Cestodes of the genus Aploparaksis Clerc, 1903 (Cyclophyllidea, Aploparaksidae) reported from gulls, with a description of new species

Fifteen species of Aploparaksis Clerc, 1903 described from gulls or reported to infect gulls are reviewed. The re‐examination showed that gulls are parasitised by the following six species: A. borealis, A. brachyphallus, A. diagonalis, A. rissae, A. xemae and A. shigini n. sp. Only the latter species is considered to be a host‐specific parasite of gulls, whereas A. borealis is recognised as a common parasite of passeriform birds and the other four proved to be common parasites of shorebirds. Aploparaksis brachyphallos is redescribed from the skua Stercorarius longicaudus of Chukotka, and corrections, as well as supplements, are given for the original descriptions of A. rissae and A. xemae, based on the study of the type specimens. The new species, A. shigini, is described from Holarctic gulls; it was formerly known as A. larina Fuhrmann, 1921 sensu Shigin (1961). Synonyms of valid species, a range of definitive hosts, and their geographical distributions based on the results of the present investigation, are provided. Data are presented on the life cycles, intermediate hosts and the morphological types of the metacestodes of all species (except for A. shigini).


Aploparaksis larina
Description (based on two specimens from S. longicaudus from Chaun Bay, Chukotka). Length of pre-gravid specimen 38 mm. Maximum width of strobila 0.52 mm at level of last proglottides. Scolex ( Figure 1A) with evaginated rostellum 1976168 mm. Suckers round, prominent, 80 mm in diameter. Rostellum 69637, rostellar sheath 197653 mm, passes beyond level of posterior margins of suckers. Rostellar gland clustershape, located within cavity of rostellar sheath between its proximal part and proximal part of rostellum. Rostellar hooks 10, with thin blade and rudimentary handle ( Figure 1B). Total length of hook 16.6-17.4 mm (length of blade 10, length of base with guard 12-14, length of handle about 2 mm). Strobila flat, proglottides numerous, trapezoidal. Genital pores unilateral; alternation was only marked in one specimen in which the last five proglottides had indiscernible margins. Neck 410 mm long and 61 mm wide immediately posterior to scolex. Diameter of osmoregulatory canals: ventral to 45 mm, dorsal 4-5 mm in hermaphroditic proglottides. Transverse anastomoses not observed. Testis oval or egg-shaped, rarely slightly lobed, relatively large, 90-102647-57 mm, in centre of median field ( Figure 1C), sometimes it is displaced close to antiporal osmoregulatory canals. Cirrus sac cigar-shaped, 184-270625-37 mm, thick-walled, with a well-developed layer of muscular fibres orientated diagonally. In male proglottides, cirrus sac reaching or crossing median line. Internal seminal vesicle fills almost entire cavity of cirrus sac. External seminal vesicle egg-shaped, to 80649 mm, opposite antiporal region of cirrus sac or overlapping it dorsally. Fully evaginated cirrus ( Figure 1D) small, 45-57 mm long, with parabasal spherical swelling. Basal part of cirrus 10-1268 mm and parabasal swelling 12-16 mm in diameter covered with dense, small spines; with distal part up to 29 mm long and 4 mm wide at base, and 3 mm at distal part, unarmed.
Morphological variability. A comparison of the morphological features of A. brachyphallos from various definitive hosts from various parts of the Holarctic showed certain differences. They relate to the length of rostellar hooks, and size of the testis and the cirrus sac. In specimens from sandpipers ( Figure 1E and F) the hooks are 16-18.2 mm long, whereas their length in X. sabini ( Figure 1G) is 19.8-21 mm. The testis in specimens from Calidris alpina (Linnaeus), Limnodromus griseus (Gmelin), Phalaropus fulicarius (Linnaeus) and Stercorarius longicaudus is considerably larger than that from Arenaria interpres (Linnaeus) (Bondarenko 1975). The specimens with shorter cirrus sac and somewhat different configuration of cirrus ( Figure 2D) were also observed by us from the latter host, especially in the White Sea population (see Table I). The base of the cirrus of these specimens is slightly elongated with gradual transition into the parabasal swelling. The cirrus of the specimens from Larus dominicanus from Antarctica ( Figure 3) has an elongated base of the cirrus too. The cirrus of the specimens from other shorebirds ( Figure 2C) is shorter, and the bulbar swelling is clearly expressed (i.e. identical to those described above from S. longicaudus). Remarks. Aploparaksis brachyphallos is here recorded for the first time in the Laridae. It is one of the Aploparaksis spp. most frequently recorded in shorebirds. It was briefly described by Krabbe (1869) as a species of Taenia on the basis of material from sandpipers Calidris maritima (Brunnich) (Greenland) and C. alpina (the Faroe Islands). The description lacks information on the morphology of the proglottides and the armament of the cirrus. The type material of A. brachyphallos was not available for our study. Nevertheless, we believe that the spherical swelling on the cirrus and the form and length of the rostellar hooks are characters typical of this species; these features are clearly seen in the Figures 193 and 194 in the original description (Krabbe 1869). Moreover, Baer (1962) recorded A. brachyphallos from Tringa totanus (Linnaeus) in Iceland, i.e. close to the type localities. Comparison of the morphology of Baer's specimens   (Figures 2A-C) with that of the specimens from our collection revealed their identity.
We had the opportunity to re-examine the type-materials of two species allocated by von Linstow (1905) to the genera Diorchis Clerc, 1903and Skorikowia von Linstow, 1905, and confirmed that Fuhrmann (1908 was right in regarding both these species as synonymous with A. brachyphallos. The specimen of D. serpentata, whose transverse sections are present on the slide No. 24/79, is an exception; we identified it as A. xemae ( Figure 8D).
Examination of the type of A. rissae by Bondarenko (1993) showed that the original description (Schiller, 1951b) is composite, and includes the characters of both A. rissae and A. brachyphallos. After re-examination of the type material A. uelcal Spassky and Yurpalova, 1969 (INPA from Phalaropus fulicarius from Chukotka) and A. diminuens Linstow, 1905 (MHNG 24/77-78 from Ph. fulicarius from Taimyr), these species were also designated as synonyms of A. brachyphallos by Bondarenko and Kontrimavichus (1976a) and Bondarenko (1980).
The comparative study of the morphology of A. brachyphallos from shorebirds and Holarctic gulls and specimens of the type-material of A. larina from Antarctic L. dominicanus (MHNG 62/15-19) gave us good reasons to identify these two species as synonymous. We failed to find differences in the cirrus morphology of the above-described specimens of A. brachyphallos (Figures 1 and 2) and Fuhrmann's specimens ( Figure 3). Hence we established that A. brachyphallos has a bipolar distribution. However, we did not study Prudhoe's (1969) specimens of A. larina from Antarctic L. dominicanus or those of Johnston (1937) from the same bird, from Marquarie Island.
It should be noted that even after detailed investigation of the material available, the question about morphological variability of A. brachyphallos remains unresolved. This species is a rare parasite of gulls. In addition to the records in L. dominicanus, from Antarctica and in S. longicaudus from Chukotka, East Siberia, we also found A. brachyphallos in L. argentatus on Paramushyr Island, Kurils and in X. sabini from the Yukon River, Alaska (Bondarenko & Kontrimavichus 1999).   Metacestode. Ramicercus (Bondarenko 1993  Remarks. Aploparaksis rissae was known for long only from its original description (Schiller 1951a). Re-examination of the type specimen by Bondarenko (1993) shows that the hermaphroditic proglottis of A. brachyphallos was described and pictured by Schiller as a proglottis of A. rissae. Inaccuracies which have been admitted in the original description of A. rissae did not give any reasons for Spassky (1963), in describing A. filiformis, and Deblock and Rausch (1968), in describing A. daviesi (both species were described from shorebirds), to differentiate them from A. rissae. Bondarenko (1975) first believed that A. daviesi was a synonym of A. filiformis, and later, having investigated type-specimens of both species, came to the conclusion (Bondarenko 1993) that they are similar to A. rissae. For the morphology of A. rissae, and data about its life-cycle, see Bondarenko (1975Bondarenko ( , 1993 Spasskaya (1956Spasskaya ( , 1957 and Spasskaya and Spassky (1960) are in the INPA collection as follows: Nos. 199 Clerc (1903), Dubinina (1953), Spasskaya (1957 in part) nec Taenia cirrosa Krabbe, 1869; as A. fusus of Joyeux and Baer (1928), Skrjabin and Mathevossian (1945), Spasskaya (1956 in part), Spasskaya and Spassky (1960) nec Taenia fusus Krabbe, 1869;as A. larina of Schigin (1961), Spassky (1963 in part), Spasskaya (1966 in part), nec A. larina Fuhrmann, 1921. Aploparaksis larina is considered here as a synonym of A. brachyphallos (see above). Ovary 143 (120-200) mm wide, usually trilobed, in centre of median field, ventral to male organs, sometimes, when fully developed, occupies entire median field. Vitellarium compact, oval, 41620 (37-53621-49) mm, median, posterior to ovary. Seminal receptacle elongated-oval or rounded depending on filling by sperm, 90641 (45-120648-74) mm (in holotype not well outlined and visible only in gravid proglottides). Vagina 60-99 mm long, thin-walled, tubular, sometimes slightly twisted in conductive part, runs parallel with and dorsal to cirrus sac, under or rarely over it. Copulatory part of vagina 41-4966-8 mm, walls weakly sclerotised; conductive part to 58 mm long. Uterus first appears in hermaphroditic proglottides as transverse tube and with further maturation it acquires the form of a slightly lobed sac and occupies entire proglottis. Young eggs evenly distributed throughout uterus; with maturation, eggs were enveloped by a layer of substance, forming a package in the centre of the uterus. Eggs with thin outer shell, 66-107649-82 mm ( Figure 5G). Granular internal envelope is hardly discernible. Embryophore 29-33633-37 (25-29629-32)  Live eggs (Figure 7) were studied in a specimen from L. ridibundus from the Ob' River. The packet from 0.7060.59 to 1.0160.73 mm; number of eggs 33-80. Outer envelope of egg 55638 mm, granular envelope 46627 mm, embryophore 27634 mm , oncosphere 21629 mm, embryonic hooks of central and lateral pairs identical in shape and length, 12 mm long.

Remarks
The first detailed description of specimens from gulls under the name A. larina from the Rybinsk Reservoir was published by Shigin (1961). That description was included in the monographs by Spassky (1963) and Spasskaya (1966). Prudhoe (1969) mentioned this species as recorded in gulls in many regions from the Antarctic to the Arctic. However, any cestodes with a bulbous-like swelling on the cirrus were assigned to A. larina, and as a consequence, this species would represent a composite of what may be several independent taxa. The reported host spectrum of A. larina is wide and includes 16 species of birds (Tolkatcheva in Ryzhikov et al. 1985).
The re-examination of voucher specimens from gulls of Yakutiya, which were at first determined as A. cirrosa by Spasskaya (1957), as A. fusus by Spasskaya (1956), Spasskaya and Spassky (1960) and finally as A. larina by Spassky (1963) and Spasskaya (1966), and specimens collected by A. Shigin, showed that they were identical, although different to A. larina from the Antarctic (see above) described by Fuhrmann (1921). On the basis of the comparison with the present results, we consider the previous records of A. larina by Spassky (1963), Spasskaya (1966) and Shigin (1961) as belonging to A. shigini n. sp.
Aploparaksis shigini n. sp. is especially similar to A. spinosus, parasitising shorebirds, mainly snipes. One of the most distinguishing characters of the new species is the presence of a single packet (''pseudocapsules''), according to Belopolskaya and Kulachkova (1968), of eggs in the uterus, formed by secretion produced by the uterus walls. Analogous packets, only in larger quantities (two to five), are also present in the uterus of A. spinosus, but this species differs by smaller rostellar hooks (18-20 mm long), as compared to those (22-26 mm long) of A. shigini, and a larger cirrus (70-126618-21 mm and 61-90612-16 mm, respectively), the armament of the cirrus being similar.
Egg packets are formed in the uterus of A. mamaevi also, however their number reaches 10. Moreover, rostellar hooks in this species are smaller (17 mm) and the cirrus, up to 74 mm long, has a bulbous swelling, up to 8-10 mm in diameter, armed with smaller spines.
Aploparaksis sachalinensis is also close to the new species in size (20-24 mm) and shape of the hooks and the length of the cirrus (up to 120 mm), but the bulbous-like swelling of the cirrus of the latter is considerably larger (24.6624.6-30 mm), almost spherical, and armed with very fine, evenly and densely distributed spines (our unpublished data). Rostellar hooks of the rest of the above-mentioned species are 17-20 mm long and the cirrus differs in its armament. The study of fragments labelled by Clerc (1903) as A. cirrosa (ZIN, vial 312, Larus sp., the Urals, 1901) showed that their morphological characters correspond well to the characteristics of A. shigini n. sp., therefore, we consider A.cirrosa sensu Clerc, 1903 as a synonym of A. shigini. Schiller, 1951 ( Figure 8) Host. Xema sabini, also shorebirds of the genera Arenaria, Calidris, Gallinago, Limnodromus, Phalaropus and Tringa.

Aploparaksis (Aploparaksis) xemae
Intermediate hosts. Stylodrilus sp., Styloscolex sokolskajae Morev (Lumbriculidae), coelom, experimentally (Bondarenko 1978(Bondarenko , 1979. Metacestode: Typical diplocyst (Bondarenko 1978(Bondarenko , 1979 Addition to the Schiller's (1951b) description (based on type). Strobila lacks gravid proglottides. Scolex squashed, but 10 aploparaksoid hooks, shape and length (25-26 mm) of which correspond well with described ones, are clearly seen. Evaginated cirrus ( Figures 8D) short, 20 mm long, with basal swelling armed with dense, fine spines; distal region 10 mm long, unarmed. Ovary bi-winged, weakly lobed, in centre of median field; in hermaphroditic proglottides occupies almost total width of space between poral and antiporal osmoregulatory canals. Vitellarium posterior to ovary, under its anatomical centre, ventral to it. Vagina short, does not reach beyond poral osmoregulatory canals. Schiller (1951a) on the basis of material from a single X. sabini from the Arctic coast of Alaska and was known only from this report. After re-examination of the type-specimen Bondarenko (1979) provided some additional data on the morphology of A. xemae, and established certain inaccuracies in the original description, mainly in relation to the topography of female gonads and morphology of the cirrus, which led to a misidentification: from shorebirds A. xemae was recorded as A. andrei of Belopolskaya (1969), nec A. andrei Spassky, 1965;A. hirsuta of Belopolskaya (1969, in part), Bondarenko (1966, in part), nec A. hirsuta (Krabbe, 1869); A. orientalis of Tolkacheva in Ryzhikov et al. (1974, in part), nec A. orientalis Spassky and Bobova, 1961;Aploparaksis sp. of Bondarenko (1975). These corrections were introduced into the specific diagnosis of A. xemae. The elimination of inaccuracies made it possible to transfer the species from the subgenus Aploparaksis (Tanureria) where it was placed by Spassky and Yurpalova (1968) to the subgenus Aploparaksis (Aploparaksis). It also turned out that A. xemae was first described and pictured as an unidentified species Aploparaksis sp. from a few species of shorebirds from Chukotka by Bondarenko (1975). Eggs were single or joined together into packets. Mature single eggs were contained within an additional outer coat; coalescence of the outer coats from multiple eggs results in the formation of a packet (see Figure 17 in Bondarenko 1975).

Remarks. Described by
Re-examination of the type-specimens of D. serpentata von Linstow, 1905 (see above) revealed that one of them (MHNG 24/79), belongs to A. xemae (see Figure 8D). Bondarenko and Kontrimavichus (1999) recorded A. xemae in Alaska (i.e. in ''type localities'') from C. alpina. It is known in gulls from the first description only. row in the median field of the proglottis; the vitellarium is ventral to the testis, which also is displaced antiporally.
The investigation carried out showed that only six of the above-described species can truly parasitise gulls, whereas the other 10 species have been identified wrongly. Comments on each of them are provided below.
(1) Aploparaksis baeri Schiller, 1951. A new name for the form described by Joyeux and Baer (1928) from Larus argentatus of Europe as Haploparaksis fusus (5Taenia fusus Krabbe, 1869). After re-examination of Krabbe's material Baer (1956) confirmed that they belonged to the genus Hymenolepis and considered A. baeri as a synonym of Hymenolepis fusus.
(2) Aploparaksis caballeroi Flores-Barroeta, 1953 was described from the gull, Larus pipixan Wagler from Panama. The description of Flores- Barroeta (1953) was analysed in detail by Spassky (1956), who came to the conclusion that the species diagnosis does not correspond well with the generic diagnosis of Aploparaksis. Therefore, he suspected that A. caballeroi could not be regarded as a species of Aploparaksis, and he thought it was Microsomacantus lari Yamaguti, 1940. Later, Spassky (1963 proposed that the only generic taxon that could include A. caballeroi is Retinometra Spassky, 1955, a decision with which we agree. However, Schmidt (1986) once again included this species in Aploparaksis.
(3) Aploparaksis cirrosa (Krabbe, 1869) Clerc, 1903 from Holarctic gulls of the genera Larus Linnaeus and Sterna Linnaeus; described by Krabbe (1869) as a species of Taenia, later wrongly included in Aploparaksis by Clerc (1903). Fuhrmann (1906) established the presence of three testes in T. cirrosa and it is treated now as a species of Wardium Mayhew, 1925. We had the opportunity to re-examine the specimens recorded by Clerc (1903) as A. cirrosa from Larus sp. in Urals (ZIN,No. 312) and consider them as belonging to A. shigini (see above). (4) Aploparaksis crassirostris (Krabbe, 1869) Clerc, 1903 described from various shorebirds from several localities. The reported host range is unusually wide and includes 30 species (Belopolskaya 1977). However, the following reports of A. crassirostris lack information on the morphology and pictures of the specimens studied, and as it has been recently shown by , A. crassirostris is a host-specific species of the snipe, Gallinago gallinago L. Therefore, the record from the gull, Larus argentatus, in Yakutiya (Russia) (Gubanov & Sergeeva 1971) is doubtful. Some further records of species (Kuklin 2004;Galaktionov et al. 1997) from L. argentatus and Rissa tridactyla in Murman (Barents Sea) also seem to be doubtful because the determination was made on the basis of juvenile cestodes. (5) Aploparaksis furcigera (Rudolphi, 1819). A specific parasite of Anatidae, but considered as the species recorded in gulls on the basis of the data of Akhumyan (1966) and Kibakin and Babaev (1964) by Tolkatcheva (in Ryzhikov et al. 1985), which was confirmed neither by illustrations nor descriptions. (6) Aploparaksis fusus (Krabbe, 1869) Joyeux and Baer, 1928, recorded as a parasite of gulls in Europe. The name originated as a result of an incorrect transfer of the species from Hymenolepis, where it was placed by Fuhrmann (1906) to Aploparaksis by Joyeux and Baer (1928). The re-examination of Krabbe's original material by Baer (1956) confirmed the attribution of this species to Hymenolepis. For new data concerning H. fusus see Bondarenko and Kontrimavichus (2004 It was wrongly recognised by Yamaguti (1959) as a species of Aploparaksis judging from shape of the hooks. Schiller (1951b) indicated that a proglottis contained three testes. Bondarenko and Kontrimavichus (2004) Clerc, 1903of Spasskaya (1957 in gulls from Yakutiya, which was proposed by Deblock et al. (1960) based on cestodes characterised by a single testis and unusual shape of the eggs. Our re-examination of Spasskaya's collection revealed that the description of A. cirrosa by Spasskaya (1957) was a composite based on specimens of different genera: these slides contain specimens of both A. shigini n. sp. and Wardium fusus (Krabbe We hope that the present study will bring some clarity into the long discussion about the taxonomic status of Aploparaksis, parasitising gulls (see Spassky 1963 andSmogorzhevskaya 1976). There are good reasons to suppose that only one species, A. schigini n. sp., is a host-specific parasite of gulls. Four other species, A. brachyphallos, A. diagonalis, A. rissae and A. xemae, are usually parasites of sandpipers, whereas A. borealis is a common parasite of passeriform birds. All of them are rarely found in gulls.
The described case of the steady source of infection by A. diagonalis in the breeding colony L. argentatus allows us to suppose that a local intraspecific group adapted to infect gulls exists within this species (the question about the possibility of calling it ''a population'' remains still open). We are inclined to think that the infestation of gulls by other Aploparaksis species that are specific parasites of shorebirds and passeriform birds can be accounted for by the same phenomenon; that is, by the existence of local groups of Aploparaksis, which are adapted to parasitising Laridae (though these might be cases of an accidental infestation). Nonetheless, the case of A. diagonalis testifies to the mechanism of the micro-evolutionary process which is known as ''host switching'' (in an evolutionary sense). It is also evidence to corroborate the opinion expressed by  that from the evolutionary point of view Aploparaksis represents a young tapeworm group that was formed in the Pleistocene and is still undergoing a hostal and territorial expansion. would like to express our thanks also to Professor M. M. Belopolskaya, Professor R. Rausch, Dr. A.A. Shigin, Dr. Z.B. Smetanina, Mr S.A. Leonov and our colleagues from the Far East State University, Vladivostok, Russia for the material provided from their collections. We are also grateful to Migle Datkunaite for valuable assistance in preparing illustrations for publication and Eric Hoberg for the microphotographs of the cirrus of A. xemae. We also wish to thank two anonymous referees for making some useful comments, and both them and the editor for help with the language. This study was partly funded by The International Science Foundation (grant LE 3000) and the Lithuanian State Science and Studies Foundation.