Classification

Phylum Nemata

Superfamily Heterakoidea

Introduction

Heterakoidea is a superfamily of ascaridid nematodes that occur most often in the cecum and large intestine of amphibians, reptiles, birds, and mammals. Some species are very common with several occurring in galliform birds worldwide, while others may be found commonly in various mammals in both North America and South America. Two genera particularly, Ascaridia and Heterakis, include important parasites of birds, and both impact rearing of commercial poultry (Jansson et al., 2010).

Heterakoids are characterized by a pre-cloacal sucker in males and an esophagus with a posterior bulb and a muscular anterior corpus. The life cycle of heterakoid nematodes is simple: Eggs containing the infective third-stage juvenile (J₃) are ingested by the definitive host, although for some species, paratenic hosts may be involved.

Phylogenetic analysis of SSU rDNA sequences reveals that, as currently defined, this superfamily is not monophyletic and requires taxonomic revision (Nadler et al., 2007).

Morphology

As noted in the introduction, one of the most conspicuous characters of the heterakoid nematodes is the precloacal sucker, which is endowed with a well-developed cuticular rim. This character is present in all but a few species that are classified in the superfamily. Notable exceptions include some species of Lauroia (see Proença, 1938; Jiménez-Ruiz and Gardner, 2003) and Ascaridia. Other important features have been highlighted by Inglis (1967) who described the cuticular ornamentation of the stoma (also called the buccal cavity) and lips, and notes their homology or common origin with the cuticular derivatives of the esophagus and body wall. The typical stoma of the heterakoid is endowed with a fused esophagorhabdion and a conspicuous cheilorhabdion. Before the advent of molecular techniques, these characters had been used extensively for the description of genera and the classification of the suprageneric taxa. Other important characteristics of these nematodes include papillae in the precloacal rim and the preanal papillae (see Figure 1).

Figure 1. Heterakoid nematodes, Aspidodera spp. A) Posterior end of A. sogandaresi showing pre-cloacal sucker (s) and spicules (sp); B) posterior end of A. fasciata showing paired spicules (ps) sucker (s) and proximal end of gubernaculum (g). Scale bars = 100 μm.
(Source: S. L. Gardner, HWML. License: CC BY 4.0.)

Finally, the esophagus is divided into 3 parts, which acquire their final adult configuration in the fourth molt. These include a conspicuous pharynx, the corpus, and an esophageal bulb that is endowed in most species with a trivalved sphincter (Figure 2).

Figure 2. Examples of the structures of the hood in Aspidoderidae (phylum Nemata: superfamily Heterakoidea) as seen in the right lip.
(Source: S. L. Gardner, HWML. License: CC BY 4.0.)

Diagnosis

The Heterakoidea are members of the class Secernentea, order Ascaridiomorpha. Three lips are present, with a dorsal lip that is bilaterally symmetrical featuring double papillae and ventral lips, each with a single papilla. There is a conspicuous cheilorhabdion lining the buccal cavity or stoma and a medially located esophagorhabdion. The esophagus is muscular, divided into 3 conspicuous parts, including a pharynx that projects into the lips, corpus, and bulb. There is a heavily cuticularized precloacal sucker with a robust rim, 2 spicules, and a gubernaculum that guides the spicules during copulation. The vulva is usually located at midbody. In the uterus, the eggs are usually unembryonated and the shell is smooth, some with polar pores.

Distribution and Host Associations

Members of the taxon include dwellers of the cecum or large intestine of terrestrial tetrapods, with a single case of infection reported in fish (Meterakis japonica, Moravec and Sey). Most of the taxonomic diversity is present in scaled reptiles and birds, followed by several taxa present in frogs and mammals. The heterakoid nematodes have a cosmopolitan distribution being found in the large intestines of reptiles, birds, and mammals on all continents except Antarctica. Very few species appear to be endemic to temperate land masses, with notable exceptions, such as Hatterianema hollandei and Kiwinema gracilicauda, which appear to be limited to the main islands of New Zealand. Both species occur in endemic tetrapods of these islands such as the tuatara (Sphenodon punctatus) and an unidentified species of kiwi of the genus Apteryx. Species diversity of these taxa is very low, as only 1 species is known for each genus (Inglis, 1991). This taxon also includes a third genus of limited diversity, since Mammalakis includes 2 known species in naked mole rats from South Africa and Europe (Inglis, 1991).

The biogeography and host associations for subfamilies Spinicaudinae and Meteterakinae are in sharp contrast to one another. Prevailing hypotheses posit that Spinicaudinae has a cosmopolitan distribution, yet members of the Meteterakinae show a disjunct and perhaps relictual distribution confined to southeast Asia and the Neotropics (Baker, 1984). These 2 groups are associated with frogs and semiaquatic reptiles.

A different pattern is evident in species in the family Aspidoderidae, for which distribution is chiefly Neotropical with documented dispersions into North America (Jiménez-Ruiz et al., 2012). These parasites chiefly infect mammals of a Neotropical origin and are the only family that predominantly shows this distribution and host association. Interestingly, the relationships of members of the family with other members of the Heterakoidea are yet to be resolved.

The rest of the groups in the family, namely Ascaridiinae and Narsingianellinae, show contrasting patterns. The latter appears to be restricted to toads in southeast Asia and the Indian subcontinent (Rao, 1978; Rizvi, 2009), whereas the former is cosmopolitan, with species occurring in birds, and occasionally in mammals and reptiles.

General Biology

The precise dietary requirements of these nematodes have not been determined, although it has long been speculated that because of their habitat they must feed on cecal or gut bacteria. Experimental manipulations show that varying levels of fiber in the host diet induce conspicuous differences in the survival and fecundity on the cecal-dwelling Heterakis gallinarum (see Daş et al., 2014). Fiber-rich diets increase the volume of the ceca and the fermentation activity induced by bacteria.

Experimental infections that help illustrate their life cycle have been completed for just 6 species, yet they all seem predominantly to feature direct transmission. In some cases, earthworms and other terrestrial invertebrates are used as vectors for the eggs (Ackert, 1917; Frank, 1953). The thin-shelled nature of the eggs, featuring 2 polar pores, may make them prone to prompt dehydration, thus making them highly dependent on humid environments. There is ample evidence, however, that humidity is the key environmental condition that promotes the development of these worms. Experimental work on Heterakis gallinarum has been used to characterize the typical life cycle of members of the superfamily. As such, this can be generalized to be monoxenous (without an intervening intermediate host), with females laying unembryonated eggs that complete embryogenesis in the external environment and juveniles undergoing 2 molts (Araújo and Bressan, 1977). The development of the infective stage is temperature dependent; it takes 7 to 12 days to form the infective stages in temperatures ranging between 17 and 29 °C (Graybill, 1921). When temperature is maintained at 27 °C and 33 °C, development completes in 6 and 4 days, respectively. Usually, eggs become infective 24 hours after the second molt (Roberts, 1937).

Experimental approaches to test the animals’ endurance in adverse conditions document their resistance to dry environments and drastic temperature and humidity changes, as well as their prolonged retention of infectivity. The eggs can remain infective after being passed through the digestive system of earthworms and grasshoppers (Ackert, 1917; Frank, 1953). The nematodes are able to complete migration to their target organ 48 hours post-infection (hpi).

In contrast, some of the species appear to be able to complete their development optimally while completely submerged in tap water (Petter, 1968; Bain, 1970). In the case of Spinicauda freitasi and S. inglisi, the development of the infective stage takes between 14 and 15 days when submerged in tap water at 26 °C. Infective juveniles feature a rhabditiform esophagus. When fed to a definitive host, the nematodes reach their target organ typically 40 dpi (Petter, 1968). Experimental infections of larvated eggs of insects showed that the juveniles of Strongyluris brevicaudata can migrate and encapsulate in the thorax of cockroaches and occasionally in mosquitoes (Bain, 1970).

As nematodes develop throughout their life, there is a drastic reconfiguration of both internal organs and external appearance. Detailed accounts of this metamorphosis document the transformation for Spinicauda inlgisi, Sp. freitasi (see Petter, 1968), Strongyluris brevicaudata (in Bain, 1970), and Heterakis gallinarum (shown by Dorman, 1928). These juveniles undergo changes and molt twice to develop into infective forms, featuring a rhabditiform esophagus that is devoid of a bulb. During the migration through the digestive system of the definitive host, the nematodes mature with the concomitant development of the characteristic esophageal bulb (Petter, 1968; Bain, 1970).

Evolution

Based on their geographic distribution and the features of their anterior end and cuticular ornamentation, and their association with ectothermic tetrapods, Inglis (1967) offered an interpretation of their evolution with emphasis on their changes of association with vertebrates (specifically, host switching) and major morphological transitions. This notion was further elaborated by Baker (1984) who concentrated on a handful of species in 2 subfamilies and speculated on an origin in the Cretaceous for members of Heterakoidea. Studies on the phylogenetic associations between nematodes of this taxon and their hosts using replicable datasets started with the cophyletic approach for South American species of Paraspidodera spp. infecting hystricognath rodents (Gardner, 1991). The historical association among the Aspidoderidae and their wide array of hosts was further addressed in work by Jiménez-Ruiz and colleagues (2006; 2008; 2012). A holistic approach addressing the origin of the Heterakoidea has not yet been produced.

Systematics and Phylogeny

Analysis for species included in suprageneric taxa are not clearly defined, and the relationships and even the classification of the families are still in flux (Rao, 1978; Inglis and Harris, 1990; Jiménez-Ruiz et al., 2008; 2012). There are a few proposals of the phylogenetic arrangement for members of the Heterakoidea, yet all of them concentrate on the relationships among species in a genus or a family (Bouamer and Morand, 2008; Jiménez-Ruiz et al., 2013) (see Table 1 for a Linnean classification for the Heterakoidea).

Building on the foundation of the systematic approaches presented by Mozgovoi (1953) and Skrjabin and Shikhobalova (1951), Inglis (1967) proposed an overall classification structure for the group identifying 3 main synapomorphies:

1. Very well-developed rhabdions (cuticular structures derived from the esophagus and the body wall that cover the inner lining of the mouth; see Figure 3)
2. Lips
3. A ventral sucker with a cuticular rim

This systematic arrangement has survived until the present, although some phylogenetic reconstructions challenge its monophyly (Nadler et al., 2007).

The accelerated rate of species descriptions of Meteterakis species from the Southeast Asian archipelago seems to suggest the notion that the groups are diverse, yet the taxonomic impediment (that is, a lack of qualified, trained taxonomists) hinders the documentation of biodiversity.

Figure 3. En face view of 4 species of Aspidoderidae showing the positions of the lips. Dorsal lip is labeled 1 in all images; ventral side includes 2 lateroventral lips labeled as 2 (sinistroventral) and 3 (dextroventral). Aspidodera scoleciformis (i), A. bolivari (ii), A. scapteromi (iii), and Paraspidodera uncinata (iv).
(Source: Jiménez-Ruiz et al., 2008. License: CC BY-NC-SA 4.0.)

Superfamily Heterakoidea

Family Ascaridiidae Travassos, 1919

It is important to note that this family name is very similar to the family name Ascarididae Baird, 1853, which is included within the superfamily Ascaridoidea (discussed in another chapter). It is unfortunate that they are so similarly named, but be clear that Ascarididae and Ascaridiidae are absolutely separate groups.

One species within the Ascaridiidae of interest is Ascaridia galli, which is a cosmopolitan parasite of the small intestine of domestic fowl and game birds. Males reach a length of 77 mm, and females reach 115 mm. Juveniles within eggs hatch after they are ingested with contaminated food or water. The life cycle does not involve extensive tissue migration. Instead, 8 or 9 days after infection, juveniles molt to the third stage (J₃) and begin to burrow into the mucosa, where they generally remain with their tails still in the intestinal lumen. After molting to J₄ at about 18 days, they return to the lumen, where they undergo their final molt. Probably a majority of worms complete their 2 molts and attain maturity without ever leaving the lumen. However, some juveniles burrow their anterior ends into the intestinal mucosa where they remain for up to 2 months before molting and returning to the lumen to complete development to the adult stage.

Table 1. Linnean Classification for the Superfamily Heterakoidea, as of 2014

Heterakoidea

Kiwinematidae Inglis and Harris, 1990

Kiwinematinae Inglis and Harris, 1990

Kiwinema Inglis and Harris, 1990

Kiwinema gracilicauda Inglis and Harris, 1990

Hatterianema Chabaud and Dollfus, 1966

Hatterianema hollandei Chabaud and Dollfus, 1966

Mammalakinae Inglis, 1991

Mammalakis Inglis, 1991

Mammalakis macrospiculum

Mammalakis spalacis

Heterakidae Railliet and Henry, 1912

Heterakinae Railliet and Henry, 1912

Heterakis Dujardin, 1945

Pseudaspidodera Baylis and Doubney, 1922

Odonterakis Skjabin and Schikhobalova, 1947

Musserakis Hasegawa, Dewi and Asagawa, 2014

Musserakis sulawesiensis Hasegawa, Dewi and Asagawa, 2014

Neoheterakis Kumar and Thienpoint, 1974

Haroldakis Inglis, 1991

Meteterakinae

Meteterakis Karve, 1970

Gireterakis Lane, 1917

Bufonerakis Baker, 1980

Cagourakis Petter, Chermette and Vassart, 1988

Narsingellinae Rao, 1978

Narsingiella Rao, 1978

Spinicaudinae

Spinicauda Travassos, 1920

Africana Travassos, 1920

Moaciria Texeira de Freitas, 1956

Strongyluris Mueller, 1894

Pseudostrongyluris Guerrero, 1970

Aspidoderidae Skrjabin and Shikhobalova 1947

Aspidoderinae Skrjabin and Shikhobalova 1947

Aspidodera Railliet and Henry, 1912

Ansiruptodera Skrjabin and Shikhobalova 1947

Nematomystes Sutton, Chabaud and Durette-Desset, 1980

Lauroiinae Skrjabin and Shikhobalova 1947

Lauroia Proença, 1938

Paraspidodera Travassos, 1914

Ascaridiidae Travassos, 1919

Ascaridia Dujardin, 1845

Those that attack the mucosa cause extensive damage, and Ascaridia galli causes production losses in chickens. High-intensity infections can obstruct the small intestine and cause death. In addition, adult A. galli are sometimes found in chicken eggs destined for human consumption. This is obviously of concern to egg producers. Improved management practices to control infection through sanitation are important because in some countries few anthelminthics are approved for use in poultry.

Family Heterakidae Railliet & Henry, 1912

Heterakis gallinarum is cosmopolitan in domestic chickens and turkeys. It was probably brought to the United States in imported ring-necked pheasants. The worms live in the cecum, where they feed on its contents. Heterakis gallinarum is unusual because in galliform birds it serves as a vector of the parasitic protozoan, Histomonas meleagridis, the causative agent of histomoniasis (blackhead). Hence, the curious phenomenon of one parasite acting as an intermediate host and vector of another is revealed.
Several species of Heterakis are known from birds, particularly in ground feeders, and one species, H. spumosa, is cosmopolitan in rodents.

Three large lips and an esophageal basal bulb as well as lateral alae are found in this genus. Males are as long as 13 mm and possess wide caudal alae supported usually by 12 pairs of papillae (Figure 4). Their tail is sharply pointed, and there is a prominent preanal sucker. Spicules are strong and dissimilar, and a gubernaculum is absent. Females have the vulva near the middle of their body and a long, pointed tail.

Figure 4. The anterior end of Paraspidodera sp. from a rodent from Bolivia showing the 3 lips.
(Source: S. L. Gardner, HWML. License: CC BY 4.0.)

Biology

Eggs of Heterakis gallinarum contain a zygote when laid. They develop into the infective stage in 12 to 14 days at 22 °C and can remain infective for 4 years in soil. Infection is contaminative: When embryonated eggs are eaten, third-stage juveniles (J₃) hatch in the gizzard or duodenum and pass down to the cecae. Most complete their development in the lumen, but some penetrate the mucosa, where they remain for 2 to 5 days without further development. Then, returning to the lumen, they mature about 14 days after infection. If eaten by an earthworm, a juvenile may hatch and become dormant in the worm’s tissues, remaining infective to chickens for at least a year. Since these nematodes do not develop further until eaten by a bird, an earthworm is a paratenic host. Grasshoppers, flies, and sowbugs can also serve as mechanical vectors of eggs.

Epidemiology

As a result of the longevity of the eggs, it is difficult to eliminate Heterakis gallinarum from a domestic flock. The many different mechanisms for persistent contamination of poultry farms by eggs remains a challenge to implementing sanitation procedures, such as cleaning and disinfection, without concurrent use of strict hygiene barriers. In addition, wild birds may also serve as sources of infection. Furthermore, as earthworms feed in contaminated soil, they accumulate large numbers of juveniles, which in turn cause massive infections in the unlucky birds that eat them.

Pathogenesis

Generally speaking, Heterakis gallinarum is not highly pathogenic in itself. Chickens typically have only minor histopathological lesions when infected, but show localized cellular immune effects, particularly a Th2-dominated response at the site of infection (Schwarz et al., 2011). However, the protozoan, Histomonas meleagridis, is transmitted between birds within eggs of He. gallinarum (see Long et al., 1987). This protozoan is the etiological agent of blackhead, a particularly serious disease in turkeys where mortality in captive flocks can exceed 85%. Unlike in chickens, blackhead can be directly transmitted between turkeys by fecal contamination. Typically, the protozoan is eaten by the nematode and multiplies in the worm’s intestinal cells, ovaries, and finally the embryo within the egg. Hatching of the worm within a new host releases Hi. meleagridis. In chickens co-infected with He. gallinarum and Hi. meleagridis, severe ulceration of the cecal mucosa may occur. The protozoan infection elicits a different, Th1-dominated immune response and a higher T-cell infiltration rate than with infection of He. gallinarum alone (Schwarz et al., 2011).

Diagnosis and Treatment

Heterakis gallinarum can be diagnosed by finding eggs in feces of its host. Birds allowed to roam a barnyard usually are infected. Worms are effectively eliminated with mebendazole. Usually, a flock of birds routinely gets this or other drugs in its feed or water. Other benzimidazole drugs that are effective against juvenile stages, such as albendazole and febendazole, have been shown to be useful for preventing establishment of Histomonas meleagridis by preventing nematode infection (Hegngi et al., 1999). Unfortunately, drugs directly effective against Hi. meleagridis have been found to be carcinogenic and are no longer registered for use in poultry. Without effective drugs or a vaccine, control of blackhead disease currently relies on management practices, including prophylaxis by regular deworming. In some countries, regulatory bans on keeping laying hens in metal cages have led to husbandry conditions that increase transmission of these nematodes, providing new challenges to their control (Jansson et al., 2010).

Ecology

Heterakoid worms appear to be moderately prevalent in the populations of tetrapods sampled in a systematic manner. Navone (1990) has demonstrated that the prevalence of some species of Aspidodera in armadillos from central Argentina was greater than 50% in the wet season and reduced to roughly 30% in the dry season. The prevalence of 2 species of Aspidodera in central Florida reach a combined level of 63% (Varela-Stokes et al., 2008). Both Heterakis gallinarum and Ascaridia galli occur in several wild and domestic galliform birds, posing a problem for wildlife managers in certain regions of the world.

Economic Importance

The species with the greatest known economic impact in the group is Heterakis gallinarum, known to infect poultry (domesticated chickens and both wild and domesticated turkeys) and may produce disease from high levels of infection. Yet the pathology induced by these species seldom jeopardizes the survival of the host and the infection by these nematodes alone rarely induces much mortality in a population. Nevertheless, He. gallinarum is involved in the transmission of a species of flagellated protozoan of the order Trichomonadida that causes significant mortality in wild and captive flocks of galliform birds. As noted above, Histomonas meleagridis is the causative agent of blackhead in chickens. This trichomonad is not known to produce cysts, having only an unflagellated trophozoite stage as well as a flagellated trophozoite stage, thus the trophozoite is the only morphotype in their life cycle. The parasite is transmitted horizontally through cloacal exchange or via contamination with fresh feces. The trophozoites do not live long in feces, and chickens are little affected by this protozoan, but in turkeys it is sometimes 100% fatal to the flock.

An interesting aspect of the biology of the nematode and the protozoan is that the trophozoites of Histomonas meleagridis are able to infect the sexual organs of both female and male nematodes. In the body of the females the trophozoites migrate through the uterus and reach the ovary. In that organ they are able to infect the developing embryos before the proteinaceous shell is formed. In this way, the trophozoites colonize a structure that will act as an exterior casing for the trophozoites, isolating them from the external environment outside both the avian host and the parasitic nematode. Several species of earthworms may serve to help complete the life cycle by ingesting nematode eggs and passing the infected eggs on to chickens or turkeys. The earthworms can pick up the eggs of the heterakoid nematodes from deep in the soil. The trichomonads are then able to hatch from the egg once consumed by the definitive host, then to reach the cecum and continue growth (Figure 5). In combination, these unique biological characteristics hinder the efforts to prevent and control the disease caused by these organisms.

Figure 5. Complex transmission of Histomonas meleagridis, a venereal disease of nematodes. In the galliform host, infective eggs of Heterakis gallinarum are ingested incidentally as the bird eats earthworms or other soil-dwelling invertebrates from soil contaminated with feces from infected birds. The eggs hatch in the intestine and juvenile nematodes move to the cecae in the lower part of the gastrointestinal tract of the bird where they feed on cecal contents, grow, molt to adults, mate, and produce eggs. Histomonid protozoans living and reproducing in the cecae of the bird invade the nematode via the vulva and move through the ovijector and uterus up to the ovary of the female nematode hosts (Heterakis gallinarum) where they proliferate, utilizing the germinal zone of the ovary of the nematode as nutrients. As the protozoans increase their numerical density in the ovary of the nematode, some penetrate the developing oocytes and are encased in the newly formed eggs. Histomonas meleagridis can also invade the cloaca and vas deferens of male Heterakis and may act as a venereally transmitted protozoan. In the bird host, the protozoan escapes when the egg hatches and establishes in the cecae of the intestine.
(Source of image: Beer et al., 2022. Created with BioRender.com. License: CC BY 4.0. | Source of caption: Adapted from Anderson, 2000. License: CC BY 4.0.)

Conservation

Prominent conservation biologist Gerardo Ceballos encourages biologists to frame their studies as a conservation activity (Rojas-Bracho et al., 2018). He suggests that there is value in documenting the distribution of all species to establish the consequences of species interactions in the function of any ecosystem. A challenge for future parasitologists is to frame the study of any group of nematodes (and, in fact, all parasites) from this perspective. Although most efforts in the conservation of parasites deal with the problem of the stress maintained on the hosts (including the pathological consequences of the effects that these parasites have on their hosts), there are more possibilities including using parasites with indirect life cycles as probes for biodiversity, which refers to the fact that discovery of a single species of parasite that uses a complex life cycle in a host immediately reveals several layers of biological complexity (Gardner and Campbell, 1992) or listing the parasites that cycle through sympatric animals and identifying the factors that determine this distribution.

The Heterakoidea include some species that are associated with relictual groups of animals, including Hatterianema hollandei present in the tuatara Sphenodon punctatus. Although the species is not listed as threatened by the International Union for Conservation of Nature (IUCN; Yeates et al., 2012), it includes a unique group of animals that serves as the only known host for this species of heterakoid. Furthermore, their phylogenetic relationships appear to be blurred by the combination of characters shared with other heterakoids present in southern continents and the potential extinction of ancient lineages of scaled reptiles, birds, and lisamphibians that could have harbored them (Chabaud and Dollfus, 1966; Inglis and Harris, 1990; Inglis, 1991). The association of the parasite with its host and its geography is the result of the optimal factors that make infection possible, including the chance encounter and the compatibility among hosts (Combes, 1991). The use of different and novel hosts depends on the evolutionary distinctiveness of both parasites and hosts. Parasites would be able to hack the immune system of hosts that may be closer biologically to their original hosts (Park et al., 2018) although there is abundant evidence of the ability of parasites to infect widely disparate hosts due to deep phylogenetic historical signals (Brooks et al., 2019).

Conservation biologists have urged identification of clades with unique genetic diversity. This genetic diversity can be evaluated as to how rare the genetic information is in the members of the group. Between any 2 sister clades, the one of critical conservation importance would be the one that holds the rarest species and includes unique genetic information that would be lost with the extinction of the species that features it. Consequently, the most relictual distribution of a species of nematode in addition to a high specificity suggest that the species lineage of nematodes is particularly unique. Invoking the earlier example, Hatterianema hollandei would be a very important species worthy of extraordinary efforts at conservation (Yeates et al., 2012) since it holds unique information that summarizes an evolutionary lineage in which most of the descendants have become extinct. This evolutionary lineage includes another relict, Kiwinema gracilicauda, a parasite of kiwis. The conservation of these lineages will allow scientists to identify the important factors that regulated the interactions of biological associates, including parasites and mutualists of the earliest tetrapods (Boast et al., 2018).

Further evidence of the relevance of heterakoids in the fields of conservation and evolution is provided by the eggs of some heterakoids. In some cases, these structures have been preserved in coprolites that document the associations of recently extinct organisms (Sardella and Fugassa, 2009; Boast et al., 2018). The preservation of some of these eggs has enabled researchers to identify them based on the unique morphology of the eggs (Figure 6) and has enabled the extraction and amplification of small fragments of DNA that allow scientists to identify the egg as coming from a unique species with marked distinctiveness with species currently present in the area (Boast et al., 2018).

Figure 6. Lauroia bolivari. Lateral view of the ovijector with eggs. Scale bar = 100 mm.
(Source: Adapted from Jiménez-Ruiz and Gardner, 2003. License: CC BY 4.0.)

Acknowledgement

A portion of this section was adapted with permission from Roberts et al. (2014, p. 421–422). No byline was included for this contribution at the beginning of this section, so this serves as acknowledgement of the contribution by the authors of that borrowed section.

Reviewer

Scott L. Gardner, Harold W. Manter Laboratory of Parasitology, University of Nebraska State Museum, Lincoln, Nebraska, United States; and School of Biological Sciences, University of Nebraska–Lincoln, Lincoln, Nebraska, United States.

Literature Cited

Ackert, J. E. 1917. A means of transmitting the fowl nematode Heterakis papillosa Bloch. Science 46: 394. doi: 10.1126/science.46.1190.394

Anderson, R. C. 2000. Nematode Parasites of Vertebrates: Their Development and Transmission, 2nd edition. CAB International, Wallingford, United Kingdom, 650 p.

Araújo, P., and M. C. R. V. Bressan. 1977. Considérations sur la deuxième mue des larves d’Ascaridia galli. Annales de parasitologie humaine et comparée 52: 531–537.

Bain, O. 1970. Cycle evolutif de l’Heterakidae Strongyluris brevicaudata (Nematoda): Mise en évidence de deux mues dans l’oeuf. Annales de parasitologie humaine et comparée 45: 637–653.

Baker, M. R. 1984. The systematics and zoogeography of Spinicaudinae and Meteterakinae (Heterakoidea: Nematoda) parasitic in reptiles and amphibians. Systematic Parasitology 6: 275–287. doi: 10.1007/BF00012206

Beer, L. C., V. M. Petrone-García, B. D. Graham, B. M. Hargis, et al. Histomonas in poultry: A comprehensive review. Frontiers in Veterinary Science: Parasitology 9: 880738. doi: 10.3389/fvets.2022.880738

Boast, A. P., L. S. Weyrich, J. R. Wood, J. L. Metcalf, et al. 2018. Coprolites reveal ecological interactions lost with the extinction of New Zealand birds. Proceedings of the National Academy of Sciences of the United States of America 115: 1,546–1,551. doi: 10.1073/pnas.1712337115

Bouamer, S., and S. Morand. 2008. Morphological phylogenetic analysis of the Africana genus (Nematoda: Heterakidae). Journal of Parasitology 94: 481–486. doi: 10.1645/GE-1222.1

Brooks, D. R., E. P. Hoberg, and W. A. Boeger. 2019. The Stockholm Paradigm: Climate Change and Emerging Disease. University of Chicago Press, Chicago, Illinois, United States, 409 p.

Chabaud, A. G., and R. P. Dollfus. 1966. Hatterianema hollandei n. g., n. sp., nématode hétérakide parasite de Rhynchocéphale. Bulletin du Muséum national d’histoire naturelle, serie 2, 37: 1,041–1,045.

Combes, C. 1991. Evolution of parasite life cycles. In C. Toft, A. Aeschlimann, and L. Bolis, eds. Parasite–Host Associations: Coexistence or Conflict? Oxford University Press, Oxford, United Kingdom, p. 62–82.

Daş, G., H. Abel, T. Savaş, B. Sohnrey, et al. 2014. Egg production dynamics and fecundity of Heterakis gallinarum residing in different caecal environments of chickens induced by fibre-rich diets. Veterinary Parasitology 205: 606–618. doi: 10.1016/j.vetpar.2014.08.008

Dorman, H. P. 1928. Studies on the life cycle of Heterakis papillosa (Bloch). Transactions of the American Microscopical Society 47: 379–413. doi: 10.2307/3222238

Frank, J. F. 1953. A note on the experimental transmission of enterohepatitis of turkeys by arthropoids. Canadian Journal of Comparative Medicine Veterinary Science 17: 230.

Gardner, S. L. 1991. Phyletic coevolution between subterranean rodents of the genus Ctenomys (Rodentia: Hystricognathi) and nematodes of the genus Paraspidodera (Heterakoidea: Aspidoderidae) in the Neotropics: Temporal and evolutionary implications. Zoological Journal of the Linnean Society 102: 169–201. doi: 10.1111/j.1096-3642.1991.tb00288.x

Gardner, S. L., and M. L. Campbell. 1992. Parasites as probes for biodiversity. Journal of Parasitology 78: 596–600. doi: 10.1111/j.1096-3642.1991.tb00288.x

Graybill, H. W. 1921. Data on the development of Heterakis papillosa in the fowl. Journal of Experimental Medicine 34: 259–270. doi: 10.1084/jem.34.3.259

Hegngi, F. N., J. Doerr, T. S. Cummings, R. D. Schwartz, et al. 1999. The effectiveness of benzimidazole derivatives for the treatment and prevention of histomonosis (blackhead) in turkeys. Veterinary Parasitology 81: 29–37. doi: 10.1016/s0304-4017(98)00233-7

Inglis, W. G. 1967. The evolution, host relationships and classification of the nematode superfamily Heterakoidea. Bulletin of the British Museum (Natural History) 15: 3–28. doi: 10.5962/bhl.part.27515

Inglis, W. G. 1991. Mammalakis n. g. and Mammalakinae n. subfam. (Nematoda: Heterakoidea: Kiwinematidae): Parasites of mole rats (Rodentia: Bathyergidae and Spalacidae). Systematic Parasitology 20: 89–95. doi: 10.1007/BF00007385

Inglis, W. G., and E. A. Harris. 1990. Kiwinematidae n. fam. (Nematoda) for Kiwinema n. g. and Hatterianema Chabaud and Dollfus, 1966: Heterakoids of native New Zealand vertebrates. Systematic Parasitology 15: 75–79. doi: 10.1007/BF00009919

Jansson, D. S., A. Nyman, I. Vågsholm, D. Christensson, et al. 2010. Ascarid infections in laying hens kept in different housing systems. Avian Pathology 39: 525–532. doi: 10.1080/03079457.2010.527923

Jiménez-Ruiz, F. A., and S. L. Gardner. 2003. Aspidoderid nematodes from Bolivian armadillos, with the description of a new species of Lauroia (Heterakoidea: Aspidoderidae). Journal of Parasitology 89: 978–983. doi: 10.1645/GE-3053

Jiménez-Ruiz, F. A., R. A. Carreno, and S. L. Gardner. 2013. Aspidodera kinsellai n. sp. (Nematoda: Heterakoidea) from nine-banded armadillos in Middle America with notes on phylogeny and host-parasite biogeography. Journal of Parasitology 99: 1,056–1,061. doi: 10.1645/GE-3045.1

Jiménez-Ruiz, F. A., S. L. Gardner, G. T. Navone, and G. Ortí. 2012. Four events of host-switching in Aspidoderidae (Nematoda) involve convergent lineages of mammals. Journal of Parasitology 98: 1,166–1,175. doi: 10.1645/GE-3045.1

Jiménez-Ruiz, F. A., S. L. Gardner, D. Noronha, and R. M. Pinto. 2008. The systematic position of Lauroiinae Skrjabin and Schikhobalova, 1951 (Nemata: Heterakoidea: Aspidoderidae), as revealed by the analysis of traits used in its diagnosis. Cladistics 24: 459–476. doi: 10.1111/j.1096-0031.2007.00194.x

Jiménez-Ruiz, F. A., S. L. Gardner, and A. Varela-Stokes. 2006. Aspidoderidae from North America with the description of a new species of Aspidodera (Nematoda: Heterakoidea). Journal of Parasitology 92: 847–854. doi: 10.1645/GE-735R.1

Long, P. L., W. L. Current, and G. P. Noblet. 1987. Parasites of the Christmas turkey. Parasitology Today 3: 360–366. doi: 10.1016/0169-4758(87)90241-9

Mozgovoi, A. A. 1953. [Ascaridata of animals.] Trudy Gelmintologischeskoi Laboratorii. Akademii Nauk USSR, Leningrad, Soviet Union. [In Russian.]

Nadler, S. A., R. A. Carreno, H. Mejía-Madrid, J. Ullberg, et al. 2007. Molecular phylogeny of Clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134: 1,421–1,442. doi: 10.1017/S0031182007002880

Navone, G. T. 1990. Estudio de la distribución, porcentaje y microecología de los parásitos de algunas especies de edentados argentinos. Studies on Neotropical Fauna and Environment 25: 199–210. doi: 10.1080/01650529009360820

Park, A. W., M. J. Farrell, J. P. Schmidt, S. Huang, et al. 2018. Characterizing the phylogenetic specialism–generalism spectrum of mammal parasites. Proceedings of the Royal Society B: Biological Sciences 285: 20172613. doi: 10.1098/rspb.2017.2613

Petter, A. J. 1968. Cycle évolutif de 2 espèces d’Heterakidae parasites de caméléons malgaches. Annales de Parasitologie humaine et comparée 43: 693–704.

Proença, M. C. 1938. Sobre um novo tipo de Heterakinae Railliet et Henry, 1912 (Nematoda: Subuluroidea). In B. Silva, B. J. de Almeida, N. Ferreira, A. Gonçalves, et al., eds. Livro Jubilar Professor Travassos. Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, p. 419–420.

Rao, R. 1978. On Narsingiella narsingi, a new genus and species of aspidoderid nematode from Bufo viridis found in Berhampur, India. Proceedings of the Helminthological Society of Washington 45: 246–248.Rizvi, A. N. 2009. Two new species of amphibian nematodes from Bhadra Wildlife Sanctuary, Western Ghats, India. Zootaxa 2013: 58–68. doi: 10.11646/ZOOTAXA.2013.1.6

Roberts, F. H. S. 1937. Studies on the life history and economic importance of Heterakis gallinae (Gmelin, 1790 Freeborn, 1923), the caecum worm of fowls. Australian Journal of Experimental Biology and Medical Science 15: 429–439. doi: 10.1038/ICB.1937.30

Rojas-Bracho, L., R. C. Brusca, S. Álvarez-Borrego, J. R. L. Brownell, et al. 2018. Unsubstantiated claims can lead to tragic conservation outcomes. BioScience 69: 12–14. doi: 10.1093/biosci/biy138

Sardella, N. H., and M. H. Fugassa. 2009. Paleoparasitological analysis of rodent coprolites in holocenic samples from Patagonia, Argentina. Journal of Parasitology 95: 646–651. doi: 10.1645/GE-1809.1

Schwarz, A., M. Gauly, H. Abel, G. Das̜, et al. 2011. Pathobiology of Heterakis gallinarum mono-infection and co-infection with Histomonas meleagridis in layer chickens. Avian Pathology 40: 277–287. doi: 10.1080/03079457.2011.561280

Skrjabin, K. I., N. P. Shikhabalova, and A. A. Mozgovoi. 1951. Key to Parasitic Nematodes: Oxyurata and Ascaridata. Izdatel’stvo Akademii Nauk USSR, Leningrad, Soviet Union.

Varela-Stokes, A. S., S. Y. Ludwig, L. H. Herbst, and E. C. Greiner. 2008. Helminth fauna of the nine-banded armadillo (Dasypus novemcinctus) in north-central Florida. Journal of Parasitology 94: 564–566. doi: 10.1645/ge-1346.1

Yeates, G. W., Z. Q. Zhao, R. A. Hitchmough, and I. A. N. Stringer. 2012. The conservation status of New Zealand Nematoda. New Zealand Entomologist 35: 128–130. doi: 10.1080/00779962.2012.686317