parasites

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.

 

 

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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.

 

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.

Two Bad Mites

This August I met two of the most important mite pests in North America. The two-spotted spider mite, Tetranychus urticae Koch (Prostigmata: Tetranychidae) is particularly devastating in greenhouses. That’s where I encountered it – slaughtering my dill. The common name ‘spider mite’ refers to the vast quantities of webbing they produce.

spider mite webbing on dill from greenhouse Aug 2014

Tetranychus urticae and its webbing on my unfortunate dill plants.

spider mites on dill from greenhouse Aug 2014

Closer view of webbing, showing the mites themselves.

This spider mite has a huge host range, having been recorded from more than 1000 plant species. It feeds by piercing host tissues with its fine stylet-like mouthparts.

Tetranychus urticae from dill 22 Aug 2014 body

Tetranychus urticae from dill 22 Aug 2014 stylets

Tetranychus urticae female: above, whole body; below, gnathosoma showing stylet-like chelicerae.

The name ‘Tetranychus‘ means ‘four claws’ and presumably refers to the four nail shaped setae (tenent hairs) on the tarsi. Why ‘urticae‘? Because they are irritating, like nettles (Urtica spp.)? Or maybe they were first identified from urticaceous hosts?

Tetranychus urticae from dill 22 Aug 2014 tenent

Four nail-like tenent hairs can be seen at the tip of this mite’s tarsus.

Tetranychus urticae has made the big journals lately for having the smallest known genome of any arthropod, and for having likely picked up genes for producing carotenoid pigments by horizontal transfer from fungi. Until recently, it was thought that all animals acquired carotenoids from plants, bacteria or fungi in their diets rather than creating the pigments through their own metabolism. But pea aphids and T. urticae are able to make carotenoids themselves, thanks to these horizontally transferred genes.

The other bad mite I met in August has a much narrower host range – bees of the genus Apis, including the domesticated honeybee Apis mellifera Linnaeus.  This mite is the infamous Varroa destructor Anderson & Trueman (Mesostigmata: Varroidae). These parasites are huge relative to their hosts, being about the size of the bee’s eye. They feed on host haemolymph, thereby weakening the bee, and can transmit crippling viruses. Although I don’t have honeybee hives in my backyard, one of my previous graduate students is a member of YEG Bees and was taking part in the first trial of urban bee-keeping in Edmonton. He invited me to one of their hive checks. Part of the check involved looking at the sticky boards under the hives for Varroa that had been knocked off the bees. Sure enough, they were there. I collected a couple and managed to get an ok photograph of one of the vaseline-covered mites.

Varroa from Beeyonce's hive with pen for scale Aug 2014

A Varroa destructor from Beeyonce’s hive. The queen of the other hive I visited was named Justin Beeber. Beeber’s hive failed – prophetic?

Varroa from Beeyonce's hive A

A V. destructor, after having had vaseline removed via a fine probe and Photoshop.

Varroa can be treated with chemicals or through careful selection of mite-free brood starters. But it is getting harder to find the latter, as V. destructor is found in almost every Apis mellifera-producing country except Australia.  Researchers and apiarists are also trying to breed a more Varroa-resistant honeybee by selecting for intense grooming behaviour.

On the one hand, these two species tarnish the image of other mites through their economic nastiness. But on the other, their bad behaviour helps to pay the salaries of many acarologists.