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Parasite Loss Or Parasite Gain? Story of Contracaecum Nematodes in Antipodean Waters

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Parasite Loss Or Parasite Gain? Story of Contracaecum Nematodes in Antipodean Waters Parasite Epidemiology and Control 3 (2019) e00087 Contents lists available at ScienceDirect Parasite Epidemiology and Control journal homepage: www.elsevier.com/locate/parepi Parasite loss or parasite gain? Story of Contracaecum nematodes in antipodean waters Shokoofeh Shamsi School of Animal and Veterinary Sciences, Graham Centre for Agricultural Innovations, Charles Sturt University, Australia article info abstract Article history: Contracaecum spp. are parasitic nematodes belonging to the family Anisakidae. They are known to Received 26 October 2018 be able to have highly pathogenic impacts on both wildlife (fish, birds, marine mammals) and Received in revised form 16 January 2019 humans. Despite having the most numerous species of any genus of Anisakidae, and despite a Accepted 16 January 2019 wide range of publications on various aspects of their pathogenicity, biology and ecology, there are no recent comprehensive reviews of these important parasites, particularly in the Southern Hemisphere. In this article, the diversity of Contracaecum parasites in Australian waters is reviewed and possible anthropological impacts on their populations are discussed. The abundance and diver- sity of these parasites may have been under-reported due to the inadequacy of common methods used to find them. Populations of Contracaecum parasites may be increasing due to anthropogenic factors. To minimise the risk these parasites pose to public health, preventive education of stake- holders is essential. There are still many unknown aspects of the parasites, such as detailed informa- tion on life cycles and host switching, that will be interesting directions for future studies. © 2019 Published by Elsevier Ltd on behalf of World Federation of Parasitologists. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). Contents 1. Introduction........................................................ 0 2. Morphological characteristics of Contracaecum ......................................... 0 3. How many Contracaecum species?.............................................. 0 4. Life cycle of Contracaecum:howmuchdoweknow?...................................... 0 5. Contracaecum andhumanhealth............................................... 0 6. Impactsofhumanactivities................................................. 0 7. Conclusions........................................................ 0 References........................................................... 0 1. Introduction The genus Contracaecum Railliet & Henry, 1912 are parasitic nematodes belonging to the family Anisakidae Railliet & Henry, 1912 and have a global distribution (Anderson, 2000). If humans are excluded from their host list, Contracaecum is the only mem- ber of the Anisakidae that, throughout its life cycle, is able to infect both terrestrial and aquatic animals (freshwater and marine), which include a wide range of vertebrates and invertebrates. It also has zoonotic significance. With over 100 species assigned to this genus (Bezerra et al., 2019), it is the most numerous and diverse genus of the Anisakidae. Members of this genus are signif- icant due to their number of species, the wide range of host species involved in their life cycles, and their adverse health impacts E-mail address: [email protected]. https://doi.org/10.1016/j.parepi.2019.e00087 2405-6731/© 2019 Published by Elsevier Ltd on behalf of World Federation of Parasitologists. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). 2 S. Shamsi / Parasite Epidemiology and Control 3 (2019) e00087 on hosts. Despite this, there has been no comprehensive literature review of these parasites. In particular, there is limited knowl- edge of these parasites in Australian waters. The aim of this article is to review the diversity of Contracaecum in Australian waters and provide insights into potential anthropological impacts on them. 2. Morphological characteristics of Contracaecum As the genus' name suggests, these nematodes have two oppositely-directed caecae as part of their digestive system (Fig. 1). They also have an excretory pore located at their anterior end. These should be considered the most significant morphological characteristics when differentiating Contracaecum species from the rest of the anisakid nematodes because they are the most con- sistent at all developmental stages. Other important features with taxonomic significance in adult Contracaecum species include the presence of interlabia and labia, the absence of labial denticulation, rounded eggs with smooth shells, the presence of two spicules, conical tails in both male and females (which are shorter in males) and the presence of post- and pre-cloacal papillae in males (Fig. 1). Species within the genus can be differentiated based on variations in these features (Mozgovoi, 1953; Hartwich, 1964a). 3. How many Contracaecum species? Deardorff and Overstreet (1981) placed the members of Contracaecum with excretory pore located close to the nerve ring, or below it, in the genus Hysterothylacium Ward & Magath, 1917 (Family Raphidascarididae Hartwich, 1954). This was later sup- ported by molecular (Nadler et al., 2005) and other morphological and ecological data; e.g., Hysterothylacium become adults in fish whereas Contracaecum become adults in marine mammals and birds (Fagerholm, 1991). This resulted in the reclassification Fig. 1. Morphology of Contracaecum nematodes: (a) anterior end of C. bancrofti showing oesophagus, ventricular appendix and intestinal caecum (scale-bar = 0.65 mm); (b) apical view of lips in C. bancrofti (scale-bar = 0.17 mm); (c) posterior end of male (C. pyripapillatum), ventral view showing cloacal papillae (scale-bar = 0.17 mm); (d & e) scanning electron micrographs of C. bancrofti, c, showing folded interlabium. Arrow indicating lateral interruption in annulation of collar (scale-bar = 0.1 mm); (e) ventral view of male tail with three double pairs of post-cloacal papillae (scale-bar = 0.1 mm). Abbreviations: NR: nerve ring, Oe: oesophagus, IC: intestinal caecum, V: ventriculus, VA: ventricular appendix, Int: intestine, IL: interlabium, SVL: subventral labium, DL, dorsal labium, P: papillum. Modified from: Shamsi et al., 2008. S. Shamsi / Parasite Epidemiology and Control 3 (2019) e00087 3 of over 70 species from Contracaecum to Hysterothylacium; however, there are still many species assigned as Contracaecum. Yamaguti (1961) alone recorded 63 species of Contracaecum in birds in his monograph and there are many more that infect ma- rine mammals (e.g., Fagerholm, 1991). Moreover, molecular studies based on approaches such as multilocus enzyme electropho- resis (Nascetti et al., 1993; Orecchia et al., 1994) and DNA-based methods (Li et al., 2005; Shamsi et al., 2009a) have shown that some single species classifications actually comprise several distinct species with different host preferences and geographical dis- tributions. Therefore, it can be estimated that, globally, there are still over one hundred species within the genus Contracaecum. Shamsi (2014) listed 15 species of Contracaecum in Australia with valid taxonomic statuses, including C. bancrofti Johnston & Mawson, 1941, C. eudyptulae Johnston & Mawson, 1942, C. heardi Mawson, 1953, C. magnipapillatum Chapin, 1925, C. microcephalum (Rudolphi, 1809), C. multipapillatum (Drasche, 1882) Lucker, 1941, C. ogmorhini sensu stricto Johnston & Mawson, 1941, C. osculatum sensu lato (Rudolphi, 1802) Baylis, 1920, C. pelagicum Johnston & Mawson, 1942, C. podicipitis Johnston and Mawson, 1949, C. pyripapillatum Shamsi, Beveridge and Gasser, 2008, C. radiatum (Linstow, 1907) Baylis, 1920, C. rudolphii sensu lato Hartwich, 1964, C. sinulabiatum Johnston & Mawson, 1941 and C. variegatum (Rudolphi, 1809). Both in Australia and elsewhere, it is difficult to calculate the exact number of species within the genus due to issues with the validity of numerous species, particularly those described before the mid-20th century. Although the contributions of the earlier re- searchers to our knowledge of Contracaecum nematodes in Australia and elsewhere are significant, some of these early reports of the species have been poorly described and, as a result, differentiation between closely-related species is not possible. In addi- tion, some of these species are unidentifiable by current standards, as their descriptions are brief and sometimes unillustrated. For example, C. nycticoracis Johnston & Mawson, 1941 was reported as a new species (Johnston and Mawson, 1941d)fromNycticorax caledonicus in Australia, based on only one male specimen with a brief description, unknown spicule length and no details of the post-cloacal papillae. The latter characteristics are the main features used to differentiate Contracaecum spp. Additionally, there are no details of the lips, size, or number of caudal papillae in the description of the new species. Therefore, this species is not differ- entiable from many other Contracaecum spp., including C. microcephalum. Another issue with early descriptions is that for many of the new species, such as C. bancrofti, C. clelandi, C. sinulabiatum and C. magnicollare, there is no information on the location of the type material in the original paper (Johnston and Mawson, 1941c). Some of these species have only been reported from Australia, such as C. clelandi, C. eudyptes, C. heardi, C. magnicollare, C. nycticoracis, C. podicipitis and C. sinulabiatum, and doubts have been raised
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