Ophiotaenia lapata, Rambeloson & Ranaivoson & Chambrier, 2012

Rambeloson, Voahirana R., Ranaivoson, Hafaliana C. & Chambrier, Alain de, 2012, Ophiotaenia lapata sp. n. (Eucestoda: Proteocephalidea) from Madagascar: a parasite of the endemic snake Madagascarophis colubrinus (Colubridae), Revue suisse de Zoologie 119 (4), pp. 547-559 : 548-557

publication ID

https://doi.org/ 10.5962/bhl.part.150205

publication LSID

lsid:zoobank.org:pub:2F6506E6-C118-49FD-9ED1-A3C38C29E54F

DOI

https://doi.org/10.5281/zenodo.6303325

persistent identifier

https://treatment.plazi.org/id/8028B07F-11C2-43B1-A798-8C5736BC72AD

taxon LSID

lsid:zoobank.org:act:8028B07F-11C2-43B1-A798-8C5736BC72AD

treatment provided by

Carolina

scientific name

Ophiotaenia lapata
status

sp. n.

Ophiotaenia lapata sp. n.

Figs 1-14 View FIGS View FIGS View FIGS

TYPE MATERIAL: Holotype MHNG-PLAT-79567 (field number Mad 007a) (1 slide) and 7 paratypes: MHNG-PLAT-79568 (Mad 007b), 3 whole mounted slides and 18 cross sections; MHNG-PLAT-82165 (Mad 007p), 1 slide; MHNG-PLAT-82166 (Mad 007x), 1 slide, scolex used for SEM; MHNG-PLAT-82167 (Mad 007z), 1 whole mounted slides and 10 transverse sections; MHNG-PLAT-79570 (Mad 008a), 1 whole mounted slide. UADBA No50001 and 50003, (Mad 007), two specimens, 2 slides.

OTHER MATERIAL: MHNG-PLAT-82172 (field number Mad 007hf), 2 whole mounted slides, (voucher material used for the study of the eggs). – MHNG-PLAT-82169 (field number Mad 007y), 1 whole mounted slides and 10 transverse sections. – UADBA No50002, 50004 (field number Mad 007), and 50005 (field number Mad 007c), 3 mounted slides. Some pieces of gravid proglottides were placed in alcohol for DNA analyses. – MHNG-PLAT-79569 (Mad 007c); MHNG-PLAT-82175 (Mad 008hf), and IPCAS C-625 , 1 whole mounted slide and 4 slides of serial cross sections (from MHNG-PLAT-82175). – MHNG-PLAT-73222, from Brygoo material; Madagascar, Befandriana S., October 1967, 1 whole mounted slide and 13 transverse sections .

TYPE LOCALITY: Ambinda Nord/Beanka (-17.93986°Lat; 44.46822°Long), 18 November 2011. All material listed above is from this locality, except MHNG-PLAT-73222 .

DESCRIPTION (based on 8 specimens, 4 complete and 4 incomplete): Proteocephalidae , Proteocephalinae.

Cestodes up to 295 mm long; maximum width 1.2 mm. Strobila acraspedote, anapolytic. All proglottides longer than wide (length: width ratio 1.03-1.52 to 4.80- 6.00, from immature to gravid). Scolex 120-150 long and 190-280 (n = 3) wide, slightly wider than neck ( Figs 1-3 View FIGS , 8 View FIGS ). Suckers uniloculate, round, slightly embedded, 85- 115 (n = 12) in diameter, representing 30-48% of scolex width ( Figs 1, 2 View FIGS ). Apical organ 40-45 in diameter, i.e. 15-19% of scolex width, surrounded by cells with finely granular cytoplasm ( Fig. 8 View FIGS ). Proliferation zone 2.5-3.6 mm long and 140-185 wide.

Internal longitudinal musculature weakly developed, anastomosed, formed by numerous tiny muscle fibres ( Figs 10, 11 View FIGS ). Ventral osmoregulatory canals overlapping testes, reaching laterally vitelline follicles, 5-25 in diameter, with secondary canals directed externally; dorsal canal narrow, thick-walled, 5-10 in diameter ( Fig. 13 View FIGS ).

Testes medullary, on one layer, in two narrow lateral bands (poral field separated by terminal genitalia to preporal and postporal groups). Testes rarely reach anterior margin of proglottis, but never reach to ovary, occupying 81-88% of total length of proglottis ( Figs 10 View FIGS , 13, 14 View FIGS ). Testes 89-170 (x = 128, n = 38, CV = 17%) in number, with 47-84 (x = 66) aporal testes, 25-49 (x = 37) preporal testes and 19-38 (x = 29) postporal testes. Testes spherical, 50-65 (x = 55, n = 22) in diameter, degenerated in gravid proglottides ( Fig. 14 View FIGS ).

Cirrus-sac elongate, thick-walled, 170-250 (x = 210, n = 53) long and 75-90 (x = 80, n = 10) wide ( Fig. 9 View FIGS ); RSCS 19-26 % (x = 22%, n = 53, CV = 8 %). Cirrus length represents about 70% of cirrus-sac length. Vas deferens strongly coiled, situated between proximal part of cirrus-sac and midline of proglottides, but never crossing it.

Genital atrium present; genital pores alternating irregularly, more or less equatorial, PGP = 43-53% (x = 49 %, n = 12, CV = 6%) ( Figs 13, 14 View FIGS ). Genital ducts passing between osmoregulatory canals.

Ovary medullary, bilobed ( Figs 11 View FIGS , 13, 14 View FIGS ), 520-840 wide, RSO = 68-81% (x = 75%; n = 55; CV = 4%). Mehlis’ glands 50-80 (x = 60, n = 9) in diameter, representing 9-12% of proglottis width ( Figs 11 View FIGS , 13, 14 View FIGS ).

– embryophore; lm – internal longitudinal musculature; mg – Mehlis glands; nl – longitudinal nerve; oe – outer envelope; on – oncospheres; ov – ovary; sc – subtegumental cells; so – small outgrowths; te – testes; ud – uterine diverticles; ut – uterus; va – vas deferens; vc – vaginal canal; vd – vitelloduct; vi – vitelline follicles; vo – ventral osmoregulatory canals; vs – vaginal sphincter. Scale-bars: 8 = 100 µm; 9 = 250 µm; 10–11 = 500 µm; 12 = 50 µm.

Vitelline follicles medullary, arranged in two lateral fields near margins of proglottides, occupying 90-95% of proglottis length, interrupted at level of cirrus-sac ( Figs 13, 14 View FIGS ).

Vaginal canal forming small seminal receptacle anterodorsal to ovarian isthmus. Terminal part of vaginal canal (pars copulathrix vaginae) surrounded by large vaginal sphincter and chromophilic cells ( Fig. 9 View FIGS ). Vagina anterior (62%; n = 26) or posterior (38%) to cirrus-sac.

Primordium of uterine stem medullary, present in immature proglottides. Development of uterus of type 1 according to de Chambrier et al. (2004): in immature proglottides, uterine stem straight, occupying most length of proglottis but never crossing ovarian isthmus, formed by wide longitudinal band of chromophilic cells situated along midline of proglottides. Lumen of uterus appearing in first mature proglottides ( Fig. 13 View FIGS ); diverticula (lateral branches) formed before first eggs appear in uterine stem. In pregravid proglottides, uterus occupying up to 33% of proglottis width, with 41-68 thin-walled lateral diverticula on each side. In gravid proglottides, diverticula occupying up to 80% of proglottis width. Uteroduct enters uterus almost at level of ovary isthmus.

Eggs round, with outer envelope 140-165 in diameter ( Fig. 12 View FIGS ). Embryophore spherical, with thick supplementary spherical layer between outer envelope and oncosphere, thus forming three-layered embryophore: internal layer 18-20 (n = 8) in diameter, middle layer 29-33 (n = 7) in diameter; external layer 34-39 (n = 8) in diameter; External layer of embryophore covered by small outgrowths 2.5-4 long; oncosphere spherical, 14-15 in diameter (n = 8), with three pairs of hooks, 8-9 long ( Fig. 12 View FIGS ). Eggs mature very fast in uterus and ripe eggs (oncospheres with hooklets) are present in the first pregravid proglottides.

TYPE HOST: Madagascarophis colubrinus (Schlegel, 1837) (Serpentes, Lamprophiidae ).

SITE OF INFECTION: Intestine.

PREVALENCE: 2/2 (100%).

ETYMOLOGY: The new species is named after the vernacular local name of the host, i.e. “lapata”.

DIFFERENTIAL DIAGNOSIS: The new species is placed in Ophiotaenia La Rue, 1911 (Proteocephalinae) because of the medullary position of the vitelline follicles, the unarmed scolex with uniloculate suckers and testes forming two separate fields ( Schmidt, 1986). Ninety-six species of Ophiotaenia parasitizing reptiles and amphibians are currently recognized as valid ( Freze, 1965; Schmidt, 1986; Ammann & de Chambrier, 2008; Marsella & de Chambrier, 2008; Coquille & de Chambrier, 2008; de Chambrier & de Chambrier, 2010; de Chambrier et al., 2010, 2012). Out of these, 64 species are parasites of snakes ( Squamata ) (see Table 1 in View TABLE de Chambrier et al., 2010).

According to Freze (1965), the species of Ophiotaenia are limited in their distribution to individual continents and/or zoogeographical regions; this assumption has been then supported by other data, like an high degree of isolation determined by the presence of a number of endemic genera such as Marsypocephalus, Sandonella (both Africa), and Goezeella (South America) for fish parasites and Rostellotaenia (Africa), Acanthotaenia (Asia) and Kapsulotaenia ( Australia, Papua New Guinea) for reptiles parasites ( Freze, 1965); furthermore, for species of Ophiotaenia from amphibian hosts ( de Chambrier et al., 2006) and from reptilian hosts ( Ammann & de Chambrier, 2008), a strict specificity (oioxenous sensu Euzet & Combes, 1980) was observed in all species of this genus. For this reason, the new species is separable from 14 Ophiotaenia species found in snakes in Africa (for their complete list, see de Chambrier et al., 2010).

Ophiotaenia lapata sp. n. differs from all but one Ophiotaenia species parasitic in African snakes by the presence of an apical organ ( Table 1 View TABLE ), the only African species possessing an apical organ being O. adiposa Rudin, 1917 described from Bitis arietans from Cameroun. Ophiotaenia lapata differs from O. adiposa by its lower number of testes (89-170 versus 170-220), position of the genital pore (situated at 43- 53% of the proglottis length from the anterior margin, i.e. almost equatorial in O. lapata , versus markedly pre-equatorial, i.e. at 20-25% length of the proglottis in O. adiposa ) and smaller scolex (width 240-280 µm in the former species versus 500-600 µm in O. adiposa ) ( Table 1 View TABLE ).

Ophiotaenia lapata n. sp. also differs from all but one Ophiotaenia species parasitic in African snakes in the possession of a third layer of the egg embryophore ( Fig. 12 View FIGS ). This layer is external to the oncosphere, i.e. it forms the internal envelope of the embryophore. The eggs of all African taxa described until now possess only a twolayered embryophore ( Beddard, 1913; Rudin, 1917; Fuhrmann, 1924; Sandground, 1928; Hilmy, 1936; Mettrick, 1960, 1963; Southwell & Lake, 1939; Freze, 1965). A similar structure, i.e. an additional layer of the embryophore, was first observed in some other Proteocephalidea tapeworms (see de Chambrier & Vaucher, 1999; de Chambrier, 2006; Coquille & de Chambrier, 2008; Marsella & de Chambrier, 2008; de Chambrier et al., 2010; de Chambrier & de Chambrier, 2010; de Chambrier et al., 2012).

This character is present in a wide range of proteocephalidean genera and geographical areas, such as Proteocephalus ( P. hobergi de Chambrier & Vaucher, 1999 ) in Paraguay, Kapsulotaenia ( K. sandgroundi Carter, 1943 ) in Indonesia, Cairaella ( C. henrii Coquille & de Chambrier, 2008 ) in Ecuador, Ophiotaenia ( O. alessandrae Marsella & de Chambrier, 2008 in Ecuador, O. gallardi (Johnston, 1911) in Australia and O. bungari de Chambrier, Binh & Scholz, 2012 in Vietnam). This additional layer of the embryophore, even if it seems to be a convergence phenomenon, is considered as a good discriminant character.

The only African species, the embryophore of which is also three-layered as in the eggs of O. lapata , is O. georgievi de Chambrier, Ammann & Scholz, 2010 described recently from Leioheterodon geayi Mocquard . This species differs from O. lapata , besides being devoid of an apical organ (see above and Table 1 View TABLE ), by the number of uterine branches (23-28 in O. georgievi versus 41-68 in O. lapata ), and by the total length of the strobila (50 mm in O. georgievi versus 295 mm in O. lapata ).

DISCUSSION

Glaw & Vences (1994) and Vences et al. (2009) listed about 300 species of reptiles in Madagascar, most of them (92%) being endemic. Up to now, only two proteocephalidean cestodes, Deblocktaenia ventosaloculata (Deblock, Rosé & Broussart, 1962) , and Ophiotaenia georgievi de Chambrier, Ammann & Scholz, 2010 , were described from these reptiles ( Freze, 1965; de Chambrier et al., 2010). Ophiotaenia lapata n. sp. is the third species of proteocephalideans and the second member of Ophiotaenia reported from this country. However, it is evident that the richness of cestode fauna of reptiles in Madagascar is poorly known and it is reasonable to expect that it is much higher than indicated by the available data.

Samples of Cestodes from reptiles and amphibians collected by G. Brygoo have been deposited in the Natural History Museum in Geneva. Nine endemic hosts were found to be infected with proteocephalidean cestodes ( Table 2 View TABLE ). The material collected by G. Brygoo between 1961 and 1970 in Madagascar in reptiles and amphibians is particularly rich. A preliminary evaluation of these specimens has indicated that there are probably as many as seven unnamed species and that each of them occurs in only one host species, thus exhibiting a strict specificity (oioxene type sensu Euzet & Combes, 1981) (see Table 2 View TABLE and de Chambrier et al., 2010). One host, Madagascarophis colubrinus , probably harbours two different cestode species, i.e. O. lapata and another species of Ophiotaenia (designated as Ophiotaenia sp. 3 in Table 2 View TABLE ), which bears a huge apical organ.

The taxonomic evaluation has also shown that only few of these seven potentially new Ophiotaenia species can be described because they are not well enough preserved to enable a morphological description. In addition, the specimens were fixed with formalin and thus are unsuitable for phylogenetic studies using molecular data. It is thus obvious that new material should be collected in order to better describe the still hidden diversity of reptilian parasites in Madagascar and to elucidate their phylogenetic relationships.

TABLE 1. Species of Ophiotaenia from reptiles in Africa (modified from de Chambrier et al., 2010)

Species Number of testes RSCS Position of the genital pore Position of the vagina Apical organ Width of scolex Total body length (mm) Uterine branches on each side Diameter of eggs
O. adiposa 170-220 26%* 20-25% ant-post yes 500-600 300-400 40-50 12**
O. congolensis 65 25% 44-47%* ant-post ? ? 80 15-20 15
O . crotaphopeltis 94-98 14%* 54%* ? no 160-180 not given 15-18 26
O . elapsoidae 100-125 24%* 50%* post-ant no 1000-1100 150 48-55  
O. gabonica 130-170 18-20% 42%* generally post no 300-600 > 380 38-46 39
O. georgievi 92-140 19-32% 44-56% post-ant no 225-235 50 23-28 31-35
O. meggitti sp. inq. 86-104 33% 50%* usually ant. ? not given > 68 35 25
O . monnigi sp. inq. 80 10-11% 51%* ant ? no scolex 50 50-57 30
O . nigricollis 176-210 20-22% 38%* ant-post no 300-310 170 16-20 26-33
O. nybelini 67-90 16-20% 47%* ant-post no 105 52 25-40 25
O . ophiodex 110-120 22-25% >50% ant-post no 790-1140 210-270 30-42 27-36
O. southwelli 170-230 46-50%* 50-55%* ant-post no 1500 90 8 to 12 30
O . theileri 160-310 20-25% 41-50%* ant-post no 400 estimated 300 35-40 18**
O. zschokkei 160-200 20-25% 50% usually ant. no 400 estimated 550-600   18**
O. lapata sp. n. 89-170 19-25% 43-53% post-ant yes 190-280 295 41-68 34-39

Abbreviations: RSCS = relative size of the cirrus-sac expressed as percentage of its length to the width of the proglottis from the anterior margin;

* - taken from figures in Freze (1965); ** - diameter of oncosphere.

TABLE 2. Cestodes parasites of reptiles and amphibiens from Madagascar (Coll. Brygoo)

No Host Genus species locality Date Parasites No MHNG-PLAT-
181/62 R.219 Chalanodon madagascariensis St Augustin 7.1962 Oochoristica sp. 73278
197/67 R.632 Ithycyphus sp. Perinet 2.1968 Deblocktaenia sp. 73277
27/68 R.638 Lioheterodon geayi Antananarivo 4.1968 Ophiotaenia georgievi 65470 - 65477
207/63 R.290 Lioheterodon modestus Tanandava 11.1962 Cestode  
28/61 R.63 Lioheterodon modestus Ejeda-Betioky 4.1961 Ophiotaenia sp. 1 62581
38/69 R.667 Lioheterodon modestus Befandriana 12.1969 Ophiotaenia sp. 1 73261
199/61 R.171 Liopholidophis lateralis Tana 11.1961 Ophiotaenia sp. 2 ?  
48/64 R.409 Liopholidophis sexlineatus Andramasina 2.1964 Ophiotaenia sp. 2 73260
181/67 a R.628 Madagascariophis colubrina Befandriana 10.1967 Ophiotaenia lapata 73222
181/67 b R.628 Madagascariophis colubrina Befandriana 10.1967 Ophiotaenia sp. 3 73225
183/67 R.629 Mimophis mahafalensis Plateau Mahafaly 10.1967 Ophiotaenia sp. 4 73276
299/62 R.242 Mimophis mahafalensis Lac Bemanta 10.1962 Ophiotaenia sp. 4 73282
208/63 R.291 Sanzinia madagascariensis Ambavaniasy 4.1963 Ophiotaenia sp. 5 73279
71/70   Anodonthyla montana Andringitra 1.1971 Ophiotaenia sp. 6 73267
78-70 R.678 Lioheterodon geayi Antananarivo 4.1968 Ophiotaenia georgievi 73212
97/65 R.531 Madagascariophis colubrina Befandriana 8.1965 Ophiotaenia sp. 3 73274
By 187   Rana mascareniensis Maintirano   Ophiotaenia sp. 7 73273
UADBA

University dAntananarivo, Department de Biologie Animale