Research Article |
Corresponding author: Jean Mariaux ( jean.mariaux@ville-ge.ch ) Academic editor: Fredric Govedich
© 2018 Jean Mariaux, Boyko B. Georgiev.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Mariaux J, Georgiev BB (2018) Bird cestodes from Huinay (Comau Fjord), Chilean Patagonia: several species of the family Dilepididae (Platyhelminthes, Cyclophyllidea), with the erection of two new genera. ZooKeys 797: 1-18. https://doi.org/10.3897/zookeys.797.28005
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Birds in the Huinay area, Los Lagos region, Chile, were studied for parasites. Here we report 2 new genera and species of the family Dilepididae (Cyclophyllidea) found in common local passerines: Janinellia peebeehi gen. n., sp. n. was found in Elaenia albiceps (Tyrannidae) and Huinaylepis elegans gen. n., sp. n. was found in Aphrastura spinicauda (Furnariidae). Other dilepidid parasites are reported for the first time from Xolmis pyrope (Tyrannidae) and from 2 species of Rhinocryptidae. Cotylorhipis sureshi Jadhav & Shinde, 1981 is considered a species inquirenda. The very high diversity and endemism of the observed cestode fauna in the Valdivian temperate rain forests is noted.
Biodiversity, Cestoda , Chile, COI, Dilepididae , Furnariidae , helminth parasites, Passeriformes , Rhinocryptidae , Tyrannidae
Chile is home to a very rich avifauna comprising more than 460 species (
This paper reports on a series of tapeworms of the family Dilepididae found in hosts belonging to the Furnariidae, Tyrannidae and Rhinocryptidae, including 2 new genera and species.
Hosts were caught with mist nets, kept in fabric bags for a short time, then killed with an overdose of diethyl-ether, and autopsied immediately after their death. The digestive system was entirely removed, cut in sections if necessary, and searched for parasites under a dissecting microscope. Cestodes were fixed in hot 4% formalin after a small fragment was preserved in ethanol for DNA studies. Fixed specimens were transferred to 70% ethanol for storage. Further treatment included staining with Mayer’s hydrochloric carmine, dehydrating in an ethanol series, clearing in eugenol and mounting in Canada balsam. Some scoleces were prepared in Berlese’s medium for examination of their rostellar armament.
Drawings and photographs were made respectively with a drawing tube and a digital camera on a Nikon 80i microscope. Unless otherwise stated all measurements are in micrometers. Minimum and maximum values are reported followed by the mean and number of observations in parentheses when applicable. Conventions for dilepidid descriptions follow
Collections acronyms: MHNG-PLAT: Muséum d’Histoire Naturelle de Genève (Invertebrates Department, Platyhelminthes Collection),
Janinellia peebeehi sp. n. by original designation.
Dilepididae, Dilepidinae. Body small to medium. Scolex without rostellum, apical structures consist of unarmed glandular pouch. Suckers weakly muscular. Genital pores irregularly alternating. Genital ducts passing between osmoregulatory canals. Cirrus sac weakly muscular, elongate. Cirrus unarmed. Vagina posterior to cirrus sac. Testes numerous, posterior, in one field. Uterus initially reticular. Parasite of South-American passerines (Tyrannidae).
The genus name (feminine) is dedicated to Prof. Janine N. Caira (Storrs, Connecticut, USA) in recognition of her remarkable and tireless action in favour of tapeworm systematics.
Dilepidids with distinct but unarmed apical structures are known from various avian hosts, and are presently classified within several genera as synthesized by
Elaenia chilensis Hellmayr, 1927 (Passeriformes, Tyrannidae), Fio-fio, Chilean White-crested Elaenia.
2/12 (16.7%).
1–2.
Small intestine.
HSFS, Comau Fjord, Los Lagos region, Chile, −42.39, −72.42. Altitude 10–30 m. (Type locality).
29.11.2008 and 2.12.2008.
3 specimens. Holotype: MHNG-PLAT-82292 (on slide). Paratypes: MHNG-PLAT-120515; MHNG-PLAT-82293 (2 specimens, on slides).
The species name phonetically reminds one of the acronyms of the NSF program that was sponsoring the project (Planet Biodiversity Inventory, PBI).
Body of small to medium size, up to 34 mm long (inferred from fragmented specimen). Strobila with almost parallel margins, gradually expanding in posterior direction: immature, mature, pregravid and gravid proglottides up to 250, 550, 700 and 1025 wide, respectively. Maximum width achieved at level of early gravid proglottides. Most complete specimens consisting of up to 157 proglottides. Proglottides weakly craspedote, wider than long except for very last gravid ones, which can be up to twice longer than wide. Two pairs of osmoregulatory canals. Ventral canals up to 50 in diameter, with posterior transverse anastomosis in each proglottis. Dorsal ones up to 11 in diameter.
Scolex (Fig.
Testes 13–17 (14.8, n = 25) in number, disposed in two dense layers, forming a continuous field filling most of posterior two thirds of median field of proglottides; posterior, lateral and dorsal to vitellarium, overlapping posterior parts of ovary; in younger proglottides, testes may occupy most of dorsal parenchyma (Fig.
Vitellarium large, up to 130 wide, central, lobate, oval or bean-shaped. Ovary transversely-elongate, massive and multilobulate, with two poorly marked and slightly asymmetrical wings, occupying entire width of median field and up to 30–40% of proglottis length. Mehlis’ gland not distinct as glandular structure. Ootype central, just anterior to vitellarium. Seminal receptacle oval 45–58 × 35–45 when empty, up to 150 × 87 when full. Vagina posterior to cirrus-sac, straight, distally thin-walled, proximally bordered with a row of large, dense cells; distal part often dilated, sometimes filled with spermatozoa (Figs
Uterus initially as loose reticulated network, then becoming denser as eggs develop, overlapping osmoregulatory canals and filling most of proglottis, including part of lateral fields (Fig.
The new species is the type species of the newly erected monotypic genus Janinellia gen. n.
Huinaylepis elegans sp. n. by original designation.
Dilepididae, Dilepidinae. Small strobila. Rostellum armed with two rows of hooks with peculiar and irregular 2-1 alternation. Rostellar pouch glandular. Suckers armed on anterior half, with largest antero-central hooks and progressively shorter ones laterally. Genital pores irregularly alternating. Genital ducts dorsal to osmoregulatory canals. Cirrus sac reaching osmoregulatory canals. Cirrus armed with strong spines. Testes in one field extending bilaterally and often also anteriorly to form circle reaching anterior proglottis margin. Ovary small. Uterus labyrinthic. Parasite of South American passerines (Furnariidae).
The genus name (feminine) derives from the name of the locality and the Latin suffix –lepis (scales).
Dilepidids with armed suckers, especially armed with true hooks and not merely spines, are very uncommon. The present material can only be compared with Cotylorhipis Blanchard, 1909, which is also found in South American furnariid birds. Although the general aspect of C. furnarii (Del Pont, 1906) and our specimens is similar because of the obvious sucker armament and despite an incomplete description of the former taxon [based on
Aphrastura spinicauda (Gmelin, 1789) (Passeriformes, Furnariidae), Rayadito, Thorn-tailed Rayadito.
4/5 (80%).
4 to about 10 specimens.
Small intestine.
HSFS, Comau Fjord, Los Lagos region, Chile, −42.39, −72.42. Altitude 10–30 m. (Type locality).
29.11–10.12.2008.
Holotype: MHNG-PLAT-82294 (on slide). Paratypes: MHNG-PLAT-82295; MHNG-PLAT-120512 to MHNG-PLAT-120514 (about 30 specimens, on slides). Additional non-type material: Locality: “Valdivia Forest Reserve, First refuge” (according to Franco Bona’s field books, deposited in
The species name refers to the elegant (Latin: elegans) aspect of the worm’s scolex.
Body of small size, up to 18 mm long and with maximum width 600 at level of gravid or late mature proglottides. Up to 36 acraspedote proglottides (observed; maximum number of proglottides inferred from various fragments is about 44). Proglottides initially wider than long, progressively becoming as long as wide at level of male proglottides, then up to about twice as long as wide (terminal gravid proglottides). Development of strobila with marked steps instead of being progressive (similar to serial maturation sensu
Scolex (Fig.
Testes 16–22, rarely only 14 or up to 24 (19, n = 84) in number, disposed in entire median field reaching anterior proglottis margin and forming U-shaped field, with converging branches, often forming circle with one or two anterior testes linking the two lateral fields (Fig.
Ovary central, small, compact, bilobed, anterior and dorsal to vitellarium. Vitellarium massive, central, compact, oval. Vagina posterior or ventral to cirrus pouch, straight, often dilated. Conductive part surrounded by thick but not dense cellular layer. Seminal receptacle oval, very large, commonly over 170 × 120, up to 217 × 160.
Young uterus saccular, becoming labyrinthic, filling space between osmoregulatory canals, containing a limited number (less than 200) of large eggs situated in 3 or 4 layers. Oncospheres ovoid, 29–37 × 19–25 (33 × 21.5, n = 21). Embryonic hooks 11–13 long (Fig.
The new species is the type species of the newly erected monotypic genus Huinaylepis gen. n.
In 2005, the late Prof. Franco V. Bona (Torino) left his tapeworm collection to the
Cotylorhipis was a monotypic genus until
Xolmis pyrope (Gmelin, 1789) (Passeriformes, Tyrannidae), Diucon, Fire-eyed Diucon.
1/1.
3 specimens.
Small intestine.
HSFS, Comau Fjord, Los Lagos region, Chile, −42.39, −72.42. Altitude 10–30 m.
1.12.2008.
MHNG-PLAT-87930.
MHNG-PLAT-87930 [CHIL-028/C2]. Partial COI sequence, Genbank MH663465.
(based on only a few available mature proglottides): Body of small size, largest specimen 12.8 mm long and maximum width 675 mm wide. Up to 86 proglottides observed (up to mature stage, no complete specimens available), wider than long, craspedote. Scolex 275–330 (n = 2) in diameter, bearing four elongated and rather weak unarmed suckers155–175 (164, n = 7) in diameter. Rostellar pouch 280–285 × 123–148 (n = 2) with dense posterior glandular zone. Rostellum large, 243–265 × 95–118 (n = 2) present, strongly muscular but with distinct central glandular zone (Fig.
Testes 16–21 (18, n = 10) in number, situated in single posterior field, in 2–3 layers, not extending beyond osmoregulatory canals. External vas deferens coiled, forming compact aggregation. Cirrus sac thin-walled 139–168 × 30–36 (149 × 33, n = 7) extending past the osmoregulatory canals. Cirrus armed with very fine spines.
Vitellarium immediately anterior to testes field, central, slightly V-shaped. Ovary lobulated and elongate transversely, anterior (poorly visible in our material). Vagina in same plane as, and posterior to, cirrus sac; wide, straight, opening in simple genital atrium about 15 deep (Fig.
This material is likely to represent a new species. However a complete description is not possible without observations of the uterine development. Its generic position remains uncertain. According to
To our knowledge the genus is monotypic and K. capsulata can easily be separated from our material by its shorter rostellar hooks and longer cirrus sac. Thus, should the observation of gravid segments confirm the placement of the present material into Kintneria, it would belong to a new species.
The two species belonging to the other similar genus, Monosertum parinum (Dujardin, 1845) and M. mariae (Mettrick, 1958), are known from European passerine birds only; furthermore, they are characterized by an osmoregulatory system forming a complicated reticular formation in the scolex and the neck (
A few specimens were retrieved from 2 species of terrestrial Rhinocryptidae with a limited distribution. Unfortunately, our material does not allow for complete descriptions of these worms. The limited available characters are briefly reported below.
Dilepididae. gen. sp. 1: Three fragments of 2 or 3 incomplete specimens, no gravid proglottides. Max length 2.6 mm for 20 proglottides weakly craspedote and wider than long, max width 560. A single scolex 312 wide. Powerful suckers 195–205 in diameter. Rostellar pouch indistinct, about 135 long. Rostellum muscular 107 × 40 with hooks mostly lost. Remaining hook fragments suggest 2 rows and a length of about 12. Neck short. Very rapid development of strobila with testes appearing in 7th proglottides and mature proglottides in 12th to 14th. Genital pores regularly alternating and genital ducts passing between osmoregulatory canals. 10–14 testes (12, n = 10) in one posterior field and 1 to 2 layers, not extending past osmoregulatory canals. Cirrus pouch 155–168 × 28–38, crossing excretory canals, slightly oblique. Cirrus armed with small spines. Ovary transverse anterior, bi-winged. Vitellarium posterior central and massive up to 58 × 96. Vagina posterior to cirrus pouch, finely armed.
MHNG-PLAT-120516. Host: Scelorchilus rubecula (Kitlitz, 1831) (Passeriformes, Rhinocryptidae), Chucao, Chucao Tapaculo. Small intestine. Prevalence: 1/6 (17%). Locality: HSFS, Comau Fjord, Los Lagos region, Chile, −42.39, −72.42, 50 m, 7.12.2008.
Dilepididae gen. sp. 2 (Fig.
MHNG-PLAT-120517. Same host and collection data as previous material.
Dilepididae gen. sp. 3: A single specimen in 2 parts, no scolex. Length 1.55 mm and 675 maximum width at gravid proglottides level. 75 proglottides, craspedote, mostly wider than long, becoming slightly longer than wide when gravid. Genital pores irregularly alternating in short series. Genital ducts in between osmoregulatory canals. Cirrus pouch 155–205 × 23–31, oblique, crossing osmoregulatory canals opening at anterior third of proglottides margin. Cirrus armed with small spines. Testes 12–16, in 2 layers, in a compact posterior field, in between osmoregulatory canals. Ovary bi-winged, anterior, difficult so see. Vitelline gland central, massive, up to 130 in diameter. Vagina posterior to cirrus pouch, copulatory part lined with short hairs/spines. Seminal receptacle large, central, anterior to vitellarium. Uterus multilobate, progressively filling entire proglottides. Eggs with thick external envelope.
MHNG-PLAT-120518. Host: Pteroptochos tarnii (King, 1831) (Passeriformes, Rhinocryptidae), Black-throated Huet-huet, Hued-hued del sur. Small intestine. Prevalence: 1/5 (20%). Locality: HSFS, Comau Fjord, Los Lagos region, Chile, −42.39, −72.42, 10 m, 10.12.2008.
It is the first record of tapeworms in this family of birds. Despite the limited material available, key characters confirm that at least 3 different species of cestodes are present. Thus an interesting diversification of dilepidids has occurred, at least locally, in these rather elusive hosts. It would obviously be very interesting to collect more of them in various areas of their range, which encompasses most of South America.
It is widely accepted that biodiversity is particularly important in tropical rainforests (
We are very grateful to Vreni Haüssermann, Günter (“Fossi”) Försterra and Rheinhardt Fitzek for their support and dedication and for their very efficient help with administrative matters. We also thank Joshua Biro, Hannes Imhoff, Michelle Marcotte, and all the Huinay Station staff for their help, as well as Janik Pralong (Geneva) for specimen preparation. We enjoyed the support of Daniel Gonzalez Acuña, Karen Ardiles Vilegas and Tomás Torres in the field and in the lab. Veronica Ivanov (Buenos Aires) provided some rare literature. The late Franco V. Bona (Torino) entrusted us with his exceptional collection, we hope to make good use of it. We are especially thankful to Andrea Waeschenbach (London) for sharing unpublished sequence data. Finally we are indebted to John Hollier (Geneva) for editing our English. Collections were made under permit 04-2008 from the HSFS. This research was supported by NSF PBI awards Nos 0818696 and 0818823. This paper is publication number 157 from the HSFS.