Ever heard of
rat kings (Rattenkönig)? It is a real, rare, and disturbing occurrence.
A rat king is a collection of rats whose tails are intertwined and bound together by one of several possible mechanisms, such as entangling material like hair or sticky substances like sap or gum or getting tied together. Historically, this alleged phenomenon is particularly associated with Germany. There are several specimens preserved in museums but very few instances of rat kings have been observed in modern times.
Such "rosette" ("little rose") shapes of rats are called "rat kings", because the king of rats would sit on top of the knot in the center, being carried around on its throne like a king.
This phenomenon has been reported extensively, so I will not do it. Read
this article if you are interested.
However, completely overlooked is another case of the "rat king" in parasites. If rats tying their tail ends into knots is scary, just imagine how terrifying it is to see parasite larvae doing the same!
And that's exactly what
zygocercous (zygo-: yoke; cercous: about the
cercaria. The "zygo-" in "zygote" comes from the fact that a zygote is formed by "yoking together" a sperm and an egg.) parasites do. Sadly, such parasites are so extremely obscure, that I literally have read all the literature on this I can find online. ALL OF THEM. The keywords I used are: "zygocercous" "macrocercous" "rat king parasite", "rattenkonigcercaria".
Here is a collection of all useful information about the zygocercous parasites I found.
The records
The first published observation of rat king cercariae was in 1880 by
Carl Claus. I can't actually find the original quote, but the next paper refers to it.
The paper is very pleasant to read, almost like a kind mom talking to me about various things of nature. It describes "cercaria Clausii Monticelli", a rat king cercaria named after two discovers,
Carl Claus and
Francesco Saverio Monticelli
It was in the late autumn of 1889 when two glasses of sea water [thought to contain mollusc embryos] arrived in Vienna for Mr. Hofrath Claus... of the Berlin aquarium... Hofrath Claus handed me the glasses, and I recognized with my near-sighted eye... that those not mollusc embryos. Many small, lively, fidgety balls of disheveled appearance floated in the water in irregular paths, which, almost reminiscent of the movement of young chironomus or other fly larvae, leaving the impression that the animals were not moving for a specific goal, but only to remain floating, to move upwards or downwards, here or there. But I couldn't even guess what I had in front of me, no matter how familiar I am with the wonderful shape of the pelagic buoyancy. That exciting expectation of discovering an unknown animal form in a glass of rich plankton, at least to my taste, makes it one of the most attractive zoological pursuits...
... I was surprised by the most wonderful picture when I looked into the microscope. Tubes radiated from a center, sometimes contracting strongly in the longitudinal direction, sometimes long, almost thread-like expanding, sometimes fidgeting and trembling, sometimes violently lashing up and down and tugging like the rest of the crowd. Now the thing spread out in the manner of a carchesium colony, now again it curled up into a small, thick lump, all the more indissoluble for the eye when the hoses were densely surrounded by long, fine, but stiff, vertically protruding, bristle-like hair, who carried small, extremely strongly refracting secret droplets everywhere. It was only when the animals became calmer under the pressure of the coverslip, and then gradually died away, that the distal end of the individual tubes became recognizable, and it was immediately clear, of course, that there was a heap of cercariae, which, in their most strange way, were entangled in the tails.
Carchesium colonies are harmless little "drinking cups" that do bear a resemblance to the rat king cercariae! While carchesium colonies are harmless, the rat king cercariae are absolutely vicious...
I soon remembered that this phenomenon had already been mentioned in the literature by Claus, who said in the 4th edition of his "Principles of Zoology" (Marburg 1880), I, p. 398: "Finally To emphasize the occurrence of marine cercariae of the genus Distomum (according to my own, yet unpublished, observations from the aquarium in Naples), which, comparable to a rat king, are interconnected at the button-shaped end of their powerfully developed, spirilla-like movable tails and vibrate like spherical lumps..."
The cercariae colonies never separate voluntarily. I saw, however, that the knot, which was loose, but still held together by the length of the intertwined parts, loosened and individual animals were released unharmed; but this only happened under the pressure of the cover slip. This never happened in the colonies floating freely in the glass... after 15 hours they fall to the ground, tired, and they would perish if the intermediate host is not found within this time...
A delicate page of figures is attached to the end of the paper.
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| Figure 1 |
Fig. 1. Colony of cercariae of Clausi Monticelli, drawn at approximately 75 times linear magnification. (Large Reichert tripod, opened tube, approx. 38 cm. Distance of the Oberil aser prism from the drawing surface. Objective 1 A.) A distinction is made between the yellow and the black pigmented individuals. Prepared in Canada balm.
Dronen, N. O. (1973). Studies on the Macrocercous Cercariae of the Douglas Lake, Michigan Area. Transactions of the American Microscopical Society, 92(4), 641. doi:10.2307/3225274.
This paper describes three almost identical species of "macrocercous cercariae", meaning parasite cercariae that have big fat tails.
Normally, rediae contained 15-25 cercariae in varying stages of development.
This can be seen in the following picture, where a redia contains a dozen bean-shaped baby cercariae.
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| Figure 9. Drawing of a mature daughter redia of C. macrocauda typical of the three macrocercous cercariae studied. |
Most infections were heavy, and as much as 80% of the visceral mass of the snail was parasite.
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| Figure 2: Composite drawing of a solitary C. gorgonocephala. |
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| Figure 3: Composite drawing of a cercarial mass of C. gorgonocephala. |
Cercaria gorgonocephala (Figs. 2, 3). Distome morphologically identical to Cercaria macrocauda (Fig. 5); tail divided into two main parts, the main-tail and rat-tail regions; cercariae shed in masses composed of 32-40 cercariae knotted together at thin region, connecting main-tail and rat-tail regions (Fig. 3); rat-tail regions trail to one side of mass on occasion providing bouyancy by trapping gas bubbles, like fingers around a ball; cercarial pigmentation light green or white to dark brown. The cercarial mass is photopositive and moves by a thrashing movement of the many cercariae. This action makes these cercariae more attractive to minnows as "bait" than Cercaria macrocauda. Cercarial masses usually emerge in the early evening. Normally four to six masses are shed every third day but occasionally a single cercaria can be found (Fig. 2).
The name "gorgonocephala" means "head of Gorgon". The Gorgons are the three Greek mythological monsters, one of which is
Medusa.
, HB Ward - The Journal of Parasitology, 1916
Under a dissecting microscope the object resembled a writhing mass of serpents tied together by the tails... The bunch contained not less than 50 separate stalks fastened firmly together at the base, all in active motion with a spiral twist passing in wave-like progression from the base to the outer end of the stalk (Fig. 5).
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| Figure 5 |
The base of each stalk carried a bulbous expansion which in some stages of contraction appeared to be sharply cut off from the rest of the stalk but at other times graded into the stalk without any distinct boundary. This basal enlargement was thicker walled than the stalk elsewhere and possessed yellow pigment granules that were not found in other parts. The stalk was very mobile, delicate in texture and provided with two irregular longitudinal stripes of granular brown pigment which terminated just short of the outer tip. This stalk which is the region of marked contractile activity, tapered slightly (Fig. 4) to the extreme outer tip where it bore the body of a young trematode that appeared to be an amphistome. About half of the stalks had already lost their attachments; most of these still twisted and vibrated nearly as actively as those that carried the young helminths; but a few were pale in color, appeared empty like dead algal filaments, and were motionless. At times all the stalks rested quietly for a brief period and then suddenly began to be violently agitated together. During this movement it was clear that the stalk alone was active whereas the worm was snapped too and fro like the lash of a whip.
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| Figure 3. Cercaria gorgoncephala rat king |
As the stalk vibrated with a coiling or twisting motion, the worm at the end was turned at every angle and it seemed as if the large posterior sucker was mounted on a stalk or at least protruded distinctly beyond the general surface of the body. The general form of the amphistome was oval with a concave ventral surface and the anterior end rolled slightly ventrad (Fig. 6) so that the oral sucker was partly concealed. The body of the worm was white, opaque and almost entirely immobile. No internal organs could be detected either in the attached worms or in those that had been shaken off and lay free in the dish. The posterior end of the detached amphistome bore a distinct projection which indicated the point at which the stalk had been attached.
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| Figure 1, 2: an individual cercaria that has detached its tail. |
A somewhat similar form was discovered by Claus in the Mediterranean in 1880 and recorded by Leuckart (1886: 87). It is referred to in various other places as a Rattenkönigcercaria. It was carefully described by Pintner (1891) under the name of Cercaria clausii given it by Monticelli in 1888. Odhner has more recently (1911) shown this to be the larval form of Phyllodistoinum acceptum Looss. Apart from the peculiar habit that both forms are borne on stalks tied in bunches there is no close similarity between Cercaria clausii and C. gorgonocephala. The details of structure in the stalk are as unlike as the structure of the two worms.
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| The whole plate in one picture. |
GOODCHILD, C. G. (1943).
THE LIFE-HISTORY OF PHYLLODISTOMUM SOLIDUM RANKIN, 1937, WITH OBSERVATIONS ON THE MORPHOLOGY, DEVELOPMENT AND TAXONOMY OF THE GORGODERINAE (TREMATODA). The Biological Bulletin, 84(1), 59–86. doi:10.2307/1538050
Odhner (1911) believed that the marine "Rattenkonigcercaria" Cercaria clausii when eaten by the fish Chrysophrys aurata develops into Phyllodistomum acceptum.
Martin, W. E., & Gregory, V. L. (1951).
Cercaria buchanani n.sp., an Aggregating Marine Trematode. Transactions of the American Microscopical Society, 70(4), 359.
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| Figure 7. Cercaria buchanani. Typical cluster of cercarie formed after emergence from snail host. |
Cercaria laramiensis sp. n., a Freshwater Zygocercous Cercaria from Physa gyrina Say, with a Discussion of Cercarial Aggregation, Gary L. Hendrickson and Newton Kingston, The Journal of Parasitology, Vol. 60, No. 5 (Oct., 1974), pp. 777-781
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Figures 1, 2. Cercaria laramiensis sp. n.
1. Aggregate with 3 distinct centers.
2. Solitary cercaria |
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| C. laramiensis. Figure 3. Simple colony with one center |
Description of a new zygocercous cercaria (Opisthorchioidea: Heterophyidae) from prosobranch gastropods collected at Heron Island (Great Barrier Reef, Australia) and a review of zygocercariae (1994).
This paper reviews the characteristics of 11 known Rattenkönigcercariae, which occur across five trematode superfamilies. It also describes a certain species of zygocercous cercaria with bright orange body and black tails.
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| Figure 6: Cercaria, entire, showing the pigmentation of the tail, lateral view. Scale-bar: 0.1 mm. |
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| Figure 10. Cercariae clustered toward the tail-end of the aggregate. Scale-bar: 0.1 mm. |
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| Figure 11. Entire aggregate showing a few turns of the spiral near the left. Scale-bar: 0.5 mm. |
Individually emerged cercariae are unable to progress (poor swimmers). However, when cercariae are aggregated or even paired, swimming becomes very efficient... The narrow amplitude of cercarial swimming movements allows dense aggregation (700 individuals in 2.5 mm$^3$).
It is difficult to imagine which organ or which part of the fish is able to withstand simultaneous penetration by several hundred cercariae, especially if cercariae migrate deep in the body. Aggregates are, therefore, probably not swallowed whole but more likely taken into the mouth and then expelled as unpalatable. Bodies may easily decaudate and perhaps quickly attach by the ventral elliptical pad, peculiar to this zygocercaria, in the buccal cavity before the cluster is rejected. Cercariae may then penetrate the buccal lining.
Imagine, then a bunch of broccolis floating in water. A fish takes a bite, then the tiny heads of the broccoli snaps free from their stems, bite onto the mouth skin and starts digging in.
Adhesive secretions in the Platyhelminthes, ID Whittington, BW Cribb - Advances in parasitology, 2001
Zygocercous cercariae aggregate in large numbers, connect together and move as one organism. Beuret and Pearson (1994) described this process for cercariae from Clypeomorus batillariaeformis, an intertidal gastropod from the Great Barrier Reef. These cercariae form large aggregates of up to 700 individuals and it was suggested that these zygocercariae first attach by the prehensile portion of their tail and that adhesion of the posterior half of the inflated part of the tail then occurs (Beuret and Pearson, 1994). These authors suggested that adhesive properties in zygocercariae may be widespread. Aggregation like this is believed to be a strategy to attract consumption by the next host in the life cycle. Perhaps the shape of the cercarial cluster mimics a free-swimming organism normally ingested by the definitive host (Combes, 1980).
Parasites and the behavior of animals, J Moore, 2002.
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| Figure 2.15. The legendary antecedent of the Rattenkonigcercariae. (Drawing by Conery Calhoon; inset photo of a real Rattenkonigcercariae courtesy of Gary Hendrickson.) |
Page 29--32:
Rattenkönigcercariae, or rat king cercariae, are cercarial aggregations that occur in some species; this is a large, noticeable mass that can be mistaken for a food item (fig. 2.14). The cercariae that engage in this behavior move slowly when solitary and may be poorly adapted to active host seeking (Hendrickson and Kingston 1974). Beuret and Pearson (1994) summarized the characteristics of 11 known Rattenkönigcercariae, which occur across five trematode superfamilies. Depending on the species, the aggregations may contain anywhere from a few to hundreds of individual cercariae. Beuret and Pearson described the most organized rat king to date from an intertidal snail (Clypeomorus batillariaeformis) on Heron Island (Great Barrier Reef). (The adult form was unknown to them, so they resisted the impulse to describe a new species.) The cercariae emerge from the mollusc's ctenidia into the mantle cavity, where they assemble and then leave through the exhalant siphon. This assembly is no mean trick: each cercaria is oriented in the same direction, and the cluster spirals around a central lumen. Individual cercariae swim poorly; the members of the aggregation rotate in the same direction, generating a current that moves the batch of up to 700 cercariae efficiently. They are positively phototactic and, using mechanisms that have yet to be understood, can reverse direction immediately if the light source moves. Beuret and Pearson suspect that many types of Rattenkonigcercariae evolved from large-tailed, preymimicking types described above; the large tails facilitate the rat king clusters.
Suddenly, a brief history of rat kings.
Officially, Rattenkonigcercariae are described as zygocercous, referring to the "yoked" tails. The term Rattenkonig, however, certainly captures the imagination (fig. 2.15). The word may have originally been associated with the Mouse King, the seven-headed rodent of an early Nutcracker tale who is the Nutcracker's nemesis. Other German fairy tales refer to rat royalty seated in carriages with knotted tails. In the Middle Ages, folks had the idea that there was a rat leader, and eventually there arose the notion of the Rat King as a group of powerful rats joined at their tails and fed by other, subservient rats. When Martin Luther inveighed against the pope, he called him (among other things) a Rattenkonig. (Luther had a fairly large suite of rodent monikers for Vatican habitues.) Presaging ecumenicism, he did not exclusively reserve these names for Catholics, but decided that some Protestant groups as well were kingdoms of rats.
Rat catchers do, on occasion, tie rats together by their tails. However, the natural occurrence of rat kings, not mediated by rat catchers, has been described all over the world. There are even published records, complete with X-rays, showing rats firmly attached (accidentally entangled?) to one another at the ends of their tails. One empiricist published his account of an attempt to produce a rat king by gluing rat tails together. He carefully recorded weight and gender, only to come to the disappointing conclusion that most rats do not want to become rat kings and are eager to abdicate (see Becker and Kemper 1964).
What should we call those parasites? "classical" (Latin) versus "barbaric" (German):
An eminent parasitologist argued for zygocercous over Rattenkonig on the basis of classical versus barbaric origins, respectively. As I consider the legend of the Rat King, in a carriage with his queen (tails entwined, of course) drawn by other loyal rats, my vote is for the barbarians. What wonderful trematodes!
Galaktionov, K. V., & Dobrovolskij, A. A. (2003).
The Trematode Life Cycle as a System of Adaptations. The Biology and Evolution of Trematodes, Chapter 2, pages 215--317.
A change in the way of infecting the host is associated with yet an- other direction in the evolution of tails, the emergence of the so-called macrocercous larvae. Forms with hypertrophied tails, many times longer than the ones typical for the group, appear independently in different families (Echi- nostomatidae, Heterophyidae, Strigeidae) (see fig. 42). They are easy to see and attract the attention of potential hosts, which swallow them readily (see pp. 282, 283). The movement of such macrocercous larvae often imitates that of other water animals, first of all, small nematodes and oligochaetes.
To enhance the attraction effect, in some representatives from, again, distant families (Echinostomatidae, Heterophyidae), the tail tips of several larvae merge to form aggregates known in the literature as “Rat-King” (“Rattenkönig”) Fig. 99, see also p. 284).
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Figure 99. Zygocercous Cercaria rhionica VII Olenev et Dobrovolskij, 1975 (Echinostomati- dae).
A, general view of a single cercaria,
B, cercariae aggregate of “Rat-King” type.
From Olenev and Dobrovolskij (1975), with permission. |
Molecular and morphological evidence for nine species in North American Australapatemon (Sudarikov, 1959): a phylogeny expansion with description of the zygocercous Australapatemon mclaughlini n. sp., Parasitology Research volume 116, pages 2181–2198 (2017)
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| Figure 2 c. Outline of cercarial zygocercous aggregate; scale bar = 200 μm |
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Figure 3. Australapatemon mclaughlini n. sp.
a. Zygocercous aggregate; scale bar = 100 μm |
Zoom in onto the head, the sucker, and the knot.
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b. Ventral view of three individual zygocercous bodies. White arrows indicate tegumental spination; scale bar = 20 μm.
c. Ventral sucker of zygocercous cercaria. White arrows indicate sucker spines; scale bar = 5 μm.
d. Zoomed-in view of cercaria tail among the aggregate tail bundle. White arrow indicates papules on tail, black arrow indicates narrowing of furcal muscles, specialized for holding on to others; scale bar = 50 μm |
Popular drawings
Amazingly, there are two drawings by artists of zygocercous parasites!
https://www.deviantart.com/the-episiarch/art/The-Rat-King-unnamed-zygocercous-cercaria-343115921 is particularly helpful, and I quote:
But there are some flukes which instead of having cercariae that swim off on their own, they aggregate into a conjoined swarm. The term used to describe those species is "zygocercous" (this only describe their morphology and is not intended to reflect their evolutionary relationship - so flukes that have zygocercous cercaria are not necessarily all closely related).
the cercariae of this species rally in the mantle cavity of the snail. They then bind to each other via the lower half of their tail, and once there is a critical mass of them, they let go and leave the snail as a single unit composed of a few dozens or up to a few hundred individuals.
Once free in the tropical waters, they synchronise their movement so that the entire aggregate swim in a wheeling, corkscrew-like motion. The reason for all this gregarious cooperation is that while each individual cercaria is tiny and barely noticeable (on the left), as an aggregated mass, they resemble zooplankton or some other tiny creature that a small fish might like to eat. This effect is enhanced by the coloration of the tail, which was described as "heavily orange pigmented".
When a fish comes along and decides to nom on this wriggling mass of parasite, they immediate latch on to the inside of the fish's mouth. Sensing that something's not right, the fish might try to spit the wriggly mass out, but by then the parasites have already stuck on using their ventral pad and begin digging into the fish's mouth. The fish might succeed in spitting out the tails, but they've already served their purpose and the parasites readily discard the tail, leaving just the main cercaria body (on the right).
the front of the parasite is equipped with a retractable, beak-like penetration organ (I have depicted it in its protruded form) with which it can use to rasp into the fish's epidermis. In addition, around the rim of the oral ring where the penetration organ is housed are a series of gland openings that can secrete digestive enzymes to help eat away at the epidermis. The parasite use the combination of both to dig their way into the fish's body.
It is currently unknown where this parasite goes once it gets inside the fish. However experimental infections conducted with a related species call Galactosomum bearupi (also from Heron Island) found that they first migrate to the connective tissue, then they become particular attracted to nervous tissues. Once they have moved into the nervous tissue, they migrate to the spinal cord and eventually end up in the optic lobes of the fish's brain. What the parasite does once it gets there is anyone's guess at the moment...
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