Effect of tapeworm parasitisation on cadmium toxicity in the bioindicator copepod, Cyclops strenuus

Highlights

• Infection of Cyclops strenuus with tapeworms increases cadmium induced mortality.

• Infection does not affect the accumulation of cadmium in Cyclops.

• Infection affects the use of crustaceans as bioindicators.

Abstract

The ubiquitous nature of crustaceans has meant that they have been considered as useful bioindicators of water quality. Although crustaceans e.g. Cyclops strenuus serve as intermediate hosts to many metazoan parasites, the effect of infection on toxicity of heavy metal pollution has not been established. The interaction between the procercoid stage of the tapeworm, Bothriocephalus acheilognathi, and its copepod host when exposed to cadmium toxicity was investigated. Exposure to 100 μg Cd/l caused a significant (P < 0.001) decrease in copepod survival of crustaceans exposed to combined parasite infection and metal treatment, compared with all other groups which had been exposed to these stressors individually. This effect was not dependent on infection intensity. Although cadmium could not be detected by EDXMA, optical emission spectroscopy revealed Cd accumulation in both treated uninfected and infected copepods. Overall, the data suggest that parasitic infection is an important consideration in determining the suitability of a bioindicator of water pollution.

Introduction

Copepods represent an essential part of the food chain in water and constitute a food source of aquatic animal fauna especially young fish (Ruppert and Barnes, 1994). Their ubiquitous nature has made them of interest as potential biomarkers of water quality, particularly as they are able to accumulate heavy metals (Dallinger, 1994). Cadmium, (Cd) which is a naturally occurring element, is also produced from a range of anthropomorphic activities e.g. mining from lead–zinc ore fields, electroplating and iron and steel manufacture. It has been ranked as high as seventh in the top 20 hazardous substances priority list by the Agency for Toxic Substances and Disease Registry, and the US Environmental Protection Agency (USEPA), and identified as a potential toxic element to different forms of life (Fay and Mumtaz, 1996). As Cd is not recycled in the environment, human exposure risk is increasing (Morselt, 1991) and usually arises in mammals through ingestion of contaminated food or water and/or inhalation. Cadmium concentration in unpolluted waters is generally between 0.01 and 0.1 μg/l although the highest Cd concentration (above 10,000 μg/l) has been reported in polluted estuarine and coastal waters in Foundry Cove, New York, USA in 1974 (Knutson et al., 1987). Numerous studies (e.g. Kraal et al., 1995, Weyts et al., 1997, Sunderman, 2001) have shown that because cadmium can cross cell membranes by interacting with membrane transporters it can have a range of physiological and pathological effects on animals.

Generally, toxicity of heavy metals in crustaceans varies depending on environmental factors such as temperature, pH and water hardness, in addition to the metal dose and the exposure time (Howard and Hacker, 1990, Sharp and Stearns, 1997, Das and Das, 2005). Whilst research on the relationship between heavy metal pollution and copepods has been somewhat limited, it has been shown that the mortality of copepods such as Diaptomus forbesi increases with increasing cadmium concentrations (Ghosal and Kaviraj, 2002). A similar toxic effect has also been observed with copper on the freshwater planktonic Cyclops viridis (Das and Das, 2005) and the estuarine calanoid copepods, Acartia tonsa and Temora longicornis (Sharp and Stearns, 1997). In seawater sediments, the acute toxicity of Cu, Ni and Zn has also been shown to affect the longevity of the estuarine harpacticoid copepod Amphiascus tenuiremis (Hagopian-Schlekat et al., 2001). This toxicity is not only limited to copepods; in other crustaceans such as adult grass shrimp, Palaemonetes pugio, exposure to low levels of Cd (1.5 and 2.5 μg/l) decreases survival particularly in gravid females compared to unexposed controls (Manyin and Rowe, 2008), and when Cd (10.5–82.1 μg/l) is applied to the freshwater amphipod Gammarus pulex for 11 days, mortality increases significantly with increasing metal concentrations (Felten et al., 2008). One factor that has received little attention is the possible effect that parasitisation may have on the complex heavy metal/crustacean interaction.

The majority of studies on the interactions between aquatic pollution, parasitisation and the host(s) have focused on the parasitic stage living inside the fish host (Sures, 2006, Sures, 2008a, Sures, 2008b, Marcogliese and Pietrcock, 2011, Costa et al., 2010), and yet several invertebrate hosts form a major component in metazoan parasite life cycles. For example, copepods are the first intermediate hosts of several cestode species such as Ligula intestinalis (Hoole et al., 2001, Hoole et al., 2010), Schistocephalus solidus (Wedekind, 1997) and Bothriocephalus acheilognathi (Hoole et al., 2001), and acanthocephalans such as Pomphorhynchus laevis, utilise amphipods such as G. pulex as an intermediate host (Hoole et al., 2001, Moore, 2002).

Sures and Radszuweit (2007) reported that crustaceans infected with parasites might be more susceptible to pollution than uninfected ones. In G. pulex infected with the acanthocephalan P. laevis, two weeks of Cd exposure was found to decrease the survival rate in both infected and uninfected individuals (Brown and Pascoe, 1989). Interestingly, although there was no significant difference in mortality between infected and uninfected gammarids exposed to 6 μg Cd/l, the rate of mortality increased significantly in the infected individuals exposed to a lower dose of the metal (2.1 μg/l) compared to uninfected animals. In addition, although there was no significant difference in the metal accumulation between infected and uninfected hosts, both Cd (Brown and Pascoe, 1989) and Pb (Siddall and Sures, 1998) levels were lower in the cystacanth stage of the parasite than in the gammarid host. Similarly, Cd and Pb have been detected in lower levels in the cystacanth of Acanthocephalus lucii than in the intermediate host Asellus aquaticus (Sures and Taraschewski, 1995).

The present paper assesses for the first time the effect of cadmium on the survival of Cyclops strenuus infected with the procercoid stage of the carp tapeworm, B. acheilognathi. In addition, optical emission spectrometer and X-ray analysis in conjugation with electron microscopy (EDXMA) were employed in an attempt to elucidate the distribution of the metal in the crustacean host and parasite.