The anisakid third stage larvae

The anisakid third stage larvae are not strictly host specific and a wide range of marine teleost species may be found infected in most waters ranging from the Atlantic via the Mediterranean and the Pacific to the Antarctic area (Adroher et al., 1996; Mattiucci et al., 1998; McClelland and Martell, 2001). Third stage larvae of anisakid worms are mainly ingested by fish when they predate on the crustacean intermediate host or teleostean transport hosts. In the fish stomach larvae are activated and penetrate the stomach wall in order to seek residence in the peritoneal cavity, musculature or organs such as liver (Levsen and Lunestad, 2010; Mehrdana et al., 2014). Severe inflammatory reactions with tissue deformation, including marked cellular infiltration in the stomach wall and mucosa, of Atlantic cod has been associated with numerous penetrating A. simplex larvae (Levsen and Berland, 2012) and the term “stomach crater syndrome” was applied for this pathological reaction. Atlantic salmon and sea trout returning to rivers in Scotland, England and Wales were found infected with a high number of A. simplex larvae causing a “red vent syndrome”, characterized by haemorrhages and inflammation around the vent (Beck et al., 2008; Noguera et al., 2009). This species clearly provokes an inflammatory reaction in salmonids (Haarder et al., 2013) which first is seen as attraction of inflammatory bcl-2 family and partly encapsulation of the worm (Fig. 3A). Likewise, P. decipiens become encapsulated by host cells in cod muscle tissue (Fig. 3B) and C. osculatum in cod\'s livers (Fig. 3C and 3D) and it is believed that the mere presence of larvae in the tissues affect the normal function of these organs. A. simplex infections may be associated with the loss of condition of fish hosts, but in cases where the larvae are sequestered outside essential organs the effect may be less harmful. A. simplex liver infections in North Atlantic cod can be severe (Fig. 4A) but the effect on liver condition of the host may not be as devastating as expected from the worm load. Thus, a large part of the parasite\'s infrapopulation is located in an encapsulated state on the surface of the organs which may be observed when worms are removed by peeling off the surface layer of cod\'s livers. Anisakid nematode larvae such as P. decipiens and C. osculatum may affect the physiological state, health and survival of the host. Codworm infection of the fish muscle reduces swimming performance in smelt and eel which can lead to increased mortality in the wild (Sprengel and Lüchtenberg, 1991; Rohlwing et al., 1998). Excretions from P. decipiens contain several pentanols and pentanons and it has been suggested that these compounds act as local anaesthetics in the cod muscle during worm penetration (Ackman and Gjelstad, 1975) and effects on muscle contractility may therefore be expected. Reduced swimming abilities of a fish host will ease predation by marine mammals, including seals, whereby this pathogenicity factor will optimize the life cycle of anisakids. Decreased body mass indices were recorded in Antarctic ice-fishes carrying high burdens of C. osculatum larvae which may indicate a parasite induced host effect (Santoro et al., 2013). In recent years Danish and Polish investigators (Buchmann and Kania, 2012; Mehrdana et al., 2014; Horbowy et al., 2016) have documented a marked increase of P. decipiens and C. osculatum infections of Baltic cod when compared to studies in the 1970s and 1980s (Möller, 1975; Thulin et al., 1989; Myjak et al., 1994) when seal abundance was low. The cod living in the Southern Baltic area may be infected by up to several hundred third stage larvae of C. osculatum (Haarder et al., 2014; Mehrdana et al., 2014; Nadolna and Podolska, 2014) which may challenge integrity and function of this key organ and affect growth and the nutritional state (Mehrdana et al., 2014; Zuo et al., 2016). Although the tissue disturbance by C. osculatum larvae is significant, even in a relatively well nourished cod liver (Fig. 4B), the impact is more prominent when liver size has decreased (Fig. 4C). Such a negative association was already claimed by Petrushevski and Shulman (1955) studying C. osculatum infection of Baltic cod in the 1940s and 1950s. A negative association between high parasite loads and the fish population size was noted by Eero et al., 2015 demonstrating reduced abundance of larger cod, concomitant with increasing worm occurrence, despite successful recruitment of young cod. This notion was further substantiated by Zuo et al. (2016) who showed that young Baltic cod with a body length below 30cm were largely uninfected whereas cod larger than 30cm harbored severe worm burdens. It is nevertheless difficult from field data to separate the potential parasite-related effects on condition and liver indices from more manageable impacts such as feed availability (Buchmann and Børresen, 1988). Therefore controlled laboratory trials must be performed in order to confirm this phenomenon.