Sclerocollum saudii Al-Jahdali, 2010 (Acanthocephala: Cavisomidae) as a sentinel for heavy-metal pollution in the Red Sea

Abstract

Currently, fish helminth parasites, especially cestodes and acanthocephalans, are regarded as sentinel organisms to elucidate metal pollution in aquatic ecosystems. Here, 34 specimens of the fish Siganus rivulatus were collected in the Red Sea, from a seriously polluted, small lagoon named Sharm-Elmaya Bay, at Sharm El-Sheikh, South Sinai, Egypt; 22 (64.7%) were infected by Sclerocollum saudii (Acanthocephala: Cavisomidae). Thus, 22 natural infrapopulations (26-245 individuals) of this parasite were collected from infected fish. Samples of water and sediments from the bay, samples of muscle, intestine and liver from each fish, and samples from the parasite were taken for analysis of heavy metals (cadmium (Cd) and lead (Pb)). Both Cd and Pb concentrations in sediments were higher than those in water. The concentration of these metals were significantly higher in tissues (intestine, liver and muscle) of non-infected fish than those in infected fish, with Pb concentrations consistently higher than those of Cd, and both were drastically decreased in the order: liver > intestine > muscle. Metal concentrations in this acanthocephalan were much higher than those in its fish host. There were strong negative relationships between metal concentrations in tissues (intestine, liver and muscle) of infected fish and infrapopulation size, and between metal concentrations in the acanthocephalan and its infrapopulation size. These relationships strongly suggest competition for these metals between the fish host and its acanthocephalan parasite, and intraspecific competition among acanthocephalan individuals for available metals in the fish intestine. Bioconcentration factors were relatively high, since the mean Cd concentration in S. saudii was 239, 68 and 329 times higher than those in intestine, liver and muscle tissues, respectively, of its fish host. Also, mean Pb concentration was 55, 13 and 289 times higher than those in these tissues, respectively. The host-parasite system described here seems to be promising for biomonitoring of metal pollution in the Red Sea.

Acanthocephalan Worms Mitigate the Harmful Impacts of Heavy Metal Pollution on Their Fish Hosts

“…Similarly, acanthocephalan worms, due to their armed proboscises, adversely affect the health of their fish hosts by damaging the nature of intestinal tissue in these hosts at the attachment sites, causing severe histological and histopathological changes [15][16][17][18][19][20][21][22]. In contrast, several studies [13,23,24,31] have pointed to a beneficial impact of acanthocephalans on their fish hosts because these worms have much higher potential and capacity than their fish hosts to bioaccumulate different metals, especially the toxic ones, and thus can minimize the amounts of heavy metals in the tissues of these fish hosts. However, numerous studies [13,[26][27][28][29]32,34] revealed that metal concentrations in the tissues of acanthocephalan-infected fish were significantly less than those of uninfected conspecifics.…”

“…This process may affect the physiology of the fish hosts by lowering the amount of metals available in their intestine before absorption through the intestinal wall to other organs. If these metals are toxic, then the parasites have a beneficial impact on their fish hosts, by minimizing the amounts of these metals in their tissues [13,23,30,31]. Confirming this, several studies have shown that metal concentrations in the tissues of acanthocephalan-infected fish were significantly less than those of uninfected conspecifics [13,28,[32][33][34][35].…”

“…If these metals are toxic, then the parasites have a beneficial impact on their fish hosts, by minimizing the amounts of these metals in their tissues [13,23,30,31]. Confirming this, several studies have shown that metal concentrations in the tissues of acanthocephalan-infected fish were significantly less than those of uninfected conspecifics [13,28,[32][33][34][35].…”

“…This accumulation can cause severe tissue damage, various biochemical and functional disorders, and serious chronic diseases in these organs [3][4][5][6]. Liver is one of the major metabolically active organs in the body and is the main detoxification site, and its tissue tends to accumulate higher levels of heavy metals than any other tissues in the body [7][8][9][10][11][12][13]. Acanthocephala is a small phylum of mesoparasitic and gonochoristic worms.…”

“…Over the years 1995-2020, a large number of valuable studies have demonstrated that fish helminth parasites, especially those that do not have a digestive tract (i.e., acanthocephalans and cestodes), actively use their tegument to absorb nutrients from the fish'sintestine. Thus, these helminthsare good sentinels for trace metal pollution in aquatic environments since they have much higher potential and capacity than their fish hosts to bioaccumulate different metals, especially toxic ones, from the fish's intestine [13,[23][24][25][26][27][28][29]. This process may affect the physiology of the fish hosts by lowering the amount of metals available in their intestine before absorption through the intestinal wall to other organs.…”