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On Davainea minuta Cohn: 1901(Cestoda, Cyclophyllidea) andits variation in North AmericanRecurvirostridae (Aves)D.R.R. Burt a & M.D.B. Burt a ba Gatty Marine Laboratory , St. Andrews, KY16 8LB, Scotlandb Department of Biology , University of New Brunswick , BagService 45111, Fredericton, N.B., Canada , E3B 6E1Published online: 17 Feb 2007.

To cite this article: D.R.R. Burt & M.D.B. Burt (1984) On Davainea minuta Cohn: 1901 (Cestoda,Cyclophyllidea) and its variation in North American Recurvirostridae (Aves), Journal of NaturalHistory, 18:1, 15-23, DOI: 10.1080/00222938400770031

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JOURNAL OF NATURAL HrSTOR¥,1984,18:15~23

On Davainea minuta Cohn: 1901 (Cestoda, Cyclophyllidea) and its variation in North American Recurvirostridae (Ayes)

D. R. R. B U R T and M. D. B. BURT~

Gat ty Marine Laboratory, St. Andrews KY16 8LB, Scotland

Introduction Cohn (1901) described a cestode Davainea minuta from a redshank, Tringa

totanus (L.), since it had the general appearance of a davaineid and differed from known species of the genus. I t was of small size with few proglottides and was immature. In his account of its ana tomy Cohn makes the s ta tement tha t the testes are few but increase in number to 10-12 in the eighth (last) segment, although he shows only four or five in his figure (Tar. 8, fig. 5 b).

In 1908 Fuhrmann recorded D. minuta in his Cestoden der Vogel but was unable to identify the type host, Tringa totanus, which Linnaeus had described under the allied genus Scolopax.

Harvey Johnston (1911) described from a white-headed stilt, Himantopus teucocephalus Gould, in South Australia, a cestode, Davainea himantopodis, which was of small size, of few segments and with only four testes. He enumerates three differences which his species shows in comparison with D. minuta, viz. smaller scolex, fewer testes and earlier appearances of the genitalia in the strobila. He states that the uterus does not persist but tha t in segments tha t have just passed sexual matur i ty the eggs are found in great numbers in the parenchyma.

In his account of the Davaineidae, Lopez-Neyra (1931) gives Cohn's description of D. minuta followed by Johnston 's of D. himantopodi.s and suggests tha t the latter is identical with the former. His description departs from tha t of Johnston for he states tha t 'utero no persistante; huevos con capsulas uterinas y aislados en el parenchyma medular' .

The following year, Shen Tseng (1932), describes eestodes recovered from Lobivanellus cinereus collected in ~Peking, China and identifies them as Davainea himantopodis Johnston 1911. With the exception of a slight difference in hook size (11'7 #m long in his own Chinese material compared to 7/~m long in the Australian material described by Johnston) and hook shape (based presumably on the illustration provided by Johnston), Shen Tseng indicates tha t his material is identical to tha t of Johnston. He does not, however, make any comparison with Davainea minuta and nor does he refer to Lopez-Neyra (1931).

A further brief description of D. himantopodis is provided by K. S. Singh (1952) who recovered the cestodes from Himantopu8 himantopus (L.) collected in Lucknow, India. In his account~ Singh refers only to Johnston (1911) and Shen Tseng (1932) and reconciles the hook disparity noted between Johnston 's original description of this species (7/~m) and Shen Tseng's description (11"7/~m) by pointing out tha t the two rows of rostellar hooks in his material are of different sizes. The anterior row

Department of Biology, University of New Brunswick, Bag Service 45111, Fredericton, N.B., Canada, E3B 6El.

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contains hooks 11 #m long while the posterior row contains hooks 9#m long. In addition, Singh (1952) describes the peculiar arrangement of the ventral excretory vessets which converge and join in the posterior part of each proglottis prior to entering the subsequent proglottis as a common duct. This duct then divides again to pass on either side of the genitalia before once again joining near the middle of the posterior border.

D. minuta was recorded from the redshank in the U.S.S.R. by Dubinina (1953) who also recorded it from the grey plover (Squatarola squatarola L.), the spotted redshank (Tringa erythropus (Pallas)), the stilt (Himantopus himantopus (L.) ) and the avocet (Recurvirostra avo~'etta L.). She amplifies Cohn's description in noting only four testes, or occasionally five per segment in 42 worms, and states tha t (translated), 'The uterus breaks up into separate capsules containing one or several eggs'.

Baer (1959) describes D. minuta recovered from Hemiparra crassirostris (Hart- laub) which he collected in the Belgian Congo. Baer records D. himantopodis as a synonym ofD. minuta based on the work of Dubinina (1953) and Shen Tseng (1932). Baer was able to re-examine Shen Tseng's materiM ofD. himantopodis and found the length of rostellar hooks to be 9 #m but does not refer to Singh (1952) who showed tha t there are two sizes of hooks in his Indian material.

In the same year, Belopolskaya (1959) identified D. minuta from Squatarola .s'quatarola L. collected in the Murmansk region and describes rostellar hooks of 9 #m in length, as described by Cohn (1901), for the lower crown but hooks of 12#m in length for the upper crown. She refers to two previous reports of this species from the U.S.S.R.: tha t of Dubinina (1953) from the redshank (Tringa totanus (L.)) and other Charadrifformes; and also that of Saakova (1952) from Tringa erythropus (Pallas).

Davainea himantopodis Johnston, 1911, is described by K. P. Singh (1960) from Himantopus himantopus (L.) collected in India. In his material, there are two rows of hooks of different sizes ranging from 8"5 to 10 #m in one row and from 7 to 8"5 #m in the other. Although aware of the unusual arrangement of the ventral excretory vessels described earlier by K. S. Singh (1952), this could not be seen in his material. Singh compares his material with that described by Johnston (1911), Shen Tseng (1932) and K. S. Singh (1952) but does not discuss any work referring to D. minuta.

Korpaczewska (1963), in a survey of cestodes from aquatic birds in Poland, records D. minuta from Tringa totanus and Kasymjanova (1964) records D. minuta from Himantopus h.imantopus (L.) in the Kazakhstan region.

Rego and Ibanez-Herrera (1966) found immature davaineids in the black-tailed stilt, Himantopus himantopus melanurus Vieillot, in Peru and identified them as D. minuta, finding only four testes and at tr ibuting the 10-12 of Cohn to an error in interpreting his material.

Although Met, trick (1967) identifies material from Hermiparra crassirostris (Hartlaub) collected in Zambia as D. himantopodia (s(c) Johnston 1911, he states tha t separation of this species from D. minuta is questionable.

Mukherjee (1970) records D. h.i,mantopodi~ from Himantopus hima,ntopus (L.) in India (Sikar Dist.) but gives neither a description of his material nor any taxonomic discussion.

In his s tudy of the genus Davainea, Movsesyan (1970) redescribes D. minuta from Himantop.us himantopus (L.) collected in the Kazakh C.C.P. He describes the seolex as having 60 rostellar hooks, 8#m long, and bearing unarmed suckers. He also indicates tha t the uterus tends to break down, in gravid segments, into uterine capsules tha t each contain a single egg with 120-140 egg capsules per segment. In a

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comparative table of different, species of Davainea, Movsesyan differentiates between D. himantopodis and D. minuta as the former species has armed suckers whereas D. minuta has unarmed suckers. Measurements and characteristics of other organs are also given.

Spasskaya and Spasskii (1971) claimed tha t D. minuta Cohn did not belong to Davainea and erected a new genus Himantaurus to contain it in the belief tha t the uterus persists and does not break down with the formation of egg-capsules. A more detailed account ofHimantciurus minuta was given by Spasskii et al. (1975) who hold H. minuta and H. himantopodis to be identical.

Tolkacheva (1975) records large numbers (80 to several hundred) of D. minuta from two young Recurvirostra avocetta (sic) collected in the U.S.S,R. (KarasukLakes) but gives neither a description of her material nor provides any discussion.

Agreeing with the assignment of D. minuta to the new genus Himantaurus of Spasskaya and Spasskii (1971), Smogorzhevskaya (1976) reports Himantaurus ,minutu~. from a number of Charadriiformes (Himantopus himantopus, Tringa nebularia, Charadrius alexandrinus, and Recurvirostra avosetta) from the Ukraine. I t is interesting to note tha t Smogorzhevskaya, in referring to the work of Saakova (1952) and Kornyushin (1965, 1967), indicates tha t Himantaurus minutus is also found in gulls in the delta of the Danube and on the Black Sea Coast.

M0vsesyan (1977), in his monograph of eestodes (Davaineata) of the U.S.S.R. and adjacent territories repeats both the description and the figures published previously (1970) and again recognizes both D. himantopodis and D. minuta in the key provided. D. himantopodis, with 50 rostellar hooks, 7 pm long, and with 4 testes is differentiated from D. minuta which has 60 rostellar hooks, 8-9 pm tong, and which has 4-5 testes.

Borgarenko (1981)describes Himantaurus minuta from the black-winged stilt and indicates tha t these eestodes were originally identified as D. himantopodis. Baer's (1959) reduction of D. himantopodis to a synonym of D. minuta is accepted as is the assignment ofD. minuta to the genus Himantaurus on the basis tha t the uterus persists and does not break down into uterine capsules. Borgarenko states, however, tha t no fully mature uterine segments were seen and that the eggs were not yet fully developed. Further , the most posterior proglottis figured by Borgarenko, shows deep infoldings of the uterine wall characteristic of other Davainea species prior to the further separation into discrete uterine capsules.

Results Davainea minuta in N. American Recurvirostridae

Cestodes, identified as D. minuta, were collected from Recurvirostridae as follows: from both stilts (Himantopus m-exicanus (Muller)) and avocets (Recurvirostra americana Gmelin) at Lake Tulare in California and at the Bear River Marshes in Utah, and from avocets taken at kettle-holes or ponds near Garrison Dam in N. Dakota. They show variation in length and in the number of proglottides: the shorter forms, of seven or eight proglottides, measuring little over 1 mm in length; the longer forms, of 16 or 17 proglottides, of almost three times the length; while some, intermediate in length, are also present. The short forms were found in the duodenum and the longest forms in the lower region of the intestine.

Scolex: There is variation in'the size of the seolex, the diameter showing a range of 133-227pm and the diameter of the rostellum varying from 53-70#m with a variation in the number of hooks from 55-72. The closely set, double raw of hooks

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FIG. 1.

c5

Davainea mi,nuta. A. from the duodenum ofHimantopus mexicanus. B. from the hind intestine of Recurviroo'tra a,mericana. C. rostellar hook.

differ in shape from the generally accepted hammer-shape of the davaineid hook as depicted by Joyeux et al. (1961, fig. 315 d) but are precisely similar to tha t depicted by Spasskii et al. (1975, fig. 1 c). In a comparison with the classical shape of a hook, such as tha t of a taeniid, one can identify handle, blade and guard. The handle lies within the rostellum, the projecting blade is short and hooked, and the guard lies length-wise, parallel to the surface of the rostellum. The length, from the base of the -blade to the tip of the guard, tha t par t normally visible in whole mounts, is 9/~m, and a difference is seen in the hooks of the two rows, the shorter hooks being about 0"5 #m less.

Reproductive system: The arrangement of the genitalia is tha t of the descriptions of Cohn (1901), Johnston (1911) and Spasskii et al. (1975) except tha t the testes do not increase in number in the posterior segment as Cohn maintained. The cirrus has the characteristic armature of the type species; the ovary is bilobed, the two moieties being spheroidal and lacking acini, while the vitelline gland, lying posterior to the ovarian isthmus, is ovoid and particularly conspicuous in specimens stained with Semichon's acatic carmine. Short specimens of seven or eight proglottides show a rapid development from the appearance of the primordia of the genitalia in the second proglottis to the full development of the reproductive system in the sixth, the

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Davainea minuta in N. American Recurvirostridae 19

appearance of the Uterus in the seventh and its full development with contained eggs in the eighth. In some specimens, fixation did not occur at the precise point when ovary and vitelline gland were fully developed and one finds that the vitelline gland has not reached full development in one proglottis and in the next it is already reduced while some eggs appear in the uterus. In spite of this the vitelline gland is considered to be a useful marker in comparing worms of different lengths. In worms of 16 or 17 proglottides full development of the reproductive system is not reached until the eleventh proglottis. Lying immediately anterior to the vitelline gland is a small Mehlis' gland and from it the uterus leads anteriorly to branch, the branches turning posteriorly and swelling into spheroidal diverticula. There is, accordingly, a definite uterus as claimed by Spasskaya et al. (1971) and Spasskii et al. (1975) but development proceeds further with the break-down of the uterine wall and the encapsulation of the eggs. As proglottides are normally shed after eggs pass into the uterus, later stages ofgravid proglottides can only be seen in these shed proglottides, the identi ty of which is apparent from the structure of the cirrus. There is usually one egg per capsule (fig. 2).

Excretory System: The disposition of the excretory (osmoregulatory) vessels is unusual in tha t the two ventral vessels, which occupy lateral positions in the middle of each proglottis, converge at the posterior border where they join. A single, common ventral vessel passes through the posterior border of one proglottis and into the anterior portion of the next proglottis where it bifurcates immediately with the two resulting vessels passing around the genitalia, in a lateral position, before once again converging posteriorly and anastomosing near the middle of the posterior border. Although the two smaller dorsal excretory vessels also tend to converge posteriorly, prior to passing into the next proglottis, they do not join prior to diverging again. The arrangement found in the present material is similar to tha t described by Singh (1952) and Mettrick (1967) for D. himantopodis and by Borgarenko (1981) for D. minuta.

0*~ tl~m

FIG. 2. Davainea minuta. Drawing of section of 6pro thick of a shed, gravid proglottis.

Discussion There is not a doubt but tha t the cestode described from N. American stilts and

avocets is D. minuta and that D. himantopodis Johnston is synonymous with it. Johnston 's type, No. W. 292 of the Australian Museum in Sydney, was not available, but the co-types S. 83(1) and S. 83(2) of the S. Australian Museum in Adelaide were kindly lent together with other specimens taken at Yalkuri and Tailem Bend. In both co-types~ matur i ty is reached in the eighth proglottis and in S. 83(1) the developing uterus can be made out. The material from Yalkuri comprized a single,

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stained but unmounted specimen from the intestine of a stilt, Himantopus leucocephalus Gould. From this the scolex was removed to make a cleared Berlese preparat ion to display the hooks, the strobila being sectioned. The hooks are of the size and shape of the European and N. American D. minuta. In a strobila of 13 proglottides full development of the reproductive organs is apparent in the tenth proglottis, while the uterus with its spheroidal diverticula is seen in the 1 l th , and in the 13th the walls of the uterus are breaking down. I t is considered tha t the nmuerous, rounded diverticula of the uterus, extending along each side of the medulla, were mis takenly identified as testes by Cohn (1901) and led him to make the improbable s ta tement tha t the testes, few in number and depicted as four or five in his text. figure, increase in number to 10 12 in the terminal prog!ottis. In view of the difference in size, number of proglottides and rate of development of the repro- ductive system ill N. American specimens, these characters are not considered of species-differentiating value. As D. minuta is a parasi te of Recurvirostr idae in Europe, Asia, Australia and S. America its presence in N. American birds is not unexpected.

In the senior au thor ' s field notes is the observat ion tha t the longest specimens are from the hind regio n of the intestine and the shortest specimens are from the duodenum and the anterior region of the intestine. The shorter specimens have fewer proglottides and earlier development of the reproductive system, the opposite being the case with the longer specimens, and the difference in site of the parasites, an ecological difference: would appear to be the operating factor as suggested by But t (1980). Figure 3 is a vector diagram showing the growth-curves of two typical specimens, one from the duodenum (A) and one from the hind intestine (B). In these the magnitude, calculated as the product of length and breadth of individual proglottides, is plot ted on a logarithmic scale, against time, as represented by the serial number of these proglottides. Sexual ma tu r i ty (s.m.) is a t ta ined in the shorter worm in the sixth and in the longer w o r m in the eleventh proglottis. Shed proglottides continue to grow after becoming separated from the strobila and two of these are represented a t X and Y in the ext rapola ted curve A: these measure 0"66 m m in length and 0"52 mm in breadth at X and 0-73 by 0"55 m m at Y.

Reproduct ion in eestodes involves two processes. There is an asexual one, seen in the budding of proglottides from the hind region of the strobila, while the other process is a sexual one, the production and matur ing of sperm and ova and eventual ly of fertilized eggs in these proglottides. As worms in which proglott ides mature early are found in the duodenum, it could appear tha t the need for energy, in the form of food is greater than tha t for asexual reproduction, and tha t in the rich pabulum of the duodenum, development of the gonads, ma tu ra t ion and sexual reproduction are relatively more rapid than in the less nutri t ious hind intestine where the longer strobilae with relatively slower sexual development are found. The asexual process may be termed a strobiliparous one as it is comparable with strobilation in a metagenetic coelenterate such as Aurelia where young individuals, the ephyrae, are budded from the scyphis toma or hydra- tube (Fowler 1900). Support is given to the view tha t these two processes are affected by the availabil i ty of food in the work of Calow et al. (1979) on Polycelis felina. In this turbellarian, a sexual reproduction in the process of fissiparity, or the division of the whole worm, takes place when food is sparse, but sexual reproduction or ovipar i ty takes place when food is plentiful. Accordingly the mode of reproduction depends on the avai labl i ty of energy in the form of food, ovipar i ty predominat ing in the duodenum, While in the

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Davainea minuta in N. American P~ecurvirostridae 2[

w

P a .

50-

0'5

0-1

A

7

2 4 6 8 I0 I 2 14 16

S e r i a l n u m b e r of proglottid~s

FIG. 3. Davainea minuta. Growth curves of two specimens fl'om Himantopus mexicanus: A. from duodenum and B. from hind intestine. Magnitude is represented by the product, of length and breadth of proglottides as log. ram2× l02 and age by serial number of proglottides.

hind intestine ovipar i ty is a relatively slower process and strobil ipari ty predominates.

Summary Davainea minuta Cohn, 1901, widely distr ibuted and found in a number of

Charadriiformes is reviewed and its synonymy with D. himantopodis Johnston, 1911 sustained. Himantauru~ minuta (Cohn) Spasskaya et Spasskii 1971, is considered a synonym since shed, gravid proglottides continue to grow with subsequent break- down of uterus and formation of egg-capsules. D. minuta is recorded for the first t ime from North American stilts Himantopus mexicanus (Muller) and avocets (Recurvi- rostra americana Gmelin. D. minuta shows variat ion in length and in the develop- ment of the reproductive system. In short specimens of seven or eight proglottides, the sixth is fully mature sexually; while in specimens of 16 or 17 proglottides, full sexual ma tu r i t y is not a t ta ined until the l l t h . The short specimens are from the duodenum and the longer specimens from the hind intestine. In cestodes the two

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reproductive processes: (a) asexual, in the format ion of proglottides, or strobilipar- ity, and (b) sexual, in the m~turing and production by proglott ides of eggs, or ovipari ty, occur synchronously. The lat ter process predominates where food is plentiful, as in the rich pabulum of the duodenum, but in the hind intestine where there is little food, matura t ion and egg-production is a much slower process.

Acknowledgments We acknowledge with thanks the Travel and Maintenance Grant tO D.R.R.B.

from the Carnegie Trust for the Universities of Scotland, which allowed the collection of avian parasites in the fly-ways of N. America. We thank Miss Madeline Angel, Honora ry Assistant in the South Australian Museum in Adelaide, for her help with co-types and other specimens of D. himantopodis. We also thank Professor M. S. Laverack, Director of the G a t t y Marine Labora tory , for continued facilities and accommodation; Messrs A. S. Edwards and J. Stevenson of his depar tment whose photographic expertise was the basis of the drawings in this paper; and Dr. John Sullivan, Univers i ty of St. Andrews, for his help in translat ion of Russian papers.

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Isdatel'stvo 'Shtiintsa', 252 (in Russian). SPASSKII, A. A., BO]~GARENKO, L. F., and YURrnLOVA, N. M., 1975 (Description of the type

species of the genus Himantaurus (Cestoda, Cyclophyllidea)) Izvestia Akademii Nau]c Tadzhikskoi SSR, Otdelenie Biologicheskikh Nau~, 1/58, 34 38 (in Russian).

TOLKACHEVA, L. M., 1975, (Cestode fauna of aquatic and marsh birds in the Karasuk Lakes (U.S.S.R.)). Trudy Biologicheskogo Instituta. A~ademija Nauk SSR, Sibirskoe Otdelenie, 17, 100-113 (in Russian).

TSENG, SHEN, 1932, Studies on avian cestodes from China. Part 1. Cestodes from Charad- riiform birds, Parasitology, 24, 87-106.

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