Oxidative stress in native and invasive crustaceans related with
pollution and parasitism in a warming scenario
Aquatic organisms are exposed to multiple natural and anthropogenic stressors,
including pollution, parasites, invasive species and climate change. These factors
interact in a diversity of ways. However few studies consider realistic ecological
contexts taking into account the synergy between these factors on aquatic biota.
Increasing interest has been devoted to the interactions between parasitism and pollution
in aquatic ecosystems [1], but there are major gaps in knowledge of how these stressors
affect animal health [2]. For example, what are the physiological mechanisms
underlying the response of aquatic organisms to pollution and concurrent parasite
infection? Additional complexity is added by the effect of climate change which can
interact with both pollutants and parasites [3,4]. Furthermore, these stressors are
expected to affect differently the physiology of native and invasive species; invasive
species are likely to have a wider range of environmental tolerance [5].
The mechanisms of pollution-, parasitism- and temperature-induced health effects
involve oxidative stress [2,6,7]. Different enzymatic antioxidant mechanisms such as
superoxide dismutase (SOD), glutathione peroxidase (GPx) and catalase (CAT), as well
as non-enzymatic components (glutathione, carotenoids, ascorbate, etc), are used to
protect cells against oxidative stress in both vertebrates and invertebrates [7]. However,
when control mechanisms are insufficient, reactive oxygen species (ROS) can induce
damage at different levels. The evaluation of antioxidant defense mechanisms in aquatic
organisms is a useful measure of the capacity of detoxification from ROS caused by the
combined effect of endogenous (parasites) and environmental (pollution and climate
change) factors.
Brine shrimps Artemia spp. (Anostraca) are keystone organisms and essential link in
hypersaline coastal and inland systems around the world [8]; they are also an invaluable
resource in aquaculture worlwide [9]. Owing to their ability to bioaccumulate
pollutants, their wide geographic distribution, the availability of dried cysts, the ease of
laboratory culture and maintenance, their short life-cycle and high fecundity, Artemia
have become one of the most important test organisms for applied toxicology [10].
An excellent model system to study interactions between pollutants and parasites is the
highly parasitized Artemia parthenogenetica (hereafter AP) population from the Odiel
and Tinto estuary, one of the most polluted estuarine systems in Europe [11]. AP from
Odiel has extraordinarily high levels of cestode infection, mainly Flamingolepis
liguloides and Confluaria podicipina [12]. Both parasites induce strong physiological
and behavioural changes in Artemia [13,14] likely to affect its response to pollution.
Moreover this is one of the last native Artemia populations in the Iberian Peninsula,
most of which have been displaced by the American congener A. franciscana (hereafter
AF) [15]. This provides an exceptional opportunity to test for physiological mechanisms
explaining invasion resistance by comparing biomarkers of oxidative stress with AP and
AF populations from relatively unpolluted environments.
BIBLIOGRAPHY
[1] Sures B (2008) Environmental parasitology. Interactions between parasites and
pollutants in the aquatic environment. Xth EMOP, August 2008. Parasite 15, 434–438
[2] Marcogliese DJ, Brambilla LG, Gagné F, Gendron AD (2005) Joint effects of
parasitism and pollution on oxidative stress biomarkers in yellow perch Perca
flavescens. Dis Aquat Organ 63 (1): 77-84
[3] Noyes PD, MK McElwee, HD Miller, BW Clark, LA Van Tiem, KC Walcott KN
Erwin, ED Levin (2009) The toxicology of climate change: Environmental
contaminants in a warming world. Environment International, 35:971-986
[4] Okamura B, Feist SW (2011) Emerging diseases in freshwater systems. Freshwater
Biology 56:627-637
[5] Lejeusne C, Latchère O, Petit N, Rico C, Green AJ (2014) Do invaders always
perform better? Comparing response of native and invasive shrimps to temperature and
salinity gradients in south-west Spain. Estuarine, Coastal and Shelf Science 136: 102111.
[6] Vinagre C, Madeira D, Narciso L, Cabral HN, Diniz M (2012) Effect of temperature
on oxidative stress in fish: Lipid peroxidation and catalase activity in the muscle of
juvenile seabass, Dicentrarchus labrax. Ecological Indicators 23: 274-279
[7] Nunes B, Carvalho F, Guilhermino L (2006) Effects of widely used pharmaceuticals
and a detergent on oxidative stress biomarkers of the crustacean Artemia
parthenogenetica. Chemosphere 62 (4): 581-94
[8] Sánchez MI, Varo N, Green AJ, Ramos C, Amat J (2013)Cestodes change the
isotopic signature of brine shrimp hosts: implications for aquatic food webs. Int. J.
Parasitol 43(1):73-80
[9] Sorgeloos P, Dhert P, Candreva P (2001) Use of the brine shrimp, Artemia spp., in
marine fish larviculture. Aquaculture 200: 147–159
[10] Nunes BS, Carvalho FD, Guilhermino LM, Van Stappen G (2006) Use of the
genus Artemia in ecotoxicity testing. Environ Pollut. Nov;144(2):453-62.
[11] Grande JA, Borrego J, Morales JA (2000) A study of heavy metal pollution in the
Tinto-Odiel estuary in Southwestern Spain using factor analysis. Environmental
Geology 39: 1095-1101
[12] Sánchez MI, Nikolov PN, Georgieva DD, Georgiev BB, Vasileva G, Pankov P,
Paracuellos M, Lafferty K, Green AJ (2013) High prevalence and abundance of cestode
parasites throughout the annual cycle of Artemia salina and A. parthenogenetica in
coastal Spain: relationship with abundance of avian final hosts. Journal of Parasitology
112(5):1913-23
[13] Sánchez MI, Thomas F, Perrot-Minnot MJ, Bertrand-Michel J, Missé D (2009)
Neurological and physiological disorders in Artemia harboring manipulative cestodes.
Journal of Parasitology 95 (1): 20-24
[14] Sánchez MI, Georgiev BB, Green AJ (2007) Avian cestodes affect the behaviour of
their intermediate host Artemia parthenogenetica: an experimental study. Behavioural
Processes 74: 293-299
[15] Amat F, F Hontoria, O Ruiz, AJ Green, MI Sanchez, J Figuerola, F Hortas (2005)
The American brine shrimp as an exotic invasive species in the western Mediterranean.
Biological Invasions 7: 37-47