Subtle Effects of Biological Invasions: Cellular and Physiological Responses of Fish Eating the Exotic Pest Caulerpa racemosa

Abstract

The green alga Caulerpa racemosa var. cylindracea has invaded Mediterranean seabed including marine reserves, modifying the structure of habitats and altering the distributional patterns of associated organisms. However, the understanding of how such invasion can potentially affect functional properties of Mediterranean subtidal systems is yet to be determined. In this study, we show that C. racemosa changes foraging habit of the native white seabream, Diplodus sargus. In invaded areas, we found a high frequency of occurrence of C. racemosa in the stomach contents of this omnivorous fish (72.7 and 85.7%), while the alga was not detected in fish from a control area. We also found a significant accumulation of caulerpin, one of the main secondary metabolites of C. racemosa, in fish tissues. The level of caulerpin in fish tissues was used here as an indicator of the trophic exposure to the invasive pest and related with observed cellular and physiological alterations. Such effects included activation of some enzymatic pathways (catalase, glutathione peroxidases, glutathione S-transferases, total glutathione and the total oxyradical scavenging capacity, 7-ethoxy resorufin O-deethylase), the inhibition of others (acetylcholinesterase and acylCoA oxidase), an increase of hepatosomatic index and decrease of gonadosomatic index. The observed alterations might lead to a detrimental health status and altered behaviours, potentially preventing the reproductive success of fish populations. Results of this study revealed that the entering of alien species in subtidal systems can alter trophic webs and can represent an important, indirect mechanism which might contribute to influence fluctuations of fish stocks and, also, the effectiveness of protection regimes.

Concern about the spread of the invader seaweed Caulerpa taxifolia var. distichophylla (Chlorophyta: Caulerpales) towards the West Mediterranean

“…In this respect, it is worth noting that the harmful indole alkaloid caulerpin, produced by both the aquarium strain of C. taxifolia and by C. cylindracea, which is directly responsible for detrimental biological effects on native Mediterranean fauna (e.g. Felline et al, 2012), was not observed in Ctvd collected in its area of origin (Waterhouse Island, Australia) (Schwede et al, 1986). If confirmed for the Mediterranean populations, the absence of caulerpin might imply further biological differences between the two C. taxifolia alien strains, which might in turn correspond to different ecological effects on the resident biota.…”

Biomarker Approach in Marine Monitoring and Assessment: New Insights and Perspectives

“…Moreover, in the same studies [50,51] the exposure to the alga was also demonstrated to induce a) alteration of the activity of the Na + -K + -ATPase, which is responsible for the electrochemical gradient across the plasma membrane and it is critical for the osmotic balance of the cell, the resting membrane potential, and the excitable properties of muscle and nerve cells [54][55][56][57][58], b) neurotoxic effects, documented by acetylcholinesterase inhibition, and c) changes in the morphology of gonads. The observed alterations may cause detrimental health status and altered behaviour in the fish, potentially preventing the reproductive success of fish population [51].…”

“…Besides its application in chemical pollution monitoring and assessment, recently the usefulness of the biomarker approach has been demonstrated also for the detection of the impact of alien species in marine environments [50,51]. Alien species can cause severe changes in the ecosystem's functioning and are recently recognized as principal agents of global change [52].…”

“…In two recent studies [50,51] carried out along the Apulian coasts (Northern Ionian Sea, SE Italy) the authors found that C. racemosa changes foraging habit of the native white seabream, Diplodus sargus. In invaded areas, a high frequency of occurrence of C. racemosa in the stomach contents of this omnivorous fish was found in parallel with a significant accumulation of caulerpin, one of the main secondary metabolites of C. racemosa, in fish tissues.…”

“…The activation of antioxidant defences was further supported both in terms of induction of more sensitive oxidative biomarkers, i.e., glutathione S-transferases (GST) and glutathione, and as overall capability to neutralize ROS indicated by the Total Oxyradical Scavenging Capacity. Moreover, Felline et al [51], using micronucleus-frequencies as genotoxicity biomarker, were able to detect direct effects of algal compounds on the loss of DNA integrity, probably caused by the highly reactive intermediates produced during biotransformation and oxidative processes.…”