Dactylogyridae

Haliotrema angelopterum, from Plaisance et al. (2004). 1: Composite whole-mount drawing; 2: dorsal bar; 3: ventral bar; 4: dorsal anchor; 5: ventral anchor; 6: hook; 7: copulatory complex.

Belongs within: Monopisthocotylea.
Contains: Neodactylogyrus, Dactylogyrus.

Choking worms
Published 1 September 2022

The parasitic flatworms known as flukes have attained a well-deserved notoriety. Of the two largest subgroups of flukes, most of this notoriety is attached to members of the Digenea as this group includes those species that directly infect humans. However, one should not underestimate the diversity of their counterparts in the Monogenea. Monogenean flukes are mostly parasites of aquatic vertebrates (fishes and amphibians). Unlike digeneans with their complex life cycles alternating between invertebrate and vertebrate hosts, monogeneans have just a single host and lack an ecologically differentiated larval stage.

Cichlidogyrus philander, from Igeh et al. (2017). Abbreviations: ap = accessory piece; hp = haptor; pe = penis. Scale bar = 20 µm.

With over 1000 species described to date, the Dactylogyridae are one of most diverse families currently recognised among the flukes (Kmentová et al. 2022). All known species are parasites of ray-finned fishes, with different species attacking marine and freshwater hosts. The majority of species are ectoparasites on the host’s gills. Others attach to the skin or are endoparasites, inhabiting the nasal cavities, digestive tract or urinary system.

Dactylogyrids are small to medium-sized flukes, the largest growing a couple of millimetres in length. At the head end of the worm is a subterminal mouth and two to five bilateral pairs of adhesive head organs. There are often two or four eye-spots that may help the fluke in locating a host. The rear end of the body forms a large attachment organ, the opisthaptor. In typical dactylogyrids, the opisthaptor is more or less disc-shaped and carries two pairs of large hooks that are used to grasp the host. In some species, however, only one pair of hooks is present or none. Individuals are hermaphroditic with male and female gonads opening via a common genital pore.

Dactylogyrus remi, from Řehulková et al. (2020).

As is typical for soft-bodied animals with few systematically useful characters, the classification of dactylogyrids has been beset by uncertainty. Historically, several subfamilies have been recognised but they have often been poorly defined. A broad molecular phylogenetic analysis of dactylogyrids by Kmentová et al. (2022) identified two major clades within the family that the authors proposed recognising as Dactylogyrinae and Ancyrocephalinae. However, neither clade could be clearly distinguished morphologically. Though individual species are typically sensitive to salinity levels (to the extent that changes in tank salinity have been used to control monogenean gill parasites in aquaculture), both marine and freshwater taxa were included in both clades. However, molecular data did indicate that endoparasitic species formed a single clade within Dactylogyrinae.

Gill-parasitic dactylogyrids primarily impact their hosts through damage to the gill tissues, reducing their efficacy in oxygen uptake. Such damage may be induced actively by the worm’s feeding, or mechanically by the action of the opisthaptor, and may take the form of lesions. Strings of sticky parasite eggs may be visible tangled among the gill filaments, doubtless further inhibiting breathing. Efforts to develop an aquaculture industry for dhufish Glaucosoma hebraicum here in Western Australia have been stymied by heavy infestations with the species Haliotrema abaddon (Kritsky & Stephens 2001). Infested fishes suffered poor growth and vitality and were vulnerable to secondary effects such as organ dysfunction or infection by other parasites. The worms spread readily between hosts and even thwarted attempts to prevent their transmission between tanks. Evidently, those dactylogyrid eggs are easily picked up.

References

Kmentová, N., A. J. Cruz-Laufer, A. Pariselle, K. Smeets, T. Artois & M. P. M. Vanhove. 2022. Dactylogyridae 2022: a meta-analysis of phylogenetic studies and generic diagnoses of parasitic flatworms using published genetic and morphological data. International Journal for Parasitology 52: 427–457.

Kritsky, D. C., & F. Stephens. 2001. Haliotrema abaddon n. sp. (Monogenoidea: Dactylogyridae) from the gills of wild and maricultured West Australian dhufish Glaucosoma hebraicum (Teleostei: Glaucosomatidae), in Australia. Journal of Parasitology 87 (4): 749–754.

Systematics of Dactylogyridae
Dactylogyridae (see below for synonymy)
| i. s.: Uroleidoides falxus Zago, Yamada et al. 2020KC-L22
| Urogyrus Bilong Bilong, Bongiovani & da Silva 2020KC-L22
| Acolpenteron Fischthal & Allison 1941KC-L22
| Trivitellina Johnston & Tiegs 1922D56
| Bothitrema Price 1936 [Bothitrematinae]D56
| `--B. bothi (MacCallum 1913)D56
|--Linguadactyla Brinkmann 1940D56 [LinguadactylinaeKC-L22]
| `--*L. molvae Brinkmann 1940D56
|--LinguadactyloidinaeKC-L22
|--HareocephalinaeKC-L22
|--HeterotesiinaeKC-L22
|--Ancyrocephalinae [Anacanthorinae, Ancylodiscoidinae]KC-L22
| | i. s.: Ancylodiscoides Johnston & Tiegs 1922KC-L22
| | Anacanthoroides Kritsky & Thatcher 1974KC-L22
| | Anchylodiscus Johnston & Tiegs 1922KC-L22
| | Bagrobdella Paperna 1969KC-L22
| | Bifurcohaptor Jain 1958KC-L22
| | Malayanodiscoides Lim & Furtado 1986KC-L22
| | Mizelleus Jain 1957KC-L22
| | Notopterodiscoides Lim & Furtado 1986KC-L22
| | Pangasitrema Pariselle, Euzet & Lambert 2004KC-L22
| | Paraquadriacanthus Ergens 1988KC-L22
| | Philureter Viozzi & Gutiérrez 2001KC-L22
| | Protoancylodiscoides Paperna 1969KC-L22
| | Schilbetrematoides Kritsky & Kulo 1992KC-L22
| | Synodontella Dossou & Euzet 1993KC-L22
| |--Anacanthorus Mizelle & Price 1965KC-L22
| | |--+--A. lepyrophallus Kritsky, Boeger & Van Every 1992KC-L22
| | | `--A. paraxaniophallus Moreira, Carneiro et al. 2019KC-L22
| | `--A. penilabiatus Boeger, Husak & Martins 1995KC-L22
| |--+--Characithecium Mendoza-Franco, Reina & Torchin 2009KC-L22
| | | `--C. parapanemense Zago, Franceschini et al. 2021KC-L22
| | `--+--Pavanelliella Kritsky & Boeger 1998KC-L22
| | | `--P. pavanellii Kritsky & Boeger 1998KC-L22
| | |--Mymarothecium Kritsky, Boeger & Jégu 1998KC-L22
| | | `--M. viatorum Boeger, Piasecki & Sobecka 2002KC-L22
| | |--+--Onchocleidus Mueller 1936D56
| | | | `--O. similis Mueller 1936KC-L22
| | | |--Ancyrocephalus Creplin 1839D56 [AncyrocephalinaeKC-L22]
| | | | |--*A. paradoxus Creplin 1839 (see below for synonymy)D56
| | | | |--A. bychowskii Markewitch 1934D56
| | | | |--A. cruciatus (Wedl 1857)D56
| | | | |--A. forceps (Leuckart 1857)D56
| | | | |--A. parvusC02
| | | | |--A. percae Ergens 1966KC-L22
| | | | `--A. vanbenedeni (Paron & Perugia 1890)D56
| | | `--+--Ligictaluridus Beverley-Burton 1984KC-L22
| | | | `--L. pricei (Mueller 1936)KC-L22
| | | `--Actinocleidus Mueller 1937D56
| | | `--A. recurvatus Mizelle & Donahue 1944KC-L22
| | |--+--Unibarra Suriano & Incorvaia 1995KC-L22
| | | | `--U. paranoplatensis Suriano & Incorvaia 1995KC-L22
| | | `--+--Vancleaveus Kritsky, Thatcher & Boeger 1986KC-L22
| | | | `--V. janauacaensis Kritsky, Thatcher & Boeger 1986KC-L22
| | | `--Ameloblastella Kritsky, Mendoza-Franco & Scholz 2000KC-L22
| | | |--A. edentensis Mendoza-Franco, Mendoza-Palmero & Scholz 2016KC-L22
| | | `--+--A. chavarriai (Price 1938)KC-L22
| | | `--A. unapioides Mendoza-Franco, Mendoza-Palmero & Scholz 2016KC-L22
| | `--+--Urocleidoides Mizelle & Price 1964KC-L22
| | | |--U. digitabulum Zago, Yamada et al. 2020KC-L22
| | | `--+--U. uncinus Zago, Yamada et al. 2020KC-L22
| | | `--+--U. tenuis Zago, Yamada et al. 2020KC-L22
| | | `--+--Cacatuocotyle Boeger, Domingues & Kritsky 1997KC-L22
| | | | `--C. papilionis Zago, Franceschini et al. 2018KC-L22
| | | `--Diaphorocleidus Jogunoori, Kritsky & Venkatanarasaiah 2004KC-L22
| | | |--D. magnus Zago, Franceschini et al. 2021KC-L22
| | | `--D. neotropicalis Zago, Franceschini et al. 2021KC-L22
| | `--+--Unilatus Mizelle & Kritsky 1967KC-L22
| | | `--U. unilatus Mizelle & Kritsky 1967KC-L22
| | `--+--Heteropriapulus Kritsky 2007KC-L22
| | | |--H. heterotylus (Jogunoori, Kritsky & Venkatanarasaiah 2004)KC-L22
| | | `--H. simplex Li & Huang 2012KC-L22
| | `--Trinigyrus Hanek, Molnár & Fernando 1974KC-L22
| | |--+--T. anthus Franceschini, Acosta et al. 2020KC-L22
| | | `--T. carvalhoi Franceschini, Acosta et al. 2020KC-L22
| | `--T. peregrinus Nitta & Nagasawa 2016KC-L22
| `--+--+--Schilbetrema Paperna & Thurston 1968KC-L22
| | `--+--Susanlimocotyle Soares, Domingues & Adriano 2020KC-L22
| | | `--S. narina Soares, Domingues & Adriano 2020KC-L22
| | `--Hamatopeduncularia Yamaguti 1953KC-L22
| | |--H. arii Yaamaguti 1953KC-L22
| | `--+--+--H. isosimplex Lim 1996KC-L22
| | | `--H. petalumvaginata Soo & Tan 2021KC-L22
| | `--+--+--H. bagre Hargis 1955KC-L22
| | | `--‘Chauhanellus’ boegeri Domingues & Fehlauer 2006KC-L22
| | `--Chauhanellus Bychowsky & Nagibina 1969KC-L22
| | |--*C. oculatus Bychowsky & Nagibina 1968KC-L22
| | |--C. auriculatum Lim 1994KC-L22
| | `--C. intermedius Lim 1994KC-L22
| |--+--+--Bychowskyella Akhmerov 1952KC-L22
| | | | `--B. pseudobagri Akhmerov 1952KC-L22
| | | `--Quadriacanthus Paperna 1961KC-L22
| | | |--+--Q. clariadis Paperna 1961KC-L22
| | | | `--Q. fornicates Francová & Řehulková 2017KC-L22
| | | `--Q. mandibulatus Francová & Řehulková 2017KC-L22
| | `--Thaparocleidus Jain 1952KC-L22
| | | i. s.: *T. wallagonius Jain 1952KC=L22
| | |--T. campylopterocirrusKC-L22
| | `--+--+--T. siluri (Zandt 1924)KC-L22
| | | `--T. vistulensis (Sivak 1932)KC-L22
| | `--+--Cornudiscoides Kulkarni 1969KC-L22
| | | |--*C. heterotylus Kulkarni 1969KC-L22
| | | |--C. geminus Gusev 1976KC-L22
| | | `--C. proximus Gusev 1976KC-L22
| | `--Pseudancylodiscoides Yamaguti 1963KC-L22
| `--+--Aphanoblastella Kritsky, Mendoza-Franco & Scholz 2000KC-L22
| | |--A. aurorae Mendoza-Palmero, Scholz et al. 2012KC-L22
| | `--+--A. magna Yamada, Acosta et al. 2018KC-L22
| | `--A. travassosi (Price 1938)KC-L22
| `--+--+--Cosmetocleithrum Kritsky, Thatcher & Boeger 1986 (see below for synonymy)KC-L22
| | | |--+--C. bifurcum Mendoza-Franco, Mendoza-Palmero & Scholz 2016KC-L22
| | | | `--C. bulbocirrus Kritsky, Thatcher & Boeger 1986KC-L22
| | | `--C. trachydorasi (Acosta, Scholz et al. 2017) [=*Paracosmetocleithrum trachydorasi]KC-L22
| | `--Demidospermus Suriano 1983KC-L22
| | |--D. prolixus Franceschini, Zago et al. 2017KC-L22
| | `--+--D. anus Suriano 1983KC-L22
| | `--D. rhinelepisi Acosta, Scholz et al. 2017KC-L22
| `--+--‘Demidospermus’ mortenthaleri Mendoza-Palermo, Scholz et al. 2012KC-L22
| |--Nanayella Acosta, Mendoza-Palmero et al. 2019KC-L22
| | |--N. amplofalcis Acosta, Mendoza-Palmero et al. 2019KC-L22
| | `--+--N. aculeatrium Acosta, Mendoza-Palmero et al. 2019KC-L22
| | `--N. fluctuatrium Acosta, Mendoza-Palmero et al. 2019KC-L22
| `--Boegeriella Mendoza-Palmero & Hsiao 2020KC-L22
| |--B. conica (Mendoza-Palmero, Mendoza-Franco et al. 2019)KC-L22
| `--B. ophiocirrus (Mendoza-Palmero, Mendoza-Franco et al. 2019)KC-L22
`--Dactylogyrinae [Heteronchocleidinae, Pseudodactylogyrinae]KC-L22
| i. s.: NeodactylogyrusD56
|--Characidotrema Paperna & Thurston 1968KC-L22
| |--C. nursei Ergens 1973KC-L22
| `--C. vespertilio Kičinjaová & Řehulková 2019KC-L22
`--+--Kapentagyrus Kmentová, Gelnar & Vanhove 2018KC-L22
| |--K. limnotrissae (Paperna 1973)KC-L22
| `--K. tanganicanus Kmentová, Gelnar & Vanhove 2018KC-L22
`--+--DactylogyrusKC-L22
|--+--+--+--Pseudodactylogyrus Gusev 1965KC-L22
| | | | |--P. anguillae (Yin & Sproston 1948)KC-L22
| | | | `--P. bini (Kikuchi 1929)KC-L22
| | | `--+--‘Ancyrocephalus’ mogurndae (Yamaguti 1940)KC-L22
| | | `--Gobioecetes Ogawa & Ito 2017KC-L22
| | | |--G. biwaensis Ogawa & Ito 2017KC-L22
| | | `--G. longibasis Nitta & Nagasawa 2020KC-L22
| | `--+--Trianchoratus Price & Berry 1966KC-L22
| | | `--T. gussevi Lim 1986KC-L22
| | `--+--Eutrianchoratus Paperna 1969KC-L22
| | | `--E. cleithrium Lim 1989KC-L22
| | `--Heteronchocleidus Bychowsky 1957KC-L22
| | `--*H. buschkieli Bychowsky 1957KC-L22
| `--+--Tetrancistrum Goto & Kikuchi 1917D56
| | |--T. indicum (Paperna 1972)KC-L22
| | `--T. labyrinthus Al Jufaili & Palm 2017KC-L22
| `--+--+--Thylacicleidus Wheeler & Klassen 1988KC-L22
| | `--Haliotrema Johnston & Tiegs 1922KC-L22, D56
| | |--H. angelopterum Plaisance, Bouamer & Morand 2004KC-L22
| | `--H. scyphovagina Yamaguti 1968KC-L22
| `--+--‘Haliotrema’ chenhsintaoi Zhang 2001KC-L22
| `--+--+--+--Pseudohaliotrema Yamaguti 1953KC=L22
| | | | `--P. sphincteroporus Yamaguti 1953KC-L22
| | | `--Glyphidohaptor Kritsky, Galli & Yang 2007KC-L22
| | | `--G. safiensis Al Jufaili, Machkevsky et al. 2020KC-L22
| | `--+--Parancyrocephaloides Yamaguti 1938KC-L22
| | | `--P. daicoci Yamaguti 1938KC-L22
| | |--‘Haliotrema’ cromileptis Young 1968KC-L22
| | `--‘Haliotrema’ susanae Soo 2018KC-L22
| `--+--+--‘Haliotrema’ bilobatus (Yamaguti 1953)KC-L22
| | `--‘Haliotrema’ magnihamus Bychowsky & Nagibina 1970KC-L22
| `--+--Lethrinitrema Lim & Justine 2011KC-L22
| | |--L. grossecurvitubum (Li & Chen 2005)KC-L22
| | `--L. nebulosum Sun, Li & Yang 2018KC-L22
| |--Platycephalotrema Kritsky & Nitta 2019KC-L22
| | |--P. macassarense (Yamaguti 1963) [=Haliotrema macassarense]KC-L22
| | `--+--‘Haliotrema’ johnstoni Bychowsky & Nagibina 1970KC-L22
| | `--P. platycephali (Yin & Sproston 1948) [=Haliotrema platycephali]KC-L22
| `--Bravohollisia Bychowsky & Nagibina 1970KC-L22
| | i. s.: *B. magna Bychowsky & Nagibina 1970KC-L22
| |--B. plectorhynchus Li, Zhang et al. 2005KC-L22
| `--+--B. tecta Bychowsky & Nagibina 1970KC-L22
| `--+--B. maculatus (Venkatanarasaiah 1984)KC-L22
| `--Caballeria Bychowsky & Nagibina 1970KC-L22
| |--*C. pedunculata Bychowsky & Nagibina 1970KC-L22
| `--C. intermedius Lim 1995KC-L22
`--+--Xenoligophoroides Dmitrieva, Sanna et al. 2018KC-L22
| `--X. cobitis (Ergens 1963)KC-L22
|--+--Mexicana Caballero & Bravo-Hollis 1959KC-L22
| | `--M. rubra Camargo, Luque & Santos 2017KC-L22
| `--Haliotrematoides Kritsky, Yang & Sun 2009KC-L22
| |--+--H. guttati (García-Vargas, Fajer-Ávila & Lamothe-Argumedo 2008)KC-L22
| | `--H. plectridium Kritsky & Mendoza-Franco 2009KC-L22
| `--H. spinatus Kritsky & Mendoza-Franco 2009KC-L22
|--+--Enterogyrus Paperna 1963KC-L22
| | |--E. coronatus Pariselle, Lambert & Euzet 1991KC-L22
| | `--E. malmbergi Bilong Bilong 1988KC-L22
| `--+--Paradiplectanotrema Gerasev, Gayevskaya & Kovaleva 1987KC-L22
| | `--P. klimpeli Theisen, Palm et al. 2018KC-L22
| `--Pseudempleurosoma Yamaguti 1965KC-L22
| `--P. haywardi Theisen, Palm et al. 2017KC-L22
|--+--Euryhaliotrema Kritsky & Boeger 2002KC-L22
| | | i. s.: *E. chaoi Kritsky & Boeger 2002KC-L22
| | |--E. mehen (Solar-Jiménez, Garcia-Gasca & Fajer-Ávila 2012)KC-L22
| | |--E. pirulum (Plaisance & Kritsky 2004)KC-L22
| | `--+--E. johnii Triparthi 1959KC-L22
| | `--E. spirotubiforum (Zhang in Zhang, Yang & Liu 2001)KC-L22
| `--Sciadicleithrum Kritsky, Thatcher & Boeger 1989KC-L22
| |--*S. uncinatum Kritsky, Thatcher & Boeger 1989KC-L22
| |--S. bravohollisae Kritsky, Vidal-Martínez & Rodríguez-Canul 1994KC-L22
| `--S. meekii Mendoza-Franco, Scholz & Vidal-Martínez 1997KC-L22
|--Cichlidogyrus Paperna 1960KC-L22
| |--C. pouyaudi Pariselle & Euzet 1994KC-L22
| `--+--C. halli (Price & Kirk 1967)KC-L22
| `--+--C. arthracanthus Paperna 1960KC-L22
| |--C. zambezensis Douëllou 1993KC-L22
| |--+--C. attenboroughi Kmentová, Gelnar et al. 2016KC-L22
| | `--C. sclerosus Paperna & Thurston 1969KC-L22
| `--Scutogyrus Pariselle & Euzet 1995KC-L22
| |--S. longicornis (Paperna & Thurston 1969)KC-L22
| `--S. vanhovei Pariselle, Bitja Nyom & Bilong Bilong 2013KC-L22
`--+--+--Gussevia Kohn & Paperna 1964KC-L22
| | `--G. asota Kritsky, Thatcher & Boeger 1989KC-L22
| `--Parasciadicleithrum Mendoza-Palmero, Blasco-Costa et al. 2017KC-L22
| `--P. octofasciatum Mendoza-Palmero, Blasco-Costa et al. 2017KC-L22
|--Onchobdella Paperna 1968KC-L22
| |--O. aframae Paperna 1968KC-L22
| `--O. bopeleti Bilong Bilong & Euzet 1995KC-L22
|--+--Ergenstrema Paperna 1964KC-L22
| | `--E. mugilis Paperna 1964KC-L22
| `--Ligophorus Euzet & Suriano 1977KC-L22
| |--L. imitans Euzet & Suriano 1977KC-L22
| `--+--L. leporinus (Zhang & Ji 1981)KC-L22
| `--L. vanbenedenii (Parona & Perugia 1890)KC-L22
`--+--Metahaliotrema Yamaguti 1953KC-L22
| |--M. scatophagi Yamaguti 1953KC-L22
| `--+--M. digyroides (Zhang in Zhang, Yang & Liu 2001)KC-L22
| `--M. subancistroides (Zhang in Zhang, Yang & Liu 2001)KC-L22
`--Protogyrodactylus Johnston & Tiegs 1922KC-L22
|--P. alienus Bychowsky & Nagibina 1974KC-L22
`--P. hainanensis Pan, Ding & Zhang 1995KC-L22

*Ancyrocephalus paradoxus Creplin 1839 [incl. Dactylogyrus unguiculatus Wagener 1857, Tetraonchus unguiculatus]D56

Cosmetocleithrum Kritsky, Thatcher & Boeger 1986 [incl. Paracosmetocleithrum Acosta, Scholz et al. 2017]KC-L22

Dactylogyridae [Ancylodiscoididae, Ancyrocephalidae, Heteronchocleididae, Protogyrodactylidae, Pseudodactylogyridae, Urogyridae]

*Type species of generic name indicated

References

[C02] Collette, B. B. 2002. Needlefishes. Family Belonidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 287–289. Smithsonian Institute Press: Washington.

[D56] Dawes, B. 1956. The Trematoda with special reference to British and other European forms. University Press: Cambridge.

[KC-L22] Kmentová, N., A. J. Cruz-Laufer, A. Pariselle, K. Smeets, T. Artois & M. P. M. Vanhove. 2022. Dactylogyridae 2022: a meta-analysis of phylogenetic studies and generic diagnoses of parasitic flatworms using published genetic and morphological data. International Journal for Parasitology 52: 427–457.

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