Cyamidae

The term “whale lice” is a misnomer as these are in fact crustaceans, with most cyamids being dorsoventrally flattened and unable to swim, relying on direct contact for transmission from one host to another. They have a rudimentary pleon with the posterior three pairs of legs enlarged and adapted to cling onto their host. Cyamids are known to attach to whales, dolphins and porpoises (Martínez et al. 2008), where they can be highly host specific, and more than one species can be found on one host at a time.

The first cyamid described was Cyamus ceti (Linnaeus, 1758) (originally as Oniscus ceti since the genus Cyamus was described by Latreille in 1796), and a number of new species were discovered in the 1800s. Christian Frederik Lütken (Fig. 2.1b) described seven new Cyamus species as well as the genus, Platycyamus Lütken, 1870, all of which were incorporated into the first cyamid monograph (Lütken 1873). Lütken, a Danish zoologist, worked on a number of aquatic groups including corals, jellyfish, crustaceans and annelids, but his passion lay with echinoderms and fishes, and thus only a few of his papers were dedicated to cyamids. Although cyamids were known in many parts of the world, between 1888 and 1931, no new cyamid species were described.

In 1967, Yuk-Maan Leung provided the first illustrated key for the cyamids along with a guide to the literature (Leung 1967). Leung also described the first life cycle of a cyamid (Cyamus scammoni Dall, 1872 on the grey whale) which provided valuable information on the reproductive behaviour of these parasites (Leung 1976). Around the same time, Hans-Eckhard Gruner (Fig. 2.1c) completed a comprehensive catalogue of the Cyamidae (Gruner 1975). Gruner contributed to the taxonomy of amphipods and isopods and was best known for his Lehrbuch der Speziellen Zoologie (Textbook on Special Zoology) published in 1980. A few years later, in 1999, Joel Martin and John Heyning provided an updated key and checklist for these parasites, which proved helpful in subsequent studies (Martin and Heyning 1999).

As cyamids are permanently attached to constantly moving cetaceans, in-depth studies on the parasites have been difficult; however, despite these challenges, many scientists have been able to report on their ecology. Juan Antonio Balbuena and Juan Antonio Raga published many papers on parasites of marine mammals and discussed the ecology and host relationships of whale lice on pilot whales (Balbuena and Raga 1991). Furthermore, Victoria Rowntree, an American whale researcher, has noted many behavioural aspects of these amphipods (on right whales in particular). Cyamids are known to aggregate in areas where there is the least amount of stress (out of the main water flow areas), such as the skin folds on the head, eyes, flippers, blowholes, lip margins, around barnacles and callosities (Leung 1970a, b; Rowntree 1996). The abundance of the cyamids on their host is inversely proportional to the host’s swimming speed, with slower whales having several thousand on a single host and faster-swimming dolphins having fewer (Goater et al. 2014). The mouthparts of the cyamids are highly modified, with setae and short spines on the maxillae, maxillules and mandibles, for excavating and eating host skin. Rowntree (1996) confirmed that these ectoparasites eat whale skin containing pigments (seen in the intestines of the amphipods), and shortly thereafter Schell et al. (2000) confirmed this diet with the aid of stable carbon and nitrogen isotopes. More recently, Rowntree and colleagues have used genetic sequence variation in the whale lice of right whales in order to determine population histories (Kaliszewska et al. 2005).

Carl J. Pfeiffer, researcher of marine mammals, and his colleagues provided additional information on the anatomy of cyamids (marsupium, eggs, juveniles and cuticle) (Pfeiffer and Viers 1998), as well as on the ocular musculature (Levin and Pfeiffer 1999). Pfeiffer also completely revised the whale lice in a chapter dedicated to the crustaceans in the published book Encyclopaedia of Marine Mammals (Pfeiffer 2002).

Alan A. Myers and James K. Lowry, amphipod specialists from Ireland and Australia, respectively, also presented a new classification for the suborder Corophiidea (see Myers and Lowry 2003). However, most of the amphipod higher-level classification and phylogenetic relationships are still not agreed upon, with preliminary molecular work and the previously proposed relationships not being consistent (Väinölä et al. 2008). More recently, Myers and Lowry revised the amphipod classification, established a new suborder Senticaudata (including the Cyamidae), and introduced the level parvorder between infraorder and superfamily, a first for amphipod taxonomy (Lowry and Myers 2013). The family Cyamidae currently has 32 recorded species from six genera.

Hyperiidea

Parasitic amphipods, in the suborder Hyperiidea, have a large cephalothorax and eyes and are exclusively marine (mostly pelagic). These crustaceans live associated with other zooplankton where they may be parasitic or commensals on organisms such as jellyfish, ctenophores, molluscs and tunicates. The association of a hyperiid and gelatinous zooplankton is considered parasitic if the amphipod is within the tissue of the host for nutritional purposes (host tissue can be seen in the amphipod stomach contents after feeding) (de Lima and Valentin 2001).

The first three species of Hyperiidea were described in 1775. Johan Christian Fabricius (Fig. 2.1d) (a Danish zoologist) described two of these species, namely, Cystisoma spinosum (Fabricius, 1775) (nomen dubium) and Scina crassicornis (Fabricius, 1775). The third species, Phronima sedentaria (Forskål, 1775), was described by the Swedish researcher, Peter Forskål. Interestingly, both these men were students of Linnaeus at some point. Although these three species were the first named hyperiids, there was an earlier record in 1762 by H. Strøm of a hyperiid in association with a host, where Hyperia medusarum (Müller, 1776) was located inside a large jellyfish (Harbison et al. 1977).

Many of the early systematic monographs on these parasites were completed by the Swedish biologist Carl Erik Alexander Bovallius (1887a, b, c, 1889, 1890) (Fig. 2.1e) and the German zoologist Carl Friedrich Wilhelm Claus (1879a, b) (Fig. 2.1f). Thomas Elliot Bowman (an American carcinologist) (Fig. 2.1g) and Hans-Eckhard Gruner thoroughly reviewed the families and genera of Hyperiidea in 1973 (Bowman and Gruner 1973). This review became the foundation for all other systematic work on these amphipods. Not only did it focus on identifying the large collection of hyperiid Amphipoda sampled during the Dana Expedition (1928–1930), but it also included a detailed section on their morphology and ecology.

George “Richard” Harbison (Fig. 2.1h) noted that although other researchers had mentioned the parasitic mode of life, little research had been done on the life histories and host specificities of the parasitic amphipods. Using SCUBA to collect live material, Harbison and colleagues were able to observe a number of associations between the amphipods and their hosts that had never been noted before (Harbison et al. 1977; Madin and Harbison 1977). Many observations of living hyperiids were also made by Philippe Laval (from 1963 until he retired in 2004) (Fig. 2.1i). Laval was one of the first researchers to recognise that all hyperiids have a parasitic way of life (noted in his doctoral thesis in 1974), which was later confirmed by Harbison et al. (1977) and published (amongst others) an extensive paper on these parasites associated with gelatinous zooplankton (Laval 1980).

More recently, Wolfgang Zeidler (Fig. 2.2a), formerly working at the South Australian Museum, revised the taxonomy of the Hyperiidea (Zeidler 2003a, b, 2004a, b, 2006, 2009, 2012, 2015; Zeidler and De Broyer 2009). These extensive reviews included assessments of the systematic relationships between the genera as well as keys for the families, genera and species, drawings of the species and diagnoses for the different taxa. Hyperiidea has 283 accepted species and 76 genera of which Zeidler has described 12 families, 5 genera and 23 species.

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Fig. 2.2

(a) Wolfgang Zeidler, (b) Elsie Wilkins Sexton (on the right), (c) Jerry Laurens Barnard, (d) Henri Milne Edwards, (e) Jörgen Matthias Christian Schioedte, (f) Frederik Vilhelm August Meinert, (g) Harriet Richardson, (h) Thomas Roscoe Rede Stebbing, (i) Edward John Miers. Image (b) from Spooner (1960); image (c) from Thomas (1992); images (d), (e) and (h) © Wikipedia Commons public domain; image (f) from Truesdale (1993); image (g) from Damkaer (2000); image (i) from Gordon (1971)

Bopyridae

Members of this family are parasitic on other crustaceans, especially crabs and shrimps. To date, there are 10 subfamilies, 167 genera, 607 species and 12 subspecies. These parasitic isopods are usually found within the branchial chamber of their hosts causing a noticeable protuberance, but there are several species that attach to the host’s abdomen. The first described bopyrid was Bopyrus squillarum Latreille, 1802 from the Baltic prawn. This species inhabits the gill chamber of Palaemon adspersus Rathke, 1837.

French zoologists, Alfred Mathieu Giard (Fig. 2.3c) and Jules Bonnier (Fig. 2.3d), described 70 epicaridean isopod species together (38 of which were bopyrids). Bonnier proceeded to describe another 31 bopyrid species thereafter, although only six remain valid today. Bonnier started his zoological career after meeting Giard and was his student for nearly 30 years. In his 1900 review of the bopyrids, Bonnier named a species after Giard, Bopyrina giardi Bonnier, 1900, but it has since been synonymised with Bopyrina ocellata (Czerniavsky, 1868). Furthermore, the infectious protozoan parasite genus Giardia Künstler, 1882, was named in honour of Giard for providing the first description of Giardia lamblia (Lambl, 1859) Kofoid & Christiansen, 1915. Sadly, both men passed away in 1908, Giard on his 62nd birthday and Bonnier at 49 years of age from a brain disease he contracted while on a trip in 1904.

Another duo that published 36 genera and 146 nominal isopod species together are Hugo Frederik Nierstrasz (Fig. 2.3e) and Geraldo Abraham Brender à Brandis (90 still valid) (Fig. 2.3f). Of these, 23 genera and 80 species are still valid bopyrid taxa. Nierstrasz was a Dutch zoologist who summarised the isopod knowledge at that time in his contributions to the Siboga Expedition (1923–1941), which took place from March 1899 to February 1900 in the Indonesian Archipelago (Nierstrasz and Brender à Brandis 1923; Nierstrasz 1931). Brender à Brandis was a Dutch artist, and it can reasonably be inferred that he was the illustrator for the bopyrid drawings in these joint publications.

Christopher B. Boyko (Fig. 2.3g) (with more than 100 publications) is one of the world leading bopyrid specialists publishing in the present era. Boyko and Jason D. Williams (Fig. 2.3h) (both American researchers) have made valuable contributions on these isopods including a review of the global diversity of the epicarideans (Williams and Boyko 2012). This publication provided a thorough overview of the bopyrids and cryptoniscoids including phylogeny and historic patterns, human-related issues, feeding biology and impacts on the hosts as well as biogeography and biodiversity of these isopods. Furthermore, these authors have detailed the methods for detection, collection and preservation of epicaridean parasitic isopods (Boyko and Williams 2016) and presented a new classification based on a molecular phylogenetic analysis (Boyko et al. 2013).

John C. Markham (Fig. 2.3i) has made substantial contributions to bopyrid knowledge describing 29 genera and 95 species of bopyrids. Other noteworthy publications include the evolution and zoogeography of the bopyrids (Markham 1986), revision of bopyrids from the north-western Atlantic Ocean (Markham 1988), Thailand (Markham 1985) as well as from Hong Kong and southern China (Markham 1982). Jianmei An (Fig. 2.4a) has also provided many valuable contributions on bopyrids. Many of these papers include reviews of the different genera, especially from China, as well as the description of new species (36 species) (An et al. 2009, 2015a, b).

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Fig. 2.4

(a) Jianmei An, (b) Vernon Everett Thatcher (on the right), (c) Jean-Paul Trilles, (d) Richard C. Brusca, (e) Ernest H. Williams Jr, (f) Lucy Bunkley-Williams, (g) Nico J. Smit, (h) Kerry A. Hadfield, (i) Gary Poore. Image (b) from Boeger (2011)

Cymothoidae

Cymothoid isopods are obligate parasites of both marine and freshwater fishes that show high variability and consequently have often been misidentified (Smit et al. 2014). These isopods are ectoparasites, found in all oceans but with the greatest diversity in tropical and subtropical waters, feeding on fish host blood or haemolymph and possibly muscle tissue and mucus. There are 369 known cymothoid species in 43 genera. As previously mentioned, the first described parasitic isopods were Aega psora, Anilocra physodes, Cymothoa oestrum and C. scopulorum, of which the last three species are valid cymothoid isopods. The first illustrations of a cymothoid, however, appeared many years later (Desmarest 1825).

Cymothoid research has often been confined to a particular geographical region where a practicing taxonomist was based or where research vessels were sampled. An example is Vernon Everett Thatcher (Fig. 2.4b), who published on cymothoids from a previously neglected area, South America freshwaters (Thatcher 1991, 2000). Thatcher described 15 new species from the region and produced papers on the mouthpart and pleopod morphology, comparing the morphology of the marine and freshwater cymothoids in some instances (Thatcher 1995, 1997).

Jean-Paul Trilles (Fig. 2.4c), a French parasitologist, has made notable contributions to the Cymothoidae, including many redescriptions and comprehensive taxonomic synonymies. One of the most significant publications on cymothoids is his Prodromus, an extensive catalogue of the cymothoids that provided an invaluable resource for subsequent workers on this family (Trilles 1994). Several other publications were on museum holdings as well as the description of new cymothoid species (see Trilles 1972, 1977, 2008).

The invertebrate zoologist, Richard C. Brusca (Fig. 2.4d), published the first modern review and influential monograph of the Cymothoidae of the Eastern Pacific (Brusca 1981). This monograph included information on cymothoid morphology, taxonomy, history, zoogeography, phylogeny and the first hypothesis of the evolution of these parasites. It was published in the cladistic phylogeny era of Crustacea, and provided the foundation for all future work in this field, where it is still the point of comparison for all modern phylogenies. Brusca has published over 160 articles and 13 books including the largest-selling text on invertebrate zoology Invertebrates, co-authored with his brother Gary Brusca. Some of his other noteworthy works include field guides of isopods from Costa Rica (Brusca and Iverson 1985) and the phylogenetic analysis and classification of isopods (Brusca and Wilson 1991).

Ernest (Bert) H. Williams Jr (Fig. 2.4e) and Lucy Bunkley-Williams (Fig. 2.4f) (a husband and wife team from Puerto Rico) have made significant contributions to knowledge of the Cymothoidae from the Caribbean, Japan and Thailand. This couple described 27 new species, corrected many errors in literature, and provided several noteworthy ecological notes for these isopods (Williams et al. 1982; Williams and Bunkley Williams 1986, 2000; Bunkley-Williams and Williams 1998). Other contributors to the biodiversity and taxonomy of cymothoids include V. V. Avdeev (a Russian researcher) who described 15 cymothoid species, Pieter Bleeker (a Dutch medical doctor, ichthyologist and herpetologist) who described 13 species, and N. Krishna Pillai (an Indian carcinologist) who described nine cymothoid species.

Recently, Nico J. Smit (Fig. 2.4g), Niel L. Bruce (Fig. 2.3b) and Kerry A. Hadfield (Fig. 2.4h) reviewed the global diversity of the cymothoids (Smit et al. 2014). Within this review, they included historic, biogeographic, systematic, taxonomic, reproductive and ecological information for these isopods. These three authors have also completed a number of taxonomic revisions of several genera from southern Africa (Hadfield et al. 2010, 2013, 2014, 2015; Hadfield and Smit 2017), including the description of several new species. Trilles (1994) mentioned there was a lack of information from the Southern Hemisphere, and specifically South Africa and South America, and these papers aimed at addressing this knowledge gap. Furthermore, these authors produced a publication on revising poorly known type material to minimise potential future misidentifications within one of the more complicated genera, Ceratothoa Dana, 1852 (Hadfield et al. 2016).

Acrothoracica

This superorder of barnacles is only partially parasitic. These tiny barnacles, called burrowing barnacles, burrow into calcareous substrates such as mollusc and thoracican barnacle shells. Within the family Trypetesidae, there are two genera, Tomlinsonia Turquier, 1985 (with two known species), and Trypetesa Norman, 1903 (five known species), which are found exclusively inhabiting the shells of hermit crabs (Williams et al. 2011).

Trypetesa lampas (Hancock, 1849) was the first burrowing barnacle described, with Hancock discovering it in the shells of gastropods that were inhabited by hermit crabs (Hancock 1849). Charles Darwin (Fig. 2.6a) noticed it was very similar to Cryptophialus Darwin, 1854 but placed into Alcippe Hancock, 1849 (now Trypetesa Norman, 1903) (see Darwin 1854). In 1872, Noll placed both Alcippe and Cryptophialus into Darwin’s order Abdominalia. In 1905, Gruvel realised that the cirri on the terminal body segments thought to be abdominal appendages (hence the order’s name) was in fact from the thorax, so the order was changed to Acrothoracica. Around the same time, Norman (1903) changed the genus name from Alcippe to Trypetesa, as the former name was preoccupied (homonym) by birds in the family Pellorneidae.

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Fig. 2.6

(a) Charles Darwin, (b) Jack T. Tomlinson, (c) Gregory Kolbasov, (d) Johann Friedrich Theodor (Fritz) Müller, (e) Hilbrand Boschma, (f) Sven Ludvig Lovén, (g) William Anderson Newman, (h) Geoffrey Allan Boxshall, (i) Rony Huys. Images (a), (d), (e) and (f) © Wikipedia Commons public domain; image (b) from public obituary at www.oakdaleleader.com/obituaries/jack-tomlinson

Jack Tomlinson (Fig. 2.6b), who was recognised as one of the world authorities of this group, revised the burrowing barnacles known at that time, including information on all of the different systems, taxonomy and ecology (Tomlinson 1969, 1987). More recently there have been many studies on the larvae as well as phylogeny and systematics of this group by Gregory Kolbasov (Fig. 2.6c) and colleagues (Kolbasov 2002, 2009; Kolbasov et al. 2014), as well as the phylogenetic relationships of the different barnacle orders (Lin et al. 2016). However, the data on the ecology of these barnacles, especially on the Trypetesidae, are scanty.

In 2011, the first publication of egg predation by a burrowing barnacle was recorded (Williams et al. 2011). Trypetesa lampas, removed from ovigerous female hosts, were found to contain hermit crab eggs, chorions, as well as yolk in their gut. There is still uncertainty surrounding how these barnacles feed, but this research documented how they can have significant negative effects on hermit crab reproduction. Other studies have showed blue-green algae-like particles in the gut of Trypetesa lampas (see Kamens 1981), and it may be that barnacles in male hermit crabs filter feed on particles from the water, whereas barnacles in females feed on the hermit crab eggs (Williams et al. 2011). Murphy and Williams (2013) verified this study and suggested that the more accurate term for these barnacles may be “transient parasites” as they can be harmful in some cases but cause no harmful impact in other cases. Larsen et al. (2016) added that the barnacles do not rely on the egg predation to any substantial degree and found much of the data they collected on prevalence, load, reproductive cycles, and host relationships differed from previous studies. This highlighted the fact that there is still a lot of work to be done on these barnacles before we fully understand their ecology.

Rhizocephala

This order contains the obligate parasites and was first discovered by Cavolini (1787) but only grouped together as Rhizocephala by the German zoologist, Johann Friedrich Theodor (Fritz) Müller (Fig. 2.6d) in 1862 (Müller 1862). They are endoparasites of other crustaceans, especially decapods. Currently there are 2 orders, 11 families, 41 genera and 288 species known. The adult females have lost most of the traits usually associated with Crustacea and are also known to influence the morphology and biology of their hosts which sets them apart from other groups. These adult female parasitic barnacles consist of an “externa” (an external sac-like body for reproduction) and an “interna” (a root-like body inside the host for nutrient uptake), with the male inside the female externa, joined by a small stalk (Høeg 1995; Høeg and Lützen 1995). Many rhizocephalans are known to cause parasitic sterilisation or castration of their crustacean hosts. Depending on the species, these parasites can lower reproductive outputs, cause eggs to die within a few days or completely inhibit gonad processes required for reproduction (Høeg 1995). Along with the degeneration of the gonads, rhizocephalans can also cause feminisation of male hosts. This may include testes converting to ovaries, changes in the overall shape and size of the hosts and possibly even changing the behaviour of the host (Høeg 1995).

Rhizocephalans are divided into two orders: Akentrogonida and Kentrogonida (see Table 2.1). Whereas all kentrogonids exhibit similar characteristics (including the presence of the specialised female post-settlement stage, the kentrogon, as well as the equivalent male stage, the trichogon), all of the akentrogonids do not have similar characteristics other than the absence of the kentrogon (Walker 2001). Within the Kentrogonida is the family Sacculinidae, which is one of the more renowned groups of parasites due to their ability to cause parasitic sterilisation in crabs. The genus Sacculina Thompson, 1836, holds the majority of the rhizocephalan species with approximately 129 known species. The first described species was Sacculina carcini Thompson, 1836, making it one of the most studied barnacle parasites.

Hilbrand Boschma (Fig. 2.6e), a former director of the Rijksmuseum van Natuurlijke Historie (Naturalis), Leiden, Netherlands, had a particular interest in rhizocephalans. Boschma (and colleagues) described half of the currently recognised rhizocephalan species (2 families, 8 genera and 144 species). Most of these species are in the genus Sacculina, with 98 of the 128 known species named by Boschma. Some of his more substantial publications were on rhizocephalans from the North Atlantic (Boschma 1928), from the British Museum collections (Boschma 1933), as well as notes and new species from Sacculinidae (Boschma 1937, 1950, 1955).

Jens Thorvald Høeg (Fig. 2.5f) has also added numerous contributions on the ecology of these parasites. In 1991, Høeg reviewed the sexual system of the rhizocephalans and a year later added ultrastructure information regarding their morphology (Høeg 1992). He also completed taxonomic and phylogenetic studies with colleagues round the same time (Høeg and Rybakov 1992; Høeg and Lützen 1993), as well as revised the biology and life cycle of these barnacles (Høeg 1995).

Other contributors to this group include Olga Korn and colleagues, from the Russian Academy of Sciences, Moscow, who have published several papers on the larval development and ecology of the rhizocephalans (Kas’yanov et al. 1997; Korn et al. 2000; Kashenko et al. 2002) as well as reproductive studies on several species (Korn 1985, 1989; Korn et al. 2004). Bo Øksnebjerg, in his review of the Mediterranean and Black Sea rhizocephalans, provided a thorough summary of available information on the biology, ecology, biogeography and taxonomy of these parasites, including information for each of the 25 species known from the region at that time (Øksnebjerg 2000). Henrik Glenner, from the University of Bergen, has published many papers on barnacles and related crustacean groups too, most relating to the evolution and phylogenetic relationships of the parasitic barnacles (Glenner and Hebsgaard 2006; Glenner et al. 2010).

As rhizocephalans affect the reproductive systems of their hosts, it was proposed that these parasites could possibly aid in biological control of invasive host species. Murphy and Goggin (2000) analysed the genetic discrimination of sacculinid parasites to determine if they could control invasive European green crabs that have had a negative effect on the softshell clam fisheries in North America. Unfortunately, the parasite is not host specific, and it could spread if it were introduced as a control agent (Murphy and Goggin 2000). This was put to the test by Goddard et al. (2005). Four native North American crab species were infected with the European green crab’s natural parasite, Sacculina carcini Thompson, 1836. Although the parasite preferred the green crab, there were still a significant number of native crabs infected (all without producing a reproductive sac) which would result in the loss of many indigenous species.

Using both molecular and morphological techniques in classifying these parasitic barnacles has recently resulted in some interesting findings. A new genus, Polyascus Glenner, Lützen & Takahashi, 2003, was described after analyses on ten Sacculina species showed three asexually reproducing species formed a monophyletic clade and failed to support a monophyletic Sacculina clade (Glenner et al. 2003). Furthermore, in a different study using both techniques again, three species of Sacculina were found on a single host in a single locality for the first time (Tsuchida et al. 2006). Recent information on the phylogeny (using morphological characters and molecular data), from Høeg and Glenner and colleagues, can be seen in Chap. 10.1007/978-3-030-17385-2_9.

Cyclopoida

Cyclopoids have an abdomen that is narrower than the thorax, and the first antenna is of intermediate length (only half the length of the body). The first two cyclopoids were described by Carl Linnaeus (Fig. 2.1a), namely, Cyclops quadricornis quadricornis (Linnaeus, 1758) and Lernaea cyprinacea Linnaeus, 1758. Cyclops Müller, 1785, is one of the most common freshwater copepod genera with approximately 200 valid species. It belongs to the family Cyclopidae, which is the largest cyclopoid family with over 1100 valid species. Members of this family are predominantly free-living; however, several species are intermediate hosts for numerous pathogenic human and fish parasites such as Guinea worm (Dracunculus medinensis (Linnaeus, 1758)), as well as cestodes (tapeworms) and nematodes (round worms) (Piasecki et al. 2004). Recently, Eucyclops bathanalicola Boxshall & Strong, 2006 was described from Lake Tanganyika in a rare occurrence of a freshwater copepod parasitic on an invertebrate host (mantle cavity of Bathanalia straeleni Leloup, 1953). This association is also noteworthy as it also represents a unique account of a parasite in what is primarily a free-living family (Boxshall and Strong 2006).

The second cyclopoid species discovered by Linnaeus belongs to the genus Lernaea Linnaeus, 1758, a widely known genus of freshwater fish parasites, commonly referred to as anchor worms. Lernaea cyprinacea was originally described from Europe in 1745 under a trinomial name but was then redescribed by Linnaeus in 1758 (see Kabata 1979). Anchor worms burrow into the skin of its host fish and can cause a disease called lernaeosis where haemorrhagic ulcers occur at the attachment site. Death of the host can occur due to secondary infections and severe bleeding (Khalifa and Post 1976; Kabata 1985). This species has been recorded worldwide and is thought to have been spread through the movement of aquarium species (Innal and Oldewage 2012). The family Lernaeidae is probably one of the most studied cyclopoid groups due to its importance in aquaculture. Lernaea spp. have been reported to cause mass mortalities as early as 1880. According to Kocyłowski and Miączyński (1960), lernaeosis almost demolished an entire population of crucian carp in the Masurian Lake District (Poland) in 1880. An interesting case of catfish mortality due to gill damage (including epithelial hyperplasia, telangiectasis and haemorrhage) caused by Lernaea cyprinacea was also noted in Arkansas by Goodwin (1999). Bighead carp in the same tanks, with approximately the same number of copepods externally, did not die. Fish mortalities due to gill damage from Lernaea copepodids had never been reported before. This was most likely due to the polyculturing of the catfish with the bighead carp (an excellent host for Lernaea) and the filter-feeding apparatus of the carp preventing large infestations on their gill filaments.

Harpacticoida

This order includes mainly free-living copepods, although there are some symbiotic and parasitic species. One genus, Balaenophilus Aurivillius, 1879 (with three species), known to occur on the external surfaces of turtles, whales and manatees, appears to be both epibionts and parasites. Kazunari Ogawa and colleagues recorded the first copepod on a sea turtle and noticed the turtle’s skin inside the gut, which led the authors to the conclusion that the copepods feed on the turtle and not algae or diatoms (Ogawa et al. 1997). According to Badillo et al. (2007), there was definite evidence of Balaenophilus ingesting whale and sea turtle host tissue; however, the extent of this on the host is unknown. Mild signs of a tissue reaction was also observed in turtles with large numbers of copepods present at one time (>500). However, when Suárez-Morales et al. (2010) confirmed the presence of these copepods on manatees, they could not see any effect on the hosts. Healthy skin was observed at the site of attachment when Balaenophilus manatorum (Ortíz, Lalana & Torres, 1992) was removed, and no difference was seen in their reproduction or behaviour. Thus, their status as parasites remains unclear at this point.

The family Tisbidae contains free-living and symbiotic copepods as well as parasitic copepods. The parasitic species (many from the subfamily Cholidyinae) are usually found in the gills or on the external surfaces of octopuses (Humes and Voight 1997; Avdeev 2010). Juvenile Genesis vulcanoctopusi López-González, Bresciani & Huys, 2000, however, were located within the connective tissue of the octopod integument, indicating the possibility that these parasites may have both endo- and ectoparasitic phases (López-González et al. 2000). The first species described from this family was Tisbe furcata (Baird, 1837). Arthur Grover Humes listed specimens labelled as T. furcata from the mantle of Ocnus planci (Brandt, 1835), a sea cucumber (see Humes 1980); however, the identification was by Monticelli in 1892 and is doubtful. Massy (1909) first reported a copepod on a deep-sea octopus that was later described by Farran (1914) as Cholidya polypi Farran, 1914 (see Humes and Voight 1997).

Monstrilloida

Monstrilloids are only parasitic in the postnaupliar and preadult stages, with adults being free-swimming and non-feeding zooplankters. The endoparasitic forms are known to occur in polychaetes, molluscs and other invertebrates (Davis 1984; Huys et al. 2007). According to Mexican marine biologist and researcher, Eduardo Suárez-Morales (Fig. 2.7f) (2011), the first reported monstrilloid was from a Norwegian fjord in 1842 (Krøyer 1842). A single preadult specimen of Monstrilla typica (Krøyer, 1849) (originally named Thaumatoessa typica in the 1842 publication) was illustrated by Krøyer but without any description. This description was only provided in 1849 (with a slight alteration to the original name), along with the diagnosis of a new genus (Krøyer 1849). The monstrilloid naupliar stage was first described by Giesbrecht (1893), shortly followed by the drawings and descriptions of the nauplius and development of the endoparasites of Haemocera by Malaquin (1901). In 1994, Grygier re-examined the “Thaumatoessa (Thaumaleus) typica” type specimen in order to determine its identity and moved it into the genus Monstrilla Dana, 1849. Shortly thereafter, Grygier (1995) published an annotated chronological bibliography of the Monstrilloida.

Within this order, only one family, Monstrillidae, is recognised. Until recently, eight genera were considered valid, but Mark Joseph Grygier (Fig. 2.5e) and Susumu Ohtsuka (2008) briefly revised the status of each genus and determined only three should retain their validity, with the other five all being synonymised into the genus Monstrilla. They then proceeded to add an additional genus, Maemonstrilla Grygier & Ohtsuka, 2008. Six years later, Suárez-Morales and Mckinnon (2014) added another genus Australomonstrillopsis Suárez-Morales & McKinnon, 2014, giving a current total of five accepted genera.

Most of the species within Monstrilloida have been described by Eduardo Suárez-Morales (Fig. 2.7f) and colleagues (75 valid taxa), including a single genus, 73 species and 1 subspecies. The systematic position of this order however is still unclear. According to Huys et al. (2007), Monstrilloida fall within a fish parasitic clade of the Siphonostomatoida, sharing a common ancestor with caligiform families. However, this is considered unconfirmed by some researchers, and more information is required before any definitive changes in classification can be made (Suárez-Morales 2011). The original status of the Monstrilloida therefore remains as is at this stage (Suárez-Morales and McKinnon 2014).

Poecilostomatoida

Most poecilostomatoid copepods are ectoparasites, attaching to the external surfaces or the gills of their hosts (fish or other invertebrates); however, there are several endoparasitic species that live within the body of their hosts too. The first described species for this order was the ectoparasite Lernentoma asellina (Linnaeus, 1758), an uncommon parasite found in the gills of gurnards from the family Triglidae. This copepod is from the family Chondracanthidae that was revised by Ju-shey Ho, from California State University, Long Beach. Ho’s work on symbiotic copepods has exceeded 257 publications on these crustaceans from around the world. In 1970 and 1971, Ho revised the Chondracanthidae (when it still was in the order Cyclopoida) in order to clarify the confusion surrounding these crustacean’s identification, re-examining and redescribing every specimen and verifying its identity. At the time, only 30 genera were known; however, there are now 51 known genera in this family containing 193 species and 4 subspecies. Recently, Østergaard et al. (2003) used phylogenetic analyses to determine the phylogeny within the family, which clarified some of the questions regarding past and present subfamilies of Chondracanthidae.

The Splanchnotrophidae is a small but interesting family of copeopods which parasitise opisthobranch gastropods (including nudibranchs and pteropods) (Huys 2001). They are usually deeply embedded inside their host with only the distal urosome and egg sacs visible (Uyeno and Nagasawa 2012). Currently, there are 6 genera and 31 species within the family. The first two described species were Lomanoticola brevipes (Hancock & Norman, 1863) and Splanchnotrophus gracilis Hancock & Norman, 1863.

Another family, Ergasilidae, comprises fish parasitic copepods, where only the females are parasitic. Most species are found in freshwater and most attach to the host gills. There are 29 genera, 261 species and 2 subspecies presently regarded as valid species in this family. The first genus to be described was Ergasilus von Nordmann, 1832, with two species, Ergasilus gibbus Nordmann, 1832, and Ergasilus sieboldi Nordmann, 1832. Ergasilus sieboldi attaches to the gill filaments using its second antennae and can cause tissue damage or secondary infections at the site of attachment. The nutrition of E. sieboldi was noted by Einszporn (1965a, b), and it is known to cause severe fish losses in aquaculture (see Piasecki et al. 2004). Over the years, several researchers mentioned different life stages of E. sieboldi, but there were many discrepancies between the different reports as they were often not complete studies on the life cycle. In 1991, Abdelhalim et al. (1991) were able to provide complete information on all of the different life stages for this species.

The family Taeniacanthidae has 21 genera with 121 species. These copepods are parasitic on marine fishes and sea urchins. The first species of taeniacanthid described was Tucca impressus Krøyer, 1837, an ectoparasite on porcupinefish and pufferfish. Morphologically Taeniacanthidae are closely related to Bomolochida and were previously placed within that family until 1911 when Wilson separated the taeniacanthids and the bomolochids (Wilson 1911). However, it was only in 1932 when Wilson elevated both of these groups to family level, removing them from Ergasilidae. Dojiri and Cressey (1987) revised the family and, including new species descriptions, keys to all genera, host-parasite lists, distribution, morphology, ecology as well as notes on the relationships between the closely related Bomolochidae, Taeniacanthidae and Tuccidae.

Argulus

The first branchiuran species described was Argulus foliaceus (Linnaeus, 1758) (originally named Monoculus foliaceus), although Branchiura are thought to be mentioned as early as tenth century China. According to Piasecki and Avenant-Oldewage (2008), a monk named (Kao) Tsan-ning mentioned how goldfish that eat bark from poplar trees will not breed “lice”, and this was most likely referring to an Argulus species (Møller 2009). Wilson (1902) had originally stated that fish lice were first mentioned by a fisherman from Strasbourg, Léonard Baldner, in 1666. Baldner apparently described and pictured the birds, fishes and aquatic animals of the neighbourhood and specifically mentioned “Pou des poissons” (fish louse).

Argulus is the most specious genus of the family Argulidae, with approximately 127 species, and is widely distributed around the world. The genus was named in recognition of the numerous ommatidia in the compound eyes (diminutive of the mythical Greek beast, Argus, which had a hundred eyes) (Wilson 1902). The majority of the earlier studies focused on the first Argulus species, A. foliaceus. The nervous and genital systems as well as other microscopic anatomy of A. foliaceus were described by Leydig (1850, 1889), with studies on the larval development initiated by Claus (1875). Wilson (1902, 1904a, b) continued the larval and hatching research, with additional data added on the genital system and the circulatory system. Wilson also covered the taxonomic studies of North American Argulus (Wilson 1916, 1920a, b, 1921, 1923, 1924), some of which were revised by Meehan (1940). Wilson (1944) admired some of the new data provided by Meehan, especially the key to the genus, but disagreed with the taxonomic species revisions calling it a “serious encroachment upon the genus”. The taxonomy and identification keys of African Argulus species were completed by Cunnington (1913), Monod (1928), Fryer (1956, 1959, 1961a, b, 1965a, b, 1968) and Rushton-Mellor (1994a, b, c), while the South American species were covered by Brian (1947) and Ringuelet (1943, 1948).

More recently, research has focused on histology and ultrastructure analysis of various Argulus structures and how they relate to the ecology of these parasites. Tam and Avenant-Oldewage (2006) used gut ultrastructure to determine that the first larval stage uses yolk, and not blood, as the primary source of nutrition. Three years later, Tam and Avenant-Oldewage (2009) also used the digestive cell ultrastructure to determine that the elaborate enteral diverticula are part of the anterior midgut, and not similar to the midgut glands seen in other Crustacea.

Chonopeltis

This genus is endemic to sub-Saharan Africa and currently has 13 valid species. The first species described was Chonopeltis inermis Thiele, 1900 from Lake Rukwa. The genus is named in reference to the “cone- or funnel-shaped shield” (Møller 2009). Other than three publications (Wilson 1902; Thiele 1904; Monod 1928), almost 40 years passed from when the genus was established to new data being published on it (Brian 1940).

Probably one of the main contributors to our knowledge on this genus is Geoffrey Fryer (Fig. 2.8a). Fryer recognised three different species from the single variant species, C. inermis var. schoutedeni described by Brian (1940). One species was established as C. schoutedeni Brian, 1940, while the other two species were described by Fryer as new to science (C. congicus Fryer, 1959, and C. flaccifrons Fryer, 1960a). This discovery made him the authority of more than half of the Chonopeltis species known at the time (Fryer 1959, 1960a). Furthermore, Fryer completed noteworthy ecological studies on this genus, noting for the first time that the adults are sedentary (Fryer 1956), and there is a lack of cephalic lobe rods in C. flaccifrons (see Fryer 1960a). Fryer went on to describe several more species, produce a key for the genus and show the difference between Chonopeltis and the already known Argulus and Dolops larvae with the lack of metanauplius or juvenile-like morphology in the first descriptions of the Chonopeltis larval stages (Fryer 1964, 1974, 1977).

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Fig. 2.8

(a) Geoffrey Fryer, (b) Jo van As, (c) Liesl van As, (d) Annemariè Avenant-Oldewage, (e) Eugène Louis Bouvier, (f) Karl Asmund Rudolphi, (g) Karl Georg Friedrich Rudolf Leuckart, (h) Richard Heymons, (i) John Teague Self. Images (a), (e), (f) and (g) © Wikipedia Commons public domain; image (h) from Röhlig et al. (2010); image (i) from Janovy (1996)

The majority of the more recent species descriptions and distributions have been by South African researchers, Jo and Liesl van As (another husband and wife team) (Fig. 2.8b, c) (van As 1986, 1992; van As and van As 1993, 1996, 1999a, b) as well as Annemariè Avenant-Oldewage (Fig. 2.8d) (Avenant-Oldewage 1991; Avenant-Oldewage and Knight 1994, 2008). Additionally, van As and van As (1996) provided the first SEM image of the Chonopeltis larva; and Avenant-Oldewage and colleagues used histology to elucidate the morphology of the digestive system (Swanepoel and Avenant-Oldewage 1993; Avenant-Oldewage et al. 1994). In 2017, Van As et al. revised the southern African species of Chonopeltis and found that contrary to earlier theories, each river system does not have its own species of Chonopeltis. After careful examination of all C. meridionalis Fryer, 1964; C. victori Avenant-Oldewage, 1991; and C. koki Van As, 1992, material, it was concluded that all are indeed the same species, C. meridionalis, and occur in multiple river systems but only on cyprinid hosts (Van As et al. 2017).

Dipteropeltis

Until recently, Dipteropeltis was a monotypic genus, with the sole species being Dipteropeltis hirundo Calman, 1912, described by William Thomas Calman (a Scottish zoologist). However, recently Neethling et al. (2014) described a second species, Dipteropeltis campanaformis Neethling, Malta & Avenant-Oldewage, 2014, from Brazil. This genus is only known from South America and is the only branchiuran genus endemic to that region. These parasites infect piranhas (Carvalho et al. 2003) and can sometimes occur in certain areas with a prevalence as high as 73% (Mamani et al. 2004). As Dipteropeltis species have not been collected very often, and studies on members of this genus are very limited, information on other life stages, development and ecology is scanty.

The author would like to thank Philippe Laval, Wolfgang Zeidler, Niel Bruce, Christopher Boyko, Jason Williams, John Markham, Jianmei An, Jean-Paul Trilles, Nico Smit, Gary Poore, Mark Grygier, Jens Høeg, Gregory Kolbasov, William Newman, Rony Huys, David Damkaer and Eduardo Suárez-Morales for providing photos used in the figures.