Cryptic effects of biological invasions: Reduction of the aggressive behaviour of a native fish under the influence of an “invasive” biomolecule

Abstract

The invasive green alga Caulerpa cylindracea has become an important component of the diet of the Mediterranean white seabream Diplodus sargus. As a consequence of this “exotic diet”, the algal bisindolic alkaloid caulerpin accumulates in the fish tissues. Although the compound shows structural similarity to endogenous indolamines that modulate animal behaviour, the potential impact of caulerpin on fish behaviour still remains unexplored. In this report, behavioural experiments both on groups and on single fish responding towards a mirror were performed under different doses of dietary caulerpin. Differences between treated and control groups for each behaviour and for the overall aggressive pattern during the different experimental phases showed that the aggressiveness of D. sargus decreased with the administration of caulerpin. These results call the attention to a still unexplored potential ability of bioactive metabolites from marine invasive species, to alter the behaviour on native species, with putative negative effects on patterns of fish growth and population dynamics.

Under the canopy: Community-wide effects of invasive algae in Marine Protected Areas revealed by metabarcoding

“…For instance, they can alter food webs and the general functioning of the communities (e.g., Klein and Verlaque, 2010;Alomar et al, 2016;Cabanellas-Reboredo et al, 2010). The three species have also been shown to affect the fitness of herbivorous fish and sea urchins, including commercial species, through the ingestion of chemical compounds from the algae (Tejada et al, 2013;Felline et al, 2014;Magliozzi et al, 2017;Castanho et al, 2017). Thus, a complex pattern of direct and indirect effects emerges; however, few works have addressed the impacts on the smaller components of the communities like the present study.…”

Fishing for Targets of Alien Metabolites: A Novel Peroxisome Proliferator-Activated Receptor (PPAR) Agonist from a Marine Pest

“…In addition, the interaction of CAU with PPARα and PPARγ, both expressed in brain areas involved in regulation of behavioural and emotional processes in rodents [ 30 , 32 , 33 ], could also result in PPAR-mediated altered social behaviour of D. sargus . Indeed, dietary CAU is already known to reduce the aggressive behaviour of D. sargus [ 31 ]. Since small molecules must cross the BBB to have an effect on centrally-mediated behaviours, the high levels of CAU here detected in the fish brain suggest that, in addition to the metabolic alterations discussed above, behavioural responses to the C. cylindracea -based diet could also have substantial impact over time on D. sargus population structure and ecology.…”

“…Remarkably, the algal secondary metabolite caulerpin (CAU, Figure 1 a), which accumulates in the tissues of D. sargus and other edible Mediterranean fish species [ 11 , 12 , 16 , 17 , 18 , 23 ], shows several functional similarities to FFB since both compounds: (i) suppress activation of hypoxia-inducible factor-1 (HIF-1) [ 24 , 25 ], (ii) inhibit protein tyrosine phophatase-1B (PTP1B) [ 26 , 27 ] and (iii) show anti-inflammatory properties [ 28 , 29 ]. In addition, the PPARα-mediated effects of FFB on the social interaction of mice [ 30 ] can be paralleled to the ability of CAU of influencing the social behaviour in D. sargus [ 31 ]. However, despite considerable past efforts to identify the molecular targets of CAU, its possible direct interactions with PPARα, the main target of FFB, has not yet been investigated.…”

1H NMR Spectroscopy and MVA to Evaluate the Effects of Caulerpin-Based Diet on Diplodus sargus Lipid Profiles

“…These patterns could be explained with the gradually loss of appetite and voracity, due to an inadequate food intake, especially for the individuals fed with the highest dosage levels [ 27 ]. CAU shows structural similarity to endogenous indolamines that modulate animal behaviour and a reduction of aggressive behaviour was described in fish exposed to CAU high dose [ 28 ]. Moreover, as already reported in literature, this metabolite exerts a sedative effect via pathways involving serotonin 5-HT3 receptors [ 29 ].…”

“…It did not involve endangered or protected species and was conducted under the supervision of an accredited expert in laboratory animal science (following FELASA category C recommendations). Permission for capturing fish at the field site was granted by the Portuguese Environmental Agency (APA) and by local authorities (Cascais Environmental Agency—Cascais Ambiente—and Coast Guard—Capitania de Cascais) [ 28 ]. Juvenile fish were captured with hand nets in 2015 near Cascais, in the central Portugal region and transferred in constantly aerated tanks at ISPA-IU.…”