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In a Desert, Manners Maketh Mites: A New and Unusual Type of Microbivory

By Samuel Bolton

For any small arthropod, the topsoil and litter layers are a veritable jungle — a morass of predators, pathogens, and meals. There are two basic strategies for surviving in organically rich soils: either live fast and die young, or find a way of protecting yourself from predators. Both of these strategies work because there are plentiful food resources that allow one to either grow up quickly or go to the trouble of metabolizing a suit of armor, for instance. High degrees of sclerotization are indeed common in these organically rich habitats. A handful of topsoil from any forest contains numerous well-armored oribatids, the arachnological versions of tanks.

Samuel Bolton

If topsoil is a jungle, then deep mineral soil and sand are the desert equivalents. Food is scarce in these habitats, but then so are predators. If one can somehow adapt to these conditions, it’s a great opportunity to let one’s guard down. There is less need to invest in armor in an environment where so few predators abound. In this respect, the family of mites that I study, the Nematalycidae, represents an extreme example of this mode of living. These mites are noticeable for their highly elongate body form and for their thin and extendable integument, which must make them an exceptionally easy meal for any comparably sized predator. Their long bodies make it is easy to outflank them, whereas their soft, thin integuments can be readily penetrated by pincers or a pair of mandibles. As one would expect, these mites don’t do well in organically rich soils. They are almost exclusively found in deep mineral soil and sand. But how do nematalycids survive in an environment that has so little food? This is a topic that fascinates me, so much so that it is now a central part of my PhD research.

Nematalycidae. (a) Gordialycus from the Algodones dunes, California. (b) Osperalycus tenerphagus.

Like the majority of other mites, the Nematalycidae are fluid feeders. Many fluid-feeding mites simply insert their mouthparts into their prey items and draw up the fluid contents using the suction from their pharynx. This is easy enough when you have a large enough prey item into which to sink your mouthparts. However, in a desert-like environment such as deep soil or sand, prey items aren’t often in the big-and-easy size category. Instead, much of the biomass of these habitats is composed of bacteria and yeasts, which are far smaller than any mite. It would seem very difficult, if not impossible, for a mite to accurately insert pincer-like chelicerae — the usual cheliceral form among mites — into something as small as a bacterium or a yeast cell. Then there is the challenge of how to channel the fluid contents into the digestive system. Following the rupture of any microorganism, much of the small amount of fluid that leaks out will stick to inconvenient surfaces. And any waste in a desert-like environment has potentially fatal consequences.

My collaborators — Gary Bauchan, Ronald Ochoa, and Hans Klompen — and I recently described a new species and genus of mite that appears to have come up with an ingenious solution to this problem. When we examined this mite using low-temperature scanning electron microscopy (LT-SEM), we discovered that it has a tiny pouch into which its chelicerae slot. It wasn’t immediately obvious why their mouthparts should include a pouch. But one possible explanation is that the structure might serve as a type of holder for microbes. If the mite could somehow place a microorganism inside the pouch, which is about the right size to contain a yeast or bacterium, the chelicerae could then slot into the pouch so that the microorganism would break up, allowing the fluid contents to be drawn up underneath the labrum and into the mouth. In this way these mites could be sure to ingest all of the fluid contents of a microorganism after they have ruptured it. Carefully extracting all of the fluid of each individual microorganism could seem overly fastidious in an environment that is rich in food resources. But it should be a very useful modification where food is scarce.

The pouch of Osperalycus tenerphagus, dorsal views. (a) Chelicerae inserted into pouch. (b) Chelicerae withdrawn from pouch.

In order to feed on microorganisms, these mites would need a way of delicately picking them up and placing them inside their pouches. Our LT-SEM images revealed that each palp has a specially modified seta or hair with a tip shaped into a shallow cup.

Modified palp seta of Osperalycus tenerphagus. Short arrow pointing at shallow cup.

This would appear to be a good structure for picking up microorganisms using intermolecular adhesive forces such as van der Waals or capillarity. As the seta is being pushed forwards into a microorganism, the thin stem of the seta would provide the flexibility needed for the cup to press up flatly against the surface of the microorganism (Fig. B below). The concave surface of the cup would allow a large enough contact area to pick up a microorganism. And rather than penetrate the microorganism, the seta will bend when the palp overreaches (Fig. C below), therefore preventing the rupture of the microorganism before it is in the pouch.

The delicate collecting mechanism. (a) The cup of the seta is not yet correctly orientated to the microorganism. (b) Flexing of the neck of the seta, as the seta is pushed into the microorganism, causes the cup to align squarely. (c) Overreaching does not damage the microorganism—the seta flexes some more.

Despite several attempts, it was too difficult to directly observe these mites feeding on microorganisms. Their mouthparts are exceptionally minute, and for that reason their feeding action cannot be readily investigated with a light microscope. So instead I examined the other nematalycids more closely. This revealed a trend in the association of different feeding structures. With the exception of a single genus, none of the other genera possess specially modified palp setae. These same genera also do not have mouthparts with a pouch. This is obviously consistent with the idea that the modified palp setae of Osperalycus are indeed for picking up microorganisms for placing into the pouch. But the problem genus was Gordialycus, an extremely elongated nematalycid. Light microscopy revealed that each palp of this mite also has a seta with a cup-shaped tip. However, in order to find out if a pouch was also present, I needed specimens for LT-SEM. This is because the pouch of Osperalycus is invisible under all types of light microscopy, even confocal microscopy, so there is no good reason to think that this should be different for other nematalycids. As I only had slide-mounted specimens of Gordialycus, I had to wait until I could find fresh specimens before I could address this question. Furthermore, I needed quite a large number of Gordialycus specimens because it is unlikely that these mites can be mounted in the correct orientation on the first few attempts. Very often, the front legs and palps will obscure the view of the mouthparts under LT-SEM.

And so began my search for Gordialycus. This mite is much more commonly found in sand dunes than in any other type of habitat. Therefore, during a field trip to California in October 2013, I seized upon the opportunity to sample in the Algodones Dunes. This large field of dunes, 45 miles long by 6 miles wide, stretches from the vicinity of a large inland salt lake, Salton Sea, to the border of Mexico. The relatively close proximity to Hollywood has made these dunes a popular filming location for dramatic desert settings, and they make up the scenery of a number of feature films, including Return of the Jedi and Flight of the Phoenix.

Located right in the middle of the dunes is the Hugh T. Osborne Lookout Park, which is accessible by road. It was there that I parked my car before I walked out onto the open dunes. I collected close to four gallons of sand from one spot at the base of a big dune. Such large samples are needed to help ensure that if Gordialycus is present at all, I would have enough specimens for LT-SEM. Smaller samples of around a gallon or so often don’t produce many specimens. I had not found Gordialycus very often in the past, but wherever I did collect it, it was consistently present in very low numbers.

I only collected from that one spot in the middle of the dunes — my car was already nearly full of samples from other sites in the California desert. I freely admit I was hoping for some luck, and I have no idea how representative that single sample is of the whole of the dunes. My journey back to the car was an interesting one; the profusion of recreational dune buggies made the scene more reminiscent of Mad Max than Return of the Jedi or Flight of the Phoenix.

When I got back to my lab at the University of California, Riverside, where I was based for the duration of my California trip, I used a flotation technique to extract the micro-arthropods from the Algodones Dunes sample. I was surprised and jubilant to find nematalycids in abundance. They all belonged to Gordialycus. Besides Gordialycus, there was only one other species of mite, and in extremely low numbers — a predatory mite (Arhagidia) that possibly feeds on Gordialycus. This dry-adapted mite is probably one of the few types of predatory mites that can survive in the inhospitable habitat it shares with Gordialycus. But whereas there were only a few of these predatory mites, there were around five hundred specimens of Gordialycus. My sample had more than sufficient numbers to guarantee success with LT-SEM.

A few weeks later I was at the Beltsville Agricultural Research Center (BARC), in Maryland, where I finally got the chance to observe the mouthparts of Gordialycus using LT-SEM. The anticipation was almost unbearable. Would these mouthparts reveal a pouch? Ronald Ochoa was on hand to maneuver the front legs of these mites so that they do not get in the way of our views of the mouthparts. His skill in maneuvering and repositioning mites for LT-SEM mounting is legendary within the field, and it was not long before we had a number of SEM stubs, each with numerous Gordialycus mites mounted in various positions. With Gary Bauchan at the helm of the LT-SEM, it was then a matter of shooting the many images we needed in order to determine the morphology of the mouthparts. By this point, my technical work was largely done. I simply pointed at what I wanted to see up close while Gary skillfully and patiently got his electron microscope to perform the miracles that I demanded of it.

It turns out that Gordialycus does not have a pouch. But the mouthparts of this mite revealed something that was no less interesting. In Osperalycus, a pair of hard and sclerotized structures, known as rutella, are pressed up against the outside of the pouch. In most mites with rutella, the rutella project out in front of the mite, but in Osperalycus they function as a type of scaffold, holding the pouch in place while the chelicerae are presumably used to break up the contents of the pouch. In both Gordialycus and Osperalycus, the rutella converge and meet. But in Gordialycus, instead of a pouch, the rutella have expanded to form a large barrier at the front of the mouthparts. Although the rutella are very distinct from those of Osperalycus, this mite would still need a way to pick up an individual microorganism in order to place it behind the rutella barrier, hence the presence of a seta with a cup-shaped tip on each palp. Therefore, the basic feeding mechanism appears to be broadly the same as the one that we found on Osperalycus. Perhaps the only major difference is that in Gordialycus, the role of the pouch as a food holder would be fulfilled by the rutella, so there is no need for a pouch.

Mouthparts of Gordialycus (species from the Algodones dunes), anterior view.

Initially, the mouthparts of Gordialycus did not make a lot of sense to me. It seemed strange that the rutella project out from the base and then converge at their tips. This meant there was an inexplicable gap between each rutellum and a central projection of the mouthparts. But this mystery was cleared up by the following image, which was one of the last that we took of Gordialycus.

Mouthparts of Gordialycus (species from the Algodones dunes). (a) Ventral view of the mouthparts: chelicera retracted (nowhere in sight). (b) Anteroventral view of mouthparts: movable digits of chelicerae slotted into the gaps between the central projection and the rutella. (c) Lateral view of chelicera.

In this and the other mouthpart images of Gordialycus, the chelicerae are retracted. But image B above shows that the movable digits (the ventral biting parts of the chelicerae) are tucked behind the rutella, revealing that the gap forms a tight slot for a movable digit. The gap therefore enables the chelicera to neatly interlock with another part of the mouthparts. Any microorganism that has been inserted into this gap would be crushed or sliced up when the movable digit rotates and slots into the gap. The microorganism would not slip away because it is held within the rutella barrier. This is not very different from how the cusps of our molar teeth work when we chew. By neatly interlocking, a single pair of opposing molars can completely crush anything that is in between them. Like mammals, Gordialycus has two sets of hard, interlocking structures next to the entrance of its digestive system; its rutella and cheliceral digits are substitutes for mandibular and maxillary molars.

This latest finding suggests that there are variants of the same feeding mechanism. Another species of Gordialycus, which I collected from Indiana, has distinct rutella from the species I found in the Algodones Dunes. This appears to represent yet another modification of the feeding mechanism.

It is curious that desert living has led to such an unusual way of feeding. These mites seem to have solved the problem of wasteful eating by evolving a form of cutlery for delicately picking up microorganisms and placing them into a feeding holder. Who would have guessed that there are well-mannered mites?

More information is available from our main article, which was recently published online in Arthropod Structure & Development.

Samuel Bolton is currently a PhD student at the Acarology Lab at Ohio State University. His research is largely based on the evolution and systematics of the Endeostigmata (including the Nematalycidae) — an extremely ancient and basal group of mites that dates back to the Devonian.

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