Mystery of the Mangy Squirrel Slurry – solved!

A few posts ago I presented a puzzle – what were the strange arthropod-like creatures I found in a KOH-dissolved slurry of eastern gray squirrel skin? I canvassed colleagues from around the world, and none had a definitive answer (though Terry Galloway from the University of Manitoba guessed the correct order, or suborder depending on your taxonomy). Yesterday I received a second square of skin from the same squirrel, also sent by Jamie Rothenburger. This time I didn’t dissolve it in KOH but rather just plopped it in ethanol and examined it underneath a dissecting scope. Lo! Dozens of the tiny mystery animals were attached to the squirrel’s hairs. Even better, four older instars, including an adult, were also present. So, what did they turn out to be? Sucking lice (Anoplura), most likely Enderleinellus longiceps Kellogg & Ferris based on papers by Kim (1996 a, b). UPDATE: no, it is not E. longiceps, it doesn’t even belong to that genus. I keyed out the adult female today and she turned out to be Neohaematopinus sciuri Jancke based on Kim et al. (1986). I was a bit too eager to get photos of the critters and didn’t wait until the slides were completely cured, so the images below are a little blurry. First are photos of embryonic lice still in eggs, then photos of what I think is a second nymphal instar. The scalloped structure beneath the tarsal claw that was particularly obvious on the legs of the animals in the original post are less striking in the nymph.

Nits on squirrel hair.

Two eggs on a squirrel hair, one occupied.

Enderleinellus in egg B

Close-up of one embryo popping out of the egg.

Enderleinellus nymph habitus B

Nymphal sucking louse, Neohaematopinus sciuri.

Enderleinellus nymph head

Internal mouthparts of the nymph.

Enderleinellus nymph claw with scallop

Tarsus of second leg showing faint scalloped structure.

Enderleinellus nymph scales

A nice scaly patch of integument from the dorsum of the nymph.

Neohaematopinus sciuri female habitus

Adult female Neohaematopinus sciuri.

Neohaematopinus sciuri sternum

Relative sizes of tarsal claws of legs I to III and shape of the sternal sclerite (arrow) helped to identify the female as belonging to the family Polyplacidae and the genus Neohaematopinus.

References

Kim, K.C. 1966. The species of Enderleinellus (Anoplura, Hoplopleuridae) parasitic on the Sciurini and Tamiasciurini. J. Parasitol. 52: 988-1024

Kim, K.C. 1966 The nymphal stages of three North American species of the genu Enderleinellus Fahrenholz (Anoplura: Hoplopleuridae). J. Med. Ent. 2: 327-330.

Kim, K.C., H.D. Pratt and C.J. Stojanovich. 1986. The Sucking Lice of North America: an Illustrated Manual for Identification. Pennsylvania State University Press, University Park.

Who likes shrews? These mites do!

My friend Allan Lindoe, fossil preparator extraordinaire, lives on an acreage near Athabasca and makes the journey south to Edmonton about once a week to carefully remove rocky matrix from around the skeletons of long-dead fishes, mosasaurs, and dinosaurs. Two cats share his home and frequently bring him presents of wild game. A few weeks ago I washed a mixed bag (literally) of a dozen shrews he had accumulated over the summer and fall of 2015. Chewed-on shrews are not easy to identify unless you know a lot about insectivore teeth, but based on tail length and known distributions of shrew species in Alberta, they were one or more of the masked shrew (Sorex cinereus), Arctic shrew (S. arcticus), pygmy shrew (S. hoyi) and/or dusky shrew (S. monticolus)*. Some of the shrews were rather decomposed, so I wasn’t expecting much from the washings, but I was pleasantly surprised: 6 species of mites! Members of both major lineages were present. From the Acariformes were Prostigmata (Myobiidae, Pygmephoridae and Trombiculidae) and Sarcoptiformes (Glycyphagidae). From the Parasitiformes there were larval hard ticks (Ixodida: Ixodidae) and what look like Melicharidae (Mesostigmata).  Myobiids, trombiculids, and ixodids are parasitic, and the others are all likely just phoretic. Who knew the zoo on shrews? Now you do.

Protomyobia female ex shrew

Protomyobia nr. claparedei female (note egg).

 

Protomyobia ex shrew

Protomyobia nr. claparedei male (note well-sclerotized aedeagus).

 

Protomyobia lv I think A

Larval Protomyobia nr. claparedei (note styletiform chelicerae).

 

pygmephorid ex shrew

Ventral view of one of the many pygmephorids from the shrew washings.

 

pygmephorid ex shrew legs I

Pygmephorid showing modified legs I.

 

chigger ex shrew A

Dorsal view of a shrew chigger (Trombiculidae).

 

chigger ex shrew B

Prodorsal shield of a shrew chigger, showing the posterior pair of trichobothria and single anterior median seta (just the base can be seen here) indicative of the family Trombiculidae, as opposed to members of the Leeuwenhoekiidae, which have two anterior median setae.

 

prob Oryctoxenus A

An Oryctoxenus sp. deutonymph (Glycyphagidae). Anterior is pointing up, and yes, it doesn’t have mouthparts.

 

prob Oryctoxenus B

Posterior hair-clasping structures of an Oryctoxenus deutonymph.

 

ixodid larva ex shrew A

A larval hard tick (Ixodidae).

 

ixodid larva ex shrew B

Retrorse spines on the tick’s hypostome help keep it attached to the host.

 

maybe Proctolaeleps A

Maybe a female Proctolaelaps sp.(Melicharidae). Not in great shape.

 

maybe Proctolaeleps B

The ‘procto’ part of Proctolaelaps refers to the large anal opening, or so the etymological legend goes.

*Smith, H.C. 1993. Alberta Mammals: an Atlas and Guide. The Provincial Museum of Alberta, Edmonton, Alberta.

 

 

A Less Notorious Bee Mite

The mite Varroa destructor has become famous in the wake of colony collapse disorder as a nasty parasite of the domestic honey bee Apis mellifera. But it is not the only bee-associated member of the family Varroidae, nor is A. mellifera the only host of varroids. Last week a former honours student of mine, Dr. Geoff Williams, sent me specimens of Euvarroa from a nest of the dwarf honey bee Apis florea Fabricius from just north of Chiang Mai in Thailand, where they had been collected by a local student, Patcharin Phokasem.

Like Varroa, Euvarroa are very large, heavily sclerotized mites. The ones that Geoff sent were 1 mm long: five Notoedres from a mangy squirrel skin could lie nose-to-tail on the venter of one Euvarroa.

Euvarroa with Notoedres

Euvarroa sinhai is a big mite, shown here with a 200 um long Notoedres for scale.

There are two named species in the genus Euvarroa, E. sinhai Delfinado & Baker and E. wongsirii Lekprayoon & Tangkanasing. Euvarroa sinhai is associated with Apis florea, whereas E. wongsirii is found on A. andreniformis Smith.  The species differ in general body shape (very triangular for E. wongsirii) and length:width ratio for the anal plate (longer than wide in E. sinhai, the opposite for E. wongsirii)*. Based on these host and morphological features, the mites from Geoff are E. sinhai.

I don’t think that much is known of the biology of either Euvarroa species, but they are very spiffy-looking mites. Here are some closer views of parts of their anatomy.

Euvarroa chelicera

The bee-piercing chelicerae of Euvarroa sinhai.

Euvarroa peritreme

Euvarroa sinhai‘s u-shaped peritreme; stigma to the upper left.

Euvarroa ambulacrum

“My, what big ambulacra you have!” “All the better for holding onto bees, my dear.”

*Lekprayoon, C. and P. Tangkanasing. 1991. Euvarroa wongsirii, a new species of bee mite from Thailand. International Journal of Acarology 17: 255–258.

Mystery of the Mangy-Squirrel Slurry

A few years ago I worked with members of the Vancouver Rat Project to investigate the cause of lumpy ears in rats from one of the shipping ports in that city. The rodents turned out to have ear mange caused by the sarcoptid mite Notoedris muris (Astigmata: Sarcopidae). As far as we could tell, this was the first record of N. muris in Canada. About two weeks ago, one of the co-authors of this paper, Jamie Rothenburger (now a Doctor of Veterinary Medicine doing her Ph.D. at the University of Guelph in Ontario), emailed to ask if I could look at a chunk of skin taken from a mangy squirrel. Jamie suspected Notoedres centrifera Jansen. This sarcoptid species has been reported to cause mange in many species of sciurids in North America and may be hindering recovery of the western gray squirrel.

image (1)

Diagnosis and drawings of Notoedres centrifera from Klompen (1992).

Jamie had only histological sections through mangy squirrel skin, though, which are difficult to match to species descriptions. I said sure and soon received a small frozen chunk of integument via courier. The skin sat in a saturated KOH solution for a couple of days to encourage its dissolution. The single mite I managed to find in the smelly skin slurry matched Klompen’s illustrations of N. centrifera (above), and was a similar size (200 um).

Notoedres prob centrifera Jansen ex squirrel skin ventral

Ventral view of the sarcoptid mite I found in the squirrel slurry.

Notoedres prob centrifera Jansen ex squirrel skin dorsal

Dorsal view of same.

So, diagnosis confirmed, end of story, right? Well, actually, the mite isn’t the reason for the ‘mystery’ in the title of this post. In addition to the one tiny Notoedres, I found several almost as miniscule (600 um), translucent cigar-shaped objects in the digested squirrel skin. Out of curiosity, I mounted three of them yesterday. [UPDATE: I revisited the slurry and found a fourth critter, images of which are at the bottom of the post]. Today I spent several hours futilely trying to pin them down to a taxon finer than ‘probably some sort of arthropod’. My first thought as I mounted them was follicle mites (Demodicidae) in cysts, but nope, not enough legs. There seem to be only two pairs! Plus they end in single large claws or clawlike tarsi, whereas follicle mites have two small claws per leg. Embryonic insects in eggshells? Still not enough legs, unless the first pair develop much more slowly than the last ones. Maybe…see third photo below. What insects might be on squirrels? The critters don’t look much like lice, because to my knowledge no lice have a big tuft of bum setae. And what are those weird flash-shaped setae at the head end? Are those round things spiracles? And why is there scalloped ornamentation on the bases of the four well-developed legs? None of the many entomology texts I consulted had images at all similar to these.

ex squirrel mystery embryo ventral

Ventral view of one of the four-legged embryos (?) from the squirrel skin. Note the long whippy bum setae (I assume that’s the bum end).

ex squirrel mystery embryo lateral

Lateral view of one of the other embryos.

ex squirrel mystery first legs maybe

It looks like there might be another pair of very poorly sclerotized anterior legs, with the faint leg tips clasping on of the more posterior legs.

ex squirrel mystery flask setae

Flask shaped setae on the head-ish end.

ex squirrel mystery ant spiracle maybe

Something that might be an anterior spiracle.

 

ex squirrel mystery post spiracles maybe

A row of abdominal spiracles?

ex squirrel mystery leg fans

There’s a fan-shaped structure at the base of each of the sclerotized legs (most clear on second leg from the right). They remind me of the ventromental plates of chironomid larvae.

ex squirrel trachea and split fan

I managed to mount one of the mystery critters with legs spread out and saw that the fan is actually split, like an open bivalve shell. Note also the trachea.

ex squirrel weird round things

At the anterior end of the thing are two sets of what look like trichobothrial bases, but there are no trichobothria or other setae coming out of them on any of the four critters that I mounted.

 

I am thoroughly stumped. Help!

Reference:

Klompen J.S.H. 1992. Phylogenetic Relationships in the Mite Family Sarcoptidae (Acari: Astigmata). Museum of Zoology. Ph.D. thesis, The University of Michigan, Ann Arbor, MI, USA.

Is That a Wombat on Your Belly, Or Are You Just Happy to See Me?

I attended a Ph.D. defense a few weeks ago on the effects of salmon lice (which are copepods, not insects) on their juvenile hosts. The student showed some gory photos and pointed out that for such a little fish, carrying a louse was like a human lugging around a raccoon on his back. Some mites can be just as burdensome, such as this Macrocheles muscaedomesticae (Scopoli) attached to the abdomen of an unfortunate Drosophila hydei Sturtevant.

Scanning electron micrograph of a Drosophila hydei carrying a female Macrocheles muscaedomesticae (image by HP)

Scanning electron micrograph of a Drosophila hydei carrying a female Macrocheles muscaedomesticae (image by HP)

Females of many species of Macrocheles (Mesostigmata: Macrochelidae) hitch rides on winged insects to move from a place to place, a phenomenon called phoresy. Strictly phoretic organisms do not feed on the host while attached. A great many mite taxa fall into this ‘purely phoretic’ category. Others may facultatively snack on the host while in transit. My colleague Lien Luong has investigated one such mite species, Macrocheles subbadius (Berlese), and its cactus-associated host Drosophila nigrospiracula Patterson & Wheeler. When Lien moved to the University of Alberta it proved difficult to replicate the system, in part because cacti are not common in this part of Alberta.  Compost bins are abundant, however, and Lien and her students are investigating the ecological relationship between two compost-associated species, Macrocheles muscaedomesticae and Drosophila hydei. Does M. muscaedomesticae feed on its host while attached, or is it just holding on? One way to test this is to determine whether the mite’s mouthparts pierce the fly’s integument. In this N = 1 sample, the mite just seems to be holding on firmly, probably uncomfortably so from the fly’s point of view.

mite biting medium close

Piercing or just pinching?

 

mite biting close

Looks like pinching, probably painfully.

But by definition, facultative parasites aren’t always parasitic. More mites must be examined, and other lines of evidence followed, such as presence of melanized wounds on hosts after the mites have dropped off, or presence of Drosophila DNA in the guts of the Macrocheles.

 

Brazilian Beauties

A couple of weeks ago my colleague Fabio Akashi Hernandes* from the Universidade Estadual Paulista sent me the file for a poster that I immediately printed on high-gloss paper and proudly affixed to the door of my office. The poster depicts some of the feather mites that Fabio has found on birds from Brazil and a few other tropical countries. Eye candy for acarologists! They are all scaled to the mm mark at bottom right, where you can see the gigantic Laminalloptes phaetontis (Fabricius) from tropicbirds. Among the selected mites are the hoatzin-dwelling Opisthocomacarus umbellifer (Trouessart) (mite #40) in which both sexes are adorned with feather-like setae of unknown function. Typically, though, male feather mites are more elaborate than females. The poster includes species whose males have vicious-looking hind legs (e.g., 1, 28), or are asymmetrical (e.g., 31, 32, 58), or are very well-endowed (20).

Fabio is doing some marvelous work on taxonomy and ecology of these mites, including the very recent discovery of a host-switch from wild cuckoos to domestic poultry. But even though he and his colleague Michel Valim have been working hard to describe new species, at least 80% of bird species in Brazil have yet to be investigated for their acarofauna. Many more wonders await.

Click on the poster image then mouse over and click to magnify.

Fabio's Feather mite poster 6 Oct 2015 sml

*abakashi@gmail.com

Smaller fleas

In his very long poem on the nature of poets, Jonathan Swift famously noted that parasites can themselves be parasitzed. A few weeks ago I came across an interesting case of hyperparasitism. I had washed a recently road-killed Yellow-bellied Sapsucker. It yielded many lovely mites and one feather louse. I slide-mounted the latter and representatives of the former.

Pteronyssus sphyrapicinus male and female ex YPSS HP0929 sml

Pteronyssus sphyrapicinus (Astigmata: Pteronyssidae) feather mites from a Yellow-bellied Sapsucker. Male on left, female on right.

When I looked at the louse under the compound scope I thought its Malpighian tubules had burst out of its abdomen. At higher magnification, the tubules turned out to be hyphae.

Penenirmus auritus with arrows

Fungally infected Penenirmus auritus (Phthiraptera: Philopteridae) from a Yellow-bellied Sapsucker.

I figured it must be a member of the Laboulbeniales, fascinating and highly modified ascomycotan fungi: look here and here! Almost all of the 2000 or so described species are ectoparasites – or perhaps in some cases harmless commensals – of living arthropods. One species has achieved recent notoriety due to its spreading from a native ladybird in the U.K. to an invasive one. I had seen them on various critters before, including beetles and mites, though never on a feather louse. But Googling revealed that in 1951, Wolfdietrich Eichler had published an interesting overview of the Laboulbeniales he’d seen on lice from birds*.Eichler figure

They were all from the genus Trenomyces. I asked my mycologist friend Randy Currah if he could tell whether the fungus on my louse was one that Eichler had identified. He referred me to Meredith Blackwell at Louisiana State University. She identified the images as a Trenomyces sp. (like Eickler’s) and then sent the images I emailed to her to Danny Haelewaters at Harvard University. I’m not sure whether Danny will be able to get it to species based on my bad photos, but if he does I will update. UPDATE (22 Aug 2015) – Danny has just identified the fungus as Trenomyces circinans Thaxter, a new record for Canada. Thanks, Danny!

Penenirmus auritus from YBSS trimmed

Closer view of the Trenomyces showing a big ascocarp, two ascospores (lower right) and juvenile multiseptate things that probably have proper names but I will just call ‘babies’.

*Eichler, W. 1951. Laboulbeniales bei Mallophagen und Läusen. Feddes Repertorium. 54(53):185-206.

What happens when you ask an undergrad to draw a spider?*

This summer the arthropodologists in my department are being moved from one building to another, as part of the mysterious game of reshuffling that university administrators so enjoy. As preparation for the move, I’m downsizing the contents of my filing cabinets. In a folder from 2004 I found this collection of drawings from the first time I taught Biology 108, Introduction to Biological Diversity. I had given two lectures on arthropods with a strong emphasis on differences in appendages and tagmata among the major groups. This is what I thought was an easy bonus question on the final exam: draw a spider and label the relevant parts. Here is a selection of drawings, from ‘quite respectable’ to ‘huh?’.

spider01spider02

spider04spider03spider071spider05spider06spider07spider08spider09

Based on the last image, some university students believe that spiders should be speared on toothpicks and served in martinis.

*apologies to Facebook friends who’ve already seen a version of this.

On the backs of wasps

In March, I was given two specimens of solitary wasps that were covered with mites. The first was one of several Crossocerus  (Crabronidae) that had overwintered in holes in a wooden chair left outside on the campus of the University of Alberta. I had expected the mites to be phoretic deutonymphal astigmatans, but they weren’t, they were adult female scutacarids (Prostigmata: Scutacaridae). Many scutacarid species have phoretic and non-phoretic morphs. The big anterior tarsal claws you can see (blurrily) on the photo below are typical for phoretomorphs. What wasn’t typical was a pair of strange internal structures that became apparent in well-cleared specimens.

scutacarid from Crossocerus April 2015 E

At first I thought the pair of round things near the female’s genital area were sperm-storage chambers. But when I Googled ‘Crossocerus’ and ‘Scutacaridae’, I found a paper that showed I was only half right – they were sporothecae*, not spermathecae!

scutacarid from Crossocerus April 2015 C

Two big spores tucked into the genital atrium of this female Imparipes.

scutacarid from Crossocerus April 2015 A

Ebermann & Hall (2004) described a new species of scutacarid, Imparipes haeseleri, from several species of wood-associated Hymenoptera. In the genital atrium of these mites, they observed two large round fungal spores, one on each side, looking remarkably similar to the ones in the mites from the rotting chair. I asked Evert Lindquist, an expert on the Heterostigmata (the larger group to which Scutacaridae belongs) if these mites were Imparipes. Yup, they were. Were they I. haeseleri? There is a closely related species known from North America, I. vulgaris, but several setal characters matched haeseleri rather than vulgaris so I decided to go with Imparipes cf. haeseleri.

Why are the female mites carrying spores? No doubt they and their offspring feed on the wood-digesting mycelium produced from the germinated spores. The mites that hop on wasps as they depart from their overwintering chambers take with them the starter culture for their future meals. Dr. Lindquist noted that the spores these mites were carrying looked very similar to the Nigrospora spores known to be carried by a different species of heterostigmatan, Siteroptes reniformis Krantz. In his 1984 paper, Lindquist notes that S. reniformis “not only serve to transport and place spores of Nigrospora in an environment favorable for germination and growth, they also stimulate mycelial growth, apparently by secreting a chemical substance when feeding on the fungus.”

The second wasp was collected from an overwintered artificial nesting block that was supposed to house solitary bees. It was an Ancistrocerus sp. (Vespidae: Eumeninae). Knowing this, it was easy to guess who the mites were, and slide-mounting confirmed it: deutonymphs of a Kennethiella sp. (Astigmata: Winterschmidtiidae).

Winterschmidtiid_001

Like almost all phoretic deutonymphs of Astigmata, these Kennethiella have a terminal sucker plate to adhere to hosts. Unusually, they also have anterior ocelli. Why ocelli are present in only a small number of Astigmata is unclear (at least, it’s unclear to me).

Winterschmidtiid_003

Sucker plate.

Winterschmidtiid ocelli

Pair of ocelli.

The reason I expected the mites to be Kennethiella is because the relationship between them and their host wasps is famous among acarologists. Cowan (1984) unraveled the interactions for one mite-wasp duo.  To quote the abstract: “The mite Kennethiella trisetosa is phoretic on adults of the wasp Ancistrocerus antilope and develops in the nest with immature wasps. Female mites and a large type of male develop oviparously, whereas a small male develops oviparously. Small males kill each other, but are ignored by large males. By mating with females before small males are mature, large males may monopolize fertilization. Larvae of female wasps usually destroy mites within their cells but, as adults, are reinfested when mated by mite-bearing males. Each time a male wasp mates, about half of its mites transfer to the female.”

It’s worth reading the original to appreciate the full intricacies of these intertwined life-cycles.

Ancistrocerus showing Kennethiella mites 16 Aug 2009

A home-grown Ancistrocerus with a load of Kennethiella, from my back yard in Edmonton a few years ago.

*according to Evert Lindquist, they aren’t sporothecae (which are spore-storage sacs) but simply the spores themselves, tucked into corners of the genital atrium. Thanks, Evert!

Painless mites

My freezers at work are getting rather full, so I’ve been washing birds and sending the clean bodies to the Royal Alberta Museum. Last week I washed a batch of white-throated sparrows (Zonotrichia albicollis) that had met a sad communal death by flying into a window in Edmonton. They were very mite-rich, providing dozens of specimens of Proctophyllodes (Proctophyllodidae), Mesalgoides (Psoroptoididae), and Analges (Analgidae).  All of these taxa belong to the feather mite superfamily Analgoidea. Analges means “without pain”, and the genus was called thusly by Nitzsch in 1818 because it seemed that even heavily laden birds showed no signs of distress. Almost two hundred years later, a huge comparative study by Ismael Galván and colleagues in 2012 compared feather mite load and host condition of 83 species of birds and found no evidence of a negative relationship. Feather mites in general appear to be harmless commensals of their hosts.

Analges species are interesting because of their striking male polymorphism. All males differ from females in having enlarged third legs with spear-like tarsal claws, but legs of some individuals are much more grotesquely hypertrophied than others. Such males are also larger overall.

White-throated Sparrow Analges compilation lightened

Analges sp. mites from white-throated sparrows from Edmonton, Alberta. From left to right: female, homeomorphic male, heteromorphic male (all to the same scale).

Male polymorphism is very common in feather mites and many other Astigmata. The less elaborated male forms are typically called ‘homeomorphs’ and the extravagant ones ‘heteromorphs’ (the reason for the terms being that the former are more similar to females than the latter).

But what are the modified third legs used for? Holding females? Stabbing rival males? I’m not sure that anyone knows.

White-throated Sparrow Analges male legs

Legs of homeomorphic (left) and heteromorphic (right) male Analges. The pointy tarsal claws look nasty.