Acanthocephalans have diversified into approximately 1,100 species that use fish as their primary hosts where they mature to adulthood and sexually reproduce, yet they are freely communicated to piscivorous amphibians, birds, mammals, and reptiles. Acute teleostean infestations rarely cause intestinal occlusions, yet these worms remain ubiquitous in aquatic environments including reefs (Pennell & Barton 1996; Pichelin & Cribb 2001; Cortés 2009; Shih et al. 2010; Bergen 2019; Costa Fernandes et al. 2019).

The phylum Acanthocephala comprises macroscopic multicellular endoparasitic worms, where several are nested in the class Eoacanthocephala, the order Neoechinorhynchida, and the family and subfamily Neoechinorhynchidae (Amin 2001; WoRMS 2020h). With affiliates ranked in the classes Archiacanthocephala and Palaeacanthocephala, they share ancestral lineage with organisms of the class Eurotatoria and subclass Bdelloidea and are therefore specialized rotifers (Garey et al. 1996; Near 2002; Shimek 2006). Phylogeny of this kind helps parasitologist select efficacious remedies.

Their anatomy comprises a trunk or metasoma with an anterior presoma armed with a barbed eversible proboscis enveloped in a sheath (Uzal et al. 2016; McAllister 2018; Alberta 2020). Their trunks are adorned with dermal plaques (Amin et al. 2011), whilst their probosces are used to snag intestinal lumens (Uzal et al. 2016; Alberta 2020). Acanthocephalans are pseudocoelomates insomuch as their organs move freely between the gut and body wall, whereas some contain two giant nuclei (Amin et al. 1993; Alberta 2020). Worms are gonochoric with free-floating gonads, yet their genital pores remain at their rear. A muscular neck adjoins their metasoma to their presoma (Fig 3.; Alberta 2020), whereas their lineages are discerned by the enumeration and distribution of their proboscis spines and comparative sequence analyses of their 18 svedberg (18S) ribosomal ribonucleic acid (rRNA; García-Varela et al. 2000).

Fig 2. A low-magnification acanthocephalan-featuring micrograph of a cross-section of tissue from an icefish (Chaenocephalus aceratus). Contains public sector information licensed under the Open Government License (OGL) v3.0. Consult bibliography.

Each worm’s integument is made up of a crisscross network of channels called lacunae fashioned from their multinucleated cells with walls that adhere to two vesicles that unite the trunk with their proboscis sheath or lemniscus. Fluid translocation is conceivably expedited by lacunae (Fig 1.; Fig 3.; Beermann et al. 1974; García-Varela et al. 2000; Alberta 2020) that assists absorption of their food insofar as acanthocephalans neither have a mouth nor a gut (Uzal et al. 2016; Divers & Stahl 2019; Alberta 2020).

Taxonomy

The tentative ancestries of thorny-headed worms are beset with instability and flux, which are disparities emphasized by their distribution in tropical and subtropical environments. Refer to bracketed orders and families.

Taxonomically-Informing Tropical and Subtropical Occurrences

Vietnamese reef fish of the families Belonidae, Clupeidae, Megalopidae, Mugilidae, and Sciaenidae were parasitized by Neoechinorhynchus (subgenus: Neoechinorhynchus) ascus (Neoechinorhynchida: Neoechinorhynchidae), N. (N.) johnii, N. (N.) longinucleatus, N. (N.) manubriensis, N. (N.) pennahia, N. (N.) plaquensis, and N. ampullata whose ancestries were delineated by phenotypic disparities in proboscis armory, vaginal architecture, and their lemnisci’s nuclear diameters (Amin et al. 2011).

Electron and brightfield microscopy combined with genetic analyses were used to survey Taiwan’s teleosts where Neoechinorhynchus (Neoechinorhynchus) agilis were found in grey mullet (Mugil cephalus), species of the same genus were parasitizing rabbitfish (Siganus fuscescens), and Rhadinorhynchus pristis (Palaeacanthocephala: Rhadinorhynchidae) resided in the gut of spotted mackerel (Scomber australasicus; Shih et al. 2010).

32 percent of 24 kinds of Australian flatfish were infected with adult Serrasentis sagittifer (Palaeacanthocephala: Isthmosacanthidae), species of Gorgorhynchoides and Rhadinorhynchus (Rhadinorhynchidae), and fully matured cystacanths of Corynosoma cetaceum (Polymorphidae) where the former were found in 18 species (Barton & Smales 2015).

The families Diplosentidae and Cavisomatidae were previously synonymized, whereas novel Transvenidae includes worms with two cement glands. Transvena annulospinosa were isolated from The Great Barrier Reef’s (GBR’s) Labridae: barred thicklip wrasse (Hemigymnus fasciatus), black backed wrasse (Anampses neoguinaicus), blackeye thicklip wrasse (H. melapterus), blue-spotted wrasse (A. caeruleopunctatus), and geographic wrasse (A. geographicus). The nascent genus Trajectura was proposed for T. perinsolens isolated from Australia’s Anampses neoguinaicus, whilst Diplosentis ikedai was absorbed as Trajectura ikedai. The genus Pararhadinorhynchus was ranked within Transvenidae which assimilated Diplosentis manteri as the “uncertain” species, Pararhadinorhynchus manteri (Pichelin & Cribb 2001).

Fig 3. A thorny-headed worm’s proboscis retracted by orange muscles.

Fig 4. A photograph of Acanthocephala.

A study in Brazil isolated the novel species, Filisoma caudatum (Cavisomatidae) from Indo-Pacific chub of the genus Kyphosus, whose findings were redolent of a requirement for extensive revision of the family Echinorhynchidae (Costa Fernandes et al. 2019). Notwithstanding, the World Register of Marine Species (WoRMS; https://www.MarineSpecies.org) and the National Centre for Biotechnology Information’s (NCBI’s) taxonomy browser “root” (https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/), upheld the family unaltered in 2022.

Acanthocephalans are likely widespread amongst reef ornamentals, hence support retailers that openly declare they use chemotherapeutics to control communicable disease. Natural ways of attenuating illness inspire warm fuzzy feelings, but no matter how powerful the sentiment, they will not stop a virulent pathogen from ravaging and decimating an entire facility of sensitive animals.

Clinical Signs: Aquaculture

Mild infections remain subclinical and thus aquarists are unable to tell which animals are infected. Maricultured fish are overcrowded, frequently processed and handled, and exposed to numerous blooms of macro- and micro-scopic pathogens. The infested will lack mucus and suffer growth inhibition, muscle atrophy, and emaciation (cachexia). The trunks of dull, dry skinned fish become knife-like whilst their heads seem disproportionately large (Jithendran & Kannappan 2010; Sanil et al. 2011; Gomes et al. 2017).

Undertake postmortems but thorny-headed worms rarely prove fatal, whereas the images herein and in the literature will prove invaluable for tentative diagnoses. Transfer teleosts exhibiting mild symptoms to robustly-mature fish-only quarantine and maintain 2.2 mg l^-1 of flubendazole. Insults of the alimentary canal are typically slow to recuperate and thus mitigation may take two to three months, yet fish may be infected with other therapeutic-susceptible endoparasites and as such, may respond well.

Fig 5. A low magnification micrograph of a vessel cross-section from an icefish (Chaenocephalus aceratus) with a lumen-constrained acanthocephalan. Contains public sector information licensed under the Open Government License (OGL) v3.0. Consult bibliography.

Reproduction and Life Cycle

The male has two testes that comprise vas deferens which supply the penis or an eversible copulatory organ called the bursa, where males clasp females during sexual congress and deposit sperm into their vaginas. Penises are manipulated by a muscular vesicle called the Saefftigen’s pouch, whereafter vaginas are sealed with a paternity-assuring plug of tanned protein cement (Fig 6.; Margulis & Chapman 2009; McAllister 2018; Alberta 2020).

The genitalia of juvenile females are contained in ligamentous sacs that degrade. Ovaries are divided into ovarian balls consisting of numerous free-floating unfertilized embryonated oocytes called acanthors, which become ellipsoidal post-fertilization. As the eggs drift, they recirculate through the uterine bell and selector apparatus, which returns those that are underdeveloped to the body whilst the ripened are directed to the uterus (Margulis & Chapman 2009; Paladini et al. 2017; Alberta 2020).

Cystacanths emerge from teleost-ingested arthropods and embed into the intestinal lumen or peritoneum, where they mature into adults, sexually reproduce, and shed developed acanthors, which are defecated environmentally to remain contagious in mud and sediment for years (Jithendran & Kannappan 2010; Alberta 2018; McAllister 2018). Acanthors are eaten by intermediate hosts like arthropods of the orders Amphipoda, Copepoda, Isopoda, and Ostracoda (McAllister 2018) where they transform into acanthellae that migrate into tissues, encyst, and after a time, develop into contagious cystacanths with differentiated organs and probosces (Figs 7. to 8.). A minimum period of development is required before they can instigate viable infections, so noninfective arthropods either carry immature cystacanths or have yet to forage acanthors (McAllister 2018). The life cycle progresses when an intermediate crustacean is consumed by a primary teleost (Margulis & Chapman 2009; Paladini et al. 2017; Alberta 2020).

The photophobia of amphipods helps them avoid predation, albeit remarkably, arthropods infected with cystacanths become positively phototaxic (Bethel & Holmes 1973). Parasite-motivated behavioral modification is known as “manipulation” (Murdock et al. 2017).

Control

Acanthocephalans are vulnerable to the flat- and tape-worm remedies praziquantel and flubendazole (Weber & Junge 2000; Zuskova et al. 2018). Praziquantel breaches the integuments of parasites and alters the permeability of their calcium ion (Ca²⁺) channels  which  initiates  detachment  (Park  et  al.  2019),  whereas flubendazole binds the tubulin of the eukaryotic intracellular scaffold which prevents glucose absorption and thus parasites cannot feed (Kuhlmann et al. 2017). Neither chemotherapeutic is safe for reefs, which places the onus firmly on the retailer whilst their use is likely governed by national legislation.

Fig 7. Left – a micrograph of acanthocephalan cystacanths.

Praziquantel may detach the worms from the gut which may be excreted, yet they will likely remain contagious (Zuskova et al. 2018). Medicated fish-only systems are devoid of crustaceans; however, endoparasites are somewhat shielded from chemotherapeutics, hence praziquantel-based chemotherapy may leave worms unexposed. Nevertheless, maintaining flubendazole concentrations between 1.5 and 2.2 mg l^-1, will expose the worms through teleostean drinking, because continuous seawater ingestion is vital for the osmoregulation of marine finfish.

References

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Continued after figure 8.

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