Animal Diversity Web

Geographic Range

Due to its parasitic lifestyle, the geographic distribution of the marine trematode Euhaplorchis californiensis is intrinsically bound to the range of its multiple host species. The first intermediate host, the marine California hornsnail (Cerithidea californica), occurs in salt marshes and brackish waters along the coast of California and as far south as Baja California Sur. California killifish (Fundulus parvipinnis), the second intermediate host, have a more restricted distribution, and are common inhabitants of estuaries from southern California to Baja California. The higher relative vagility of the definitive hosts, composed of several genera of fish-eating birds, could potentially serve to maintain gene flow across populations of E. californiensis (Shaw, et al 2010). (Shaw, et al., 2010)

• Biogeographic Regions
• pacific ocean
  • native

Habitat

The habitat of E. californiensis is dictated by its host species. This is true even for those brief life stages in which the parasite is free-living, as in such periods the parasite is engaged in the transition from one host to the next.

E. californiensis is a marine trematode, infecting species that occur in estuaries, salt marshes, and brackish pools along the west coast of southern North America. Martin (1950) first described the life cycle of the parasite. Adult worms infect the intestines of fish-eating birds, laying their eggs directly into the intestinal lumen. These eggs are subsequently passed into the environment within the bird’s feces. If the eggs fall into an environment containing the hornsnail C. californica, they may be consumed by the snail. The hatchling larval worm migrates to the snail’s digestive gland, where it undergoes several generations of asexual reproduction, producing clonal forms called rediae. Hundreds of rediae can infect a single snail. Following this period, rediae begin to produce the next stage of the life cycle: free-swimming forms called cercariae. Thousands of cercariae can emerge from a single snail every day, each one following environmental cues in an attempt to reach the next intermediate host. Upon encountering a California killifish, the cercaria bores into the skin of the fish and migrates through the body to the surface of the brain. Once at the brain, the parasite forms a hard cyst around itself, becoming a metacercaria. The life cycle is completed when a killifish infected by E. californiensis gets eaten by a bird. The metacercaria excysts, or breaks out of its shell, and migrates to the bird’s intestine. (Martin, 1950)

• Habitat Regions
• saltwater or marine

• Aquatic Biomes
• coastal
• brackish water

Physical Description

Like all trematodes, E. californiensis undergoes radical morphological changes from one life stage to the next. Martin (1950) recorded detailed observations of each life stage. The adult worm is small, ranging from 0.230 to 0.303 mm in length. The body shape is roughly ovoid, with the width averaging 0.115 mm at the widest point. Spines cover the worm’s cuticle in transverse rows, with their size diminishing in the posterior third of the body. The oral sucker is subterminal and ventral: it occurs just posterior to the leading edge of the body on the ventral, or “belly,” portion of the worm. This sucker leads to a muscular pharynx, which connects to the esophagus. The esophagus, in turn, leads to the gut, which forks into a pair of ceca. The ceca of E. californiensis are very short in comparison with other trematodes, terminating anterior to the acetabulum. The acetabulum, or ventral sucker, is relatively inconspicuous and enclosed within the genital sac, and may be considered a vestigial trait. Being hermaphroditic, the adult E. californisensis possesses ovaries and a single testis.

Eggs, measuring only 0.016 x 0.028 mm, are produced in great numbers and expelled into the environment within the host bird’s feces (Gibson et al. 2008). After an egg is consumed by the California hornsnail, a miracidium emerges. Miracidia are tiny, teardrop-shaped larval forms covered in cilia. The miracidium penetrates the host snail's gut wall and migrates to the snail's digestive gland. Just outside the gland, the miracidium transforms into a sporocyst. The sporocyst has an amorphous, branching, baglike body, and does not possess a pharynx or locomotive capabilities. Over its lifespan, the sporocyst produces hundreds of rediae. Rediae, similar to the sporocyst, are essentially baglike animals, with the majority of the body devoted to a uterus-like sack in which germ balls develop into either daughter rediae or cercariae (Martin 1950). Unlike the sporocyst, rediae are much smaller, unbranched, possess a mouth, pharynx, and blind gut, and are capable of locomotion. Their size is widely variable, with length ranging from 0.165 to 0.536 mm and average width from 0.055 to 0.165 mm. Rediae migrate away from the digestive gland and into the gonadal tissues of the snail, where they begin to produce cercariae (Hechinger 2014, personal communication).

Cercariae emerge from a redia from a birth pore near the redia’s pharynx, and make their way out of the host snail’s shell and into the surrounding water. The cercaria, being a highly motile form, consists of a long, thin tail attached to the posterior of the body proper. The body of a cercaria is highly contractile, making determination of absolute length a difficult task. On average, cercariae have been found to range between 0.115 to 0.189 mm in length and 0.055 to 0.063 mm in width, including the tail. The tail, which is approximately 150% of the length of the body, possesses finlike structures called fin folds: one pair extends on the lateral surfaces of the tail for approximately half its length, with another pair covering the latter half of the dorsal and ventral surfaces and merging together at the tail’s tip. Besides the tail, the cercaria’s most conspicuous feature is its pair of dark eyespots that occur just posterior to the pharynx, at roughly one third the length of the body. These eyespots consist of melanin as a pigment and exhibit a surprising degree of complexity, including the presence of double lenses and multiple nerve fiber connections (Nadakal 1960). The surface of the body is covered in short spines arranged in a checkered pattern (Martin 1950).

Upon penetrating a killifish, the cercaria loses its tail and crawls through the fish’s body until it reaches the brain. Once there, it excretes a cystogenous material which hardens into a spherical shell around the parasite’s body. The cyst itself measures approximately 0.100 mm in diameter, and contains the metacercaria as it develops into a proto-adult. A mature metacercaria possesses a fully-developed digestive tract and rudimentary reproductive organs. Upon the consumption of the host killifish by an appropriate host bird, E. californiensis emerges from its cyst, migrates to the bird’s intestine, and completes development to a mature adult. (Gibson, et al., 2008; Martin, 1950; Nadakal, 1960)

• Other Physical Features
• ectothermic
• bilateral symmetry

• Range length

  0.230 to 0.303 mm

  0.01 to 0.01 in

• Average length

  0.261 mm

  0.01 in

Development

Like all trematodes, E. californiensis progresses through several life stages, all of which are markedly different from the others. E. californiensis passes through seven distinct stages of development.

Eggs are produced by adult worms within the small intestine of the definitive host--piscivorous birds-- and pass into the environment within the host’s feces. California hornsnails (C. californica) may subsequently consume the egg-laden feces. If they do, the eggs hatch into the next developmental stage: the miracidium.

Miracidia are tiny, ciliated animals resembling protists. After hatching, a miracidium penetrates the snail’s gut lining and swims to the digestive gland. Once there, it loses its cilia and transforms into a sporocyst.

The sole purpose of the sporocyst is to asexually produce the first generation of rediae, the next life stage. Rediae are produced inside the body of the sporocyst from tiny clusters of cells called germ balls. Once mature, the rediae emerge from the sporocyst through a pore and migrate to the snail’s gonad.

Unlike sporocysts, rediae have a mouth, a muscular pharynx, and a gut, all of which they put to use in the consumption of the snail’s gonadal tissues. Using the reproductive resources of the snail for their own proliferation, rediae asexually produce further generations of daughter rediae, which in turn either produce more rediae or the next life stage. This next stage is called the cercaria.

Cercariae are an infective stage: they are the form that seeks out and penetrates the next intermediate host, the California killifish (F. parvipinnis). Possessing a long, muscular tail, eyespots, and chemical sensory structures, the cercariae swim away from an infected snail and seek out environments in which killifish are found: shallow, brackish pools of relatively still water. When a cercaria finds and penetrates a killifish, it loses its tail and crawls through the fish’s body using its suckers. Once it reaches the fish’s brain, it encysts upon the meninges as a metacercaria.

The metacercaria is a semi-dormant, developmental stage. In this stage, the body of the worm is surrounded by a hard shell. Inside the shell, the worm is developing into a proto-adult. Its digestive system transitions to its final, adult form, and reproductive structures begin to emerge. Though non-motile, metacercariae are nonetheless infective: it is this stage which passes the infection from the intermediate killifish host to the definitive bird host.

When a piscivorous bird consumes a killifish, the metacercaria hatches out of its cyst. No longer resembling its previous cercaria form, this freshly-hatched worm is essentially a young, semi-developed adult. It exits the bird’s stomach and migrates to the small intestine, where it latches onto the intestinal wall and completes development to an adult.

Adult worms are assumed to obtain nutrients from the bird’s chyme, which is the viscous, semi-fluid mass of partially digested food passed from the stomach to the small intestine. In addition, it is possible that intestinal tissues are also consumed. Once their reproductive organs are fully formed, they begin laying eggs directly into the intestinal lumen, where they pass out of the bird within the feces (Martin 1950). (Martin, 1950)

• Development - Life Cycle
• metamorphosis

Reproduction

Little is known about the reproductive behaviors of adult E. californiensis. The adults are known to be hermaphroditic, and most likely reproduce by cross-fertilization with other conspecifics within the definitive host’s intestines (Wong 1954). The mechanism for seeking out a mate remains unknown. (Wong, 1954)

While sexual reproduction occurs only within the definitive host, E. californiensis undergoes asexual reproduction within its first intermediate host. Upon being consumed by a California hornsnail, an egg hatches into a miracidium, which subsequently transforms into a primary sporocyst within the digestive gland. The primary sporocyst then produces rediae from clumps of cells called germ balls. The germ balls develop inside the body of the sporocyst, only emerging when they have matured. Rediae migrate away from the digestive gland and into the gonad of the snail, where they go through several generations of asexual reproduction, producing more rediae. Rediae, like the sporocyst, produce clonal offspring by the development of germ balls within their bodies. The germ balls of rediae are capable of developing into one of two offspring forms: another redia, or the tailed cercaria that seeks out the next host (Martin 1950). Given the successive generations of asexually-produced larvae, a single egg eaten by a California hornsnail can give rise to hundreds of thousands of infective cercariae.

The period of time from egg to gravid adulthood can be highly variable, due to the complex nature of the worm's life cycle and the potentially long periods of persistence for the intermediate stages.

Like all digenean trematodes, the adult E. californiensis produces enormous quantities of eggs, often hundreds per day. These eggs are passed into the environment within the host’s feces. Even mild infestations of a few dozen worms can thus cause the passage of hundreds of thousands of eggs per day into the environment (Shaw 2010). (Martin, 1950; Shaw, et al., 2010)

• Key Reproductive Features
• iteroparous
• year-round breeding
• simultaneous hermaphrodite
• sexual
• asexual
• fertilization
  • internal
• oviparous

• Breeding interval

  Adult E. californiensis produce eggs continuously throughout their reproductive life.

• Breeding season

  It is unknown whether E. californiensis shows seasonal variation in egg production.

E. californiensis displays no parental investment in its offspring, instead relying upon the production of enormous numbers of offspring in order to pass on its genetic material (Martin 1950). Thus, E. californiensis could be said to be heavily r-selected. (Martin, 1950)

• Parental Investment
• no parental involvement

Lifespan/Longevity

As a heavily r-selected species, Euhaplorchis californiensis experiences extremely high mortality rates in many of its life stages. Like most trematodes, adult E. californiensis worms are capable of producing hundreds to thousands of eggs in a single day. These eggs are released into the environment, where the vast majority will never be encountered by a California hornsnail (Cerithidea californica), the worm’s first host. Those eggs that do become ingested by the California hornsnail can eventually transform into rediae, clonally-produced larvae which are capable of living for as long as their host snail, potentially years (Martin 1950). The rediae produce the next life stage—cercariae. Cercariae are free-swimming larvae with a lifespan of less than 24 hours. Thousands of cercariae emerge from a single snail within a day, and almost none of them encounter the next host, a California killifish (Fundulus parvipinnis). Those few that are able to successfully infect a killifish transform into a metacercaria and encyst upon the fish’s brain. The maximum lifespan of a metacercaria is currently unknown, but in practice is likely limited by the lifespan of its host. It is unknown what proportion of metacercariae is successfully transmitted to the definitive host, piscivorous birds (Lafferty 2008, Shaw et al. 2010). Those that do survive the process of trophic transmission become adult worms. The lifespan of adult E. californiensis has yet to be measured. Adult trematode worms have been known to live from several months to years. (Lafferty, 2008; Martin, 1950; Shaw, et al., 2010; Lafferty, 2008; Martin, 1950; Shaw, et al., 2010)

Behavior

Each life stage displays markedly different behaviors. Upon being consumed by the California hornsnail (C. californica), the egg hatches into a tiny, ciliated miracidium. The miracidium bores through the gut lining and seeks out the snail’s digestive gland, where it transforms into a sporocyst. The sporocyst is non-motile, and asexually produces the “primary” infective stage within the snail: the redia. Rediae are capable of locomotion and consuming snail tissues, and migrate to the snail’s gonad, where they asexually produce either daughter rediae or the next life stage: cercariae. A cercaria possesses a long tail, and is capable of swimming away from the snail in search of the next host. Cercariae are positively phototactic, meaning they swim toward light. They are also capable of following chemical gradients toward their second intermediate host, the California killifish (F. parvippinis). Upon encountering a killifish, a cercaria penetrates the fish’s skin, sheds its tail, and migrates through the fish’s tissues to the surface of the brain, where it forms a hard shell around itself and becomes a metacercaria (Martin 1950).

The metacercariae of E. californiensis are notable for their ability to control the behavior of their host fish, to an extent. Though the mechanism of this behavioral modification is not yet known, it has been suggested that the larvae secrete neurotransmitters involved in stress-response, such as monamines like serotonin (Shaw 2009).

Little is known about the behavior of adult worms within the intestines of their host. It is known that adults are capable of locomotion and orienting themselves within the optimum environment within the host, as well as finding other adult E. californiensis in order to mate (Wong 1954). (Martin, 1950; Shaw, et al., 2009; Wong, 1954)

• Key Behaviors
• parasite

Home Range

As a parasite, E. californiensis does not possess a home range. However, interspecies competition for host colonization could be considered analogous to territory defense. In studies of competitive exclusion of trematode larvae by various species that infect the California hornsnail, E. californiensis was found to be easily displaced by other species. This is likely due to the small size of E. californiensis relative to other trematodes (Sousa 1993). (Sousa, 1993)

Communication and Perception

Little is known about the sensory perceptions of many trematode species, including E. californiensis. The senses of parasites are, by necessity, tuned to the location of hosts or environments in which hosts occur. As such, environmental cues such as light intensity and orientation, chemical gradients, gravity, and temperature are likely commonly used by trematodes to orient themselves to host-rich areas (Sukhdeo & Sukhdeo, 2004). In the case of E. californiensis, few sensory studies have been performed. Smith and Cohen (2012) provided evidence that the cercariae of E. californiensis exhibit phototactic behavior: they orient toward and swim in the direction of light sources. As the host which they are seeking, the killifish, occurs in relatively shallow waters, this behavior has a logical origin. It is unknown whether cercariae use other cues such as water pressure, temperature, chemical cues, or other factors to better locate their hosts, but evidence from other species of trematode indicates that this is likely.

The sensory perceptions of other life stages of E. californiensis are unknown. The rediae, within the snail first intermediate host, likely have some mechanism of finding and staying in the vicinity of the snail’s digestive gland. Likewise, adult worms somehow follow cues allowing them to localize in the intestines of their host birds, as well as find other conspecifics with which to mate within those intestines. It remains to be seen how these behaviors are directed. (Smith and Cohen, 2012; Sukhdeo and Sukhdeo, 2004)

• Communication Channels
• chemical

• Perception Channels
• visual
• chemical

Food Habits

As a parasitic species, E. californiensis obtains all of its nutritional needs from its various hosts. Upon being consumed by a California hornsnail, the egg of E. californiensis hatches into a mother redia and invades the digestive gland of the snail. From there, the resultant generations of clonal daughter rediae invade the snail’s gonad (Sousa 1993). Rediae consume gonadal and surrounding tissue, effectively castrating their host. The snail remains castrated for the duration of infection, which can span a lifetime. Some daughter rediae produce cercariae, the free-swimming form which seeks out the next host. Cercariae are very short-lived, with lifespans of less than 24 hours. Though possessing rudimentary digestive organs, cercariae do not take in any nutrition. If a cercaria is unable to find a killifish host within 24 hours, it will die. For those cercariae able to find a killifish and successfully infect it, the cercarial life stage ends upon encystation on the fish’s brain. At that point, the parasite becomes a metacercaria, and obtains nutrients from the killifish through the cyst wall. In the final, adult stage of the parasite’s life, it attaches to the intestinal wall of the host bird and obtains nutrients directly from the passing chyme (Martin 1950). (Martin, 1950; Sousa, 1993)

• Primary Diet
• carnivore
  • eats body fluids

• Animal Foods
• body fluids
• mollusks

Predation

Many organisms prey upon the cercariae of E. californiensis, including zooplankton, filter feeders, and planktivorous fishes. As thousands of cercariae can emerge from a single infected snail in a single day, cercariae have the potential to be important prey items. The trophic interactions of E. californiensis larvae are a subject of ongoing study. It is known that larval trematodes are capable of greatly influencing the flow of energy within their food webs (Kaplan et al. 2009, Lafferty 2008).

In addition, other life stages of E. californiensis can be victims of unintentional predation if their host species are consumed by non-host predators. For example, California hornsnails are hunted by several species of crab. If a crab consumes an infected snail, the worms parasitizing it will be unable to pass on their genes. (Kaplan, et al., 2009; Lafferty, 2008)

• Known Predators

  • zooplankton
  • filter-feeding species
  • planktivorous fish

Ecosystem Roles

A notable feature of the ecology of Euhaplorchis californiensis is its ability to usurp the body of its intermediate hosts in order to serve its own reproductive ends. Upon successfully infecting its first intermediate host—the California hornsnail (Cerithidea californica)— E. californiensis consumes the snail’s gonad, castrating it. Evolutionarily, this kills the host. As such, the snail becomes an extended phenotype of the worm, existing only to serve the ends of its parasite (Lafferty & Kuris 2009, Hechinger et al. 2009, Hechinger 2010). The effect of parasitic castrators upon an ecosystem is the subject of intensive current study.

Beyond forcing the first intermediate host into the role of extended phenotype, E. californiensis exerts another pressure upon its ecosystem: the behavioral manipulation of its second intermediate host, the California killifish (Fundulus parvipinnis). Killifish infected with E. californiensis metacercariae have been found to be 30 times more susceptible to predation by piscivorous birds than uninfected conspecifics (Lafferty & Morris 1996). This alteration of predation probability has been found to have significant effects upon ecosystems containing E. californiensis. It has been hypothesized that piscivorous birds that primarily predate killifish receive the majority of their nutritional intake from infected fish. Such benefits almost certainly outweigh the costs exacted by adult E. californiensis that eventually infect those birds, calling into question the definition of a parasite as an organism existing at the expense of its host. In the case of E. californiensis, it is likely that its definitive hosts directly benefit by its presence in their environment (Lafferty 2008).

The free-swimming larvae generated by infected hornsnails has also been found to be an important food source for planktivorous fishes within estuaries. Fish readily prey upon cercariae, and millions of cercariae can be present within a very small area (Kaplan et al. 2009). (Hechinger, et al., 2009; Hechinger, 2010; Kaplan, et al., 2009; Lafferty and Kuris, 2009; Lafferty and Morris, 1996; Lafferty, 2008)

• Ecosystem Impact
• parasite

Economic Importance for Humans: Positive

It is possible that ongoing research into the biochemistry of host manipulation by Euhaplorchis californiensis could yield important advances in the development of psychoactive drugs (Shaw et al. 2009).

Trematodes such as E. californiensis have also been studied for use as bioindicators of ecosystem health, especially in systems that have been influenced by human activity (Huspeni & Lafferty 2004, Whitney et al. 2007). (Huspeni and Lafferty, 2004; Shaw, et al., 2009; Whitney, et al., 2007)

• Positive Impacts
• research and education

Economic Importance for Humans: Negative

There are no known negative influences upon human economy by Euhaplorchis californiensis.

Conservation Status

Euhaplorchis californiensis is often extremely prevalent in its range, sometimes reaching 100% infection prevalence in its second intermediate host, Fundulus parvipinnis (Shaw et al. 2010). IUCN Red List has not yet evaluated E. californiensis, and it has no special conservation status in the United States. (Shaw, et al., 2010)

• IUCN Red List

  Not Evaluated

• US Federal List

  No special status

• CITES

  No special status

• State of Michigan List

  No special status

Other Comments

Though fairly limited in range, Euhaplorchis californiensis maintains an extremely high rate of infection of its hosts. In the first intermediate host, Martin (1950) found a prevalence of 15%, and noted even higher prevalences reported by other researchers. Such rates were noted to be surprisingly high. Shaw, et al. (2010) found even more dramatic rates within the second intermediate host; 94-100% of California killifish within their areas of study were infected with E. californiensis. The mean abundances, or average number of parasites per infected individual, have been consistently found to range between several hundred to over 1,000 (Lafferty & Morris 1996, Shaw et al. 2010). (Lafferty and Morris, 1996; Martin, 1950; Shaw, et al., 2010)

Contributors

Daniel Metz (author), Radford University, Karen Powers (editor), Radford University.

References

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