contact before actually mating. After about 30 minutes of mutual stimulation, one snail pushes a sharp pointed dart into the other. (This is often described as 'shooting', but it isn't - it's more of a hard push.) The darts aren't essential for copulation - virgin snails don't have darts, but still mate successfully. (As do snails that miss the mark - apparently around 33% of darts either don't hit the partner at all, or fail to enter their body.) So why go to the trouble of making darts (which aren't re-used, so an amorous snail must be constantly making new ones)?

It seems that the dart carries mucus along with it, & this mucus seems to paralyse the partner's female reproductive tubing. This lets more sperm make it to the sperm storage organs, where they're stored until needed to fertilise the eggs. This is important - when garden snails (Helix aspersa) mate they produce & pass to their partner a spermatophore containing 1-10 million sperm, but only about 0.025% survive in the partner's female reproductive tract (Pomiankowski & Reguera, 2001). Most of them end up in the no-return area of the bursa copulatrix, where they're digested & absorbed. But in a study of mating pairs, virgin snails that were firmly pierced by their partner's dart contained twice the stored sperm of non-stabbed virgins. And yet 

successful shooters appeard to transfer fewer sperm than did unsuccessful shooters. This suggests that successful shooters can afford to reduce the amount of sperm transferred because the penetration of dart mucus ensures a higher rate of sperm storage.

Koene & Schulenburg (2005) suggested that this may well lead to something of an arms race between the manufacture of a 'love dart' that maximises the shooter's success, and the female spermatophore-receiving organs (because the 'female' partner's reproductive success may benefit by using sperm from as wide a range of partners as possible).

But there's a lot we don't know about the finer details of snail reproduction. For example, snails may vary in how their female tracts respond to the paralysing mucus. And what's the story in those snail species that don't shoot their partners during foreplay? Hard questions to answer...

A. Pomiankowski & P. Reguera (2001) The point of love. Trends in Ecology & Evolution 16(10) 533-34

J.M.Koene & H.Schulenburg (2005) Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails. BMC Evolutionary Biology 5:25 doi:10.1186/1471-2148-5-25

Mind you, the inimitable "True Facts" also does a good line on this tale :)

 

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