Mantle-shell complex reactions elicited by digenean metacercariae in Gaimardia trapesina (Bivalvia: Gaimardiidae) from the Southwestern Atlantic Ocean and Magellan Strait

Abstract

The host response to 3 different larval digeneans affecting Southwestern Atlantic and Magellanic populations of the bivalve Gaimardia trapesina (Lamarck, 1819) (Gaimardiidae) is described. Unencysted metacercariae of 2 species of Gymnophallidae and 1 species of Lepocreadiidae co-exist in the peripheral and general extrapallial spaces. Differences in host responses to stimuli generated by each parasite are described. Infections by Gymnophallidae gen. sp. 1 metacercariae elicit a mantle-shell complex reaction involving both alteration of the mantle epithelium (hyperplasia and metaplasia) and calcium carbonate deposition to form an incomplete calcareous covering of single larvae, comprising individual crystallites in an organic matrix. The calcareous covering covers only the posterior two-thirds of the larval body, having its anterior end free in the extrapallial space, which ensures survival of the larvae. The peculiar features of the host response result from a successful process of adjustment to the parasite's life cycle. Metacercariae of Gymnophallidae gen. sp. 2 occur in one or more small groups of up to 30 individuals, either in the general or in the peripheral extrapallial spaces. The outer mantle reaction includes hyperplasia and metaplasia of the epithelium adjacent to the larvae. Deposition of calcium carbonate did not occur. Lepocreadiidae gen. sp. metacercariae were observed exclusively in the general extrapallial space lodged in single shallow pits whose shape fit the parasite's body shape and size. In simultaneous infections, metacercariae of Gymnophallidae and Lepocreadiidae elicited different responses in an individual, which suggests that each parasitic entity involves a different stimulus to the host.

A complete Holocene record of trematode–bivalve infection and implications for the response of parasitism to climate change

“…An increase in trematode prevalence will have significant implications for ecological and human health. Increased gymnophallid trematode prevalence could harm populations of the dominant molluscan macrobenthos by castrating and consuming various organs of their molluscan intermediate hosts and potentially altering their behavior to make them more susceptible to their own predators (13,14,(18)(19)(20), thereby significantly altering the estuarine trophic web at multiple levels. Moreover, estuaries serve as nurseries for many commercially important marine fishes, and their juvenile populations are particularly sensitive to climatic variation (21).…”

“…1). These traces are readily preserved in the fossil record (10,13,14) and indicate that trematodes have indeed been completing their life cycle by infesting multiple invertebrate and vertebrate hosts in deep time. Trematodes are responsible for many diseases of both humans (e.g., schistosomiasis and swimmer's itch by freshwater Schistosomatidae) and nonhuman animals, but not all trematodes are known to induce traces in their hosts.…”

Parasites of Ammonoids

“…Nevertheless, various other parasitic organisms such as fungi, unicellular organisms, nematodes or arthropods (and their eggs) as well as various other irritants including inorganic material which get stuck between mantle and shell can induce pearl formation (Götting 1974(Götting , 1979Lauckner 1983). Nevertheless, the morphology of some parasite-induced structures in extant bivalves are believed to be very specific to parasitic flatworms such as pits in shells and igloo-shaped shell secretions or to polychaete worms such as borings and can be traced back in the fossil record (Liljedahl 1985, Ruiz andLindberg 1989;Ituarte et al 2001Ituarte et al , 2005Huntley 2007;De Baets et al 2011). Blister pearls (Fig.…”

Exploration of the Oxynoticeratidae ornamental morphospace using the discrete cosine transform (DCT) to analyze rib patterns

“…Additionally, the distribution, abundance, and shape of the pits resemble those of the ammonoids. The same holds true for the digenean− nuculoid/veneroid system studied by Ituarte et al (2001Ituarte et al ( , 2005. In this case, metacercarias formed tubes surrounded by bivalve pearls.…”

“…Nevertheless, Conway Morris (1981: 493) stated that "Pearls in recent molluscs arise from a variety of irritants, but in many instances the sources are trematode larvae". In Recent bivalves, trematode−induced pearls in the shell are typically formed by metacercariae of gymnophallids and have been documented for mytiloid, nuculoid, and veneroid bivalves (Götting 1979;Keupp 1986;Ituarte et al 2001Ituarte et al , 2005Littlewood and Donovan 2003). These trematode−induced pearls/pits together with spionid− induced borings are highly characteristic and can be recog− nised in the fossil record (cf.…”