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- Intraspecific genetic lineages of a marine mussel show behavioural divergence when exposed to microplastic leachatesPublication . Cozzolino, Lorenzo; Nicastro, Katy R; Hubbard, Peter; Seuront, Laurent; McQuaid, Christopher D.; Zardi, Gerardo IWorldwide, microplastic pollution has numerous negative implications for marine biota, exacerbating the effects of other forms of global anthropogenic disturbance. Mounting evidence shows that microplastics (MPs) not only cause physical damage through their ingestion, but also act as vectors for hazardous compounds by leaching absorbed and adsorbed chemicals. Research on the effects of plastic pollution has, however, largely assumed that species respond uniformly, while ignoring intraspecific diversity (i.e., variation within a single species). We investigated the effects of plastic leachates derived from factory-fresh (virgin) and beached microplastics on the behavioural responses of two genetic lineages of the Mediterranean mussel Mytilus galloprovincialis. Through laboratory behavioural experiments, we found that during exposure to leachates from beached microplastics (beached MPLs), Atlantic specimens moved significantly less than Mediterranean individuals in terms of both (i) proportion of individuals responding through movement and (ii) net and gross distances crawled. In contrast, no significant intraspecific differences were observed in the behaviour of either adults or recruits when exposed to MPLs from virgin microplastics (virgin MPLs). Additionally, the reception of cues from three amino acids (Lcysteine, proline and L-leucine) at increasing concentrations (10-5 M to 10-3 M in charcoal-filtered seawater) was tested by electrophysiological analysis using mussels exposed to beached MPLs or control seawater. We found significant intraspecific differences in response to 10-3 M L-cysteine (regardless of treatment) and 10-4 M L-cysteine (in mussels exposed to beached MPLs) and to 10-3 M proline (in mussels exposed to beached MPLs) and 10-5 M L-leucine. Our study suggests that intraspecific variation in a marine mussel may prompt different responses to plastic pollution, potentially triggered by local adaptation and physiological variability between lineages. Our work highlights the importance of assessing the effects of intraspecific variation, especially in environmental sentinel species as this level of diversity could modulate responses to plastic pollution.
- GABA receptors in the olfactory epithelium of the gilthead seabream (Sparus aurata)Publication . Costa, Rita; Velez, Zélia; Hubbard, PeterExposure to high PCO2/low pH seawater induces behavioural alterations in fish; a possible explanation for this is a reversal of Cl-/HCO3- currents through GABAA receptors (the GABAA receptor theory). However, the main evidence for this is that gabazine, a GABAA receptor antagonist, reverses these effects when applied to the water, assuming that exposure to systems other than the CNS would be without effect. Here, we show the expression of both metabotropic and ionotropic GABA receptors, and the presence of GABAA receptor protein, in the olfactory epithelium of gilthead seabream. Furthermore, exposure of the olfactory epithelium to muscimol (a specific GABAA receptor agonist) increases or decreases the apparent olfactory sensitivity to some odorants. Thus, although the exact function of GABAA receptors in the olfactory epithelium is not yet clear, this may complicate the interpretation of studies wherein water-borne gabazine is used to reverse the effects of high CO2 levels on olfactory-driven behaviour in fish.
- Independent effects of seawater pH and high P-CO2 on olfactory sensitivity in fish: possible role of carbonic anhydrasePublication . Velez, Zélia; Costa, Rita; Wang, Wenjing; Hubbard, PeterOcean acidificationmay alter olfactory-driven behaviour in fish by direct effects on the peripheral olfactory system; olfactory sensitivity is reduced in CO2-acidified seawater. The current study tested whether this is due to elevated P-CO2 or the consequent reduction in seawater pH and, if the former, the possible involvement of carbonic anhydrase, the enzyme responsible for the hydration of CO2 and production of carbonic acid. Olfactory sensitivity to amino acids was assessed by extracellularmulti-unit recording from the olfactory nerve of the gilthead seabream (Sparus aurata L.) in normal seawater (pH similar to 8.2), and after acute exposure to acidified seawater (pH similar to 7.7) but normal P-CO2 (similar to 340 mu atm) or to high P-CO2 seawater (similar to 1400 mu atm) at normal pH (similar to 8.2). Reduced pH in the absence of elevated P-CO2 caused a reduction in olfactory sensitivity to L-serine, L-leucine, L-arginine and L-glutamine, but not L-glutamic acid. Increased P-CO2 in the absence of changes in pH caused reduced olfactory sensitivity to L-serine, L-leucine and L-arginine, including increases in their threshold of detection, but had no effect on sensitivity to L-glutamine and L-glutamic acid. Inclusion of 1 mmol l(-1) acetazolamide (a membrane-permeant inhibitor of carbonic anhydrase) in the seawater reversed the inhibition of olfactory sensitivity to L-serine caused by high P-CO2. Ocean acidification may reduce olfactory sensitivity by reductions in seawater pH and intracellular pH (of olfactory receptor neurones); the former by reducing odorant-receptor affinity, and the latter by reducing the efficiency of olfactory transduction. The physiological role of carbonic anhydrase in the olfactory receptor neurones remains to be explored.
- Physiology, endocrinology and chemical communication in aggressive behaviour of fishesPublication . Silva, Melina da; Canario, Adelino; Hubbard, Peter; Goncalves, David Manuel FloresFishes show remarkably diverse aggressive behaviour. Aggression is expressed to secure resources; adjusting aggression levels according to context is key to avoid negative consequences for fitness and survival. Nonetheless, despite its importance, the physiological basis of aggression in fishes is still poorly understood. Several reports suggest hormonal modulation of aggression, particularly by androgens, but contradictory studies have been published. Studies exploring the role of chemical communication in aggressive behaviour are also scant, and the pheromones involved remain to be unequivocally characterized. This is surprising as chemical communication is the most ancient form of information exchange and plays a variety of other roles in fishes. Furthermore, the study of chemical communication and aggression is relevant at the evolutionary, ecological and economic levels. A few pioneering studies support the hypothesis that aggressive behaviour, at least in some teleosts, is modulated by "dominance pheromones" that reflect the social status of the sender, but there is little information on the identity of the compounds involved. This review aims to provide a global view of aggressive behaviour in fishes and its underlying physiological mechanisms including the involvement of chemical communication, and discusses the potential use of dominance pheromones to improve fish welfare. Methodological considerations and future research directions are also outlined.
- Ultra-low noise PEDOT:PSS electrodes on bacterial cellulose: A sensor to access bioelectrical signals in non-electrogenic cellsPublication . Inacio, Pedro M. C.; Medeiros, Maria C. R.; Carvalho, Tiago; Félix, Rute; Mestre, Ana; Hubbard, Peter; Ferreira, Quirina; Morgado, Jorge; Charas, Ana; Freire, Carmen S. R.; Biscarini, Fabio; Power, Deborah; Gomes, Henrique L.This study is focused on the particular advantages of organic-based devices to measure cells that do not generate action potentials, also known as non-electrogenic cells. While there is a vast literature about the application of organic conductors to measure neurons, cardiomyocytes and brain tissues, electrical measurements of non-electrogenic cells are rare. This is because non-electrogenic cells generate weak signals with frequencies below 1 Hz. Designing low noise devices in a millihertz frequency range is extremely challenging due to the intrinsic thermal and 1/f type noise generated by the sensing electrode. Here, we demonstrate that the coating of cellulose nanofibers with conducting PEDOT:PSS ink allows the fabrication of a nanostructured surface that establishes a low electrical double-layer resistance with liquid solutions. The low interfacial resistance combined with the large effective sensing area of PEDOT:PSS electrodes minimizes the thermal noise and lowers the amplitude detection limit of the sensor. The electrode noise decreases with frequency from 548 nV r.m.s at 0.1 Hz to a minimum of 6 nV r.m.s for frequencies higher than 100 Hz. This low noise makes it possible to measure low frequency bioelectrical communication signals, typical of non-electrogenic cells, that have until now been difficult to explore using metallic-based microelectrode arrays. The performance of the PEDOT:PSS-based electrodes is demonstrated by recording signals generated by populations of glioma cells with a signal-to-noise ratio as high as 140.
- What do oysters smell? Electrophysiological evidence that the bivalve osphradium is a chemosensory organ in the oyster, Magallana gigasPublication . Rato, Ana; Joaquim, Sandra; Matias, Domitília; Hubbard, PeterThe sensing of chemical cues is essential for several aspects of bivalve biology, such as the detection of food and pheromones. However, little is known about chemical communication systems in bivalves or the possible role of the osphradium as a chemosensory organ. To address this, we adapted an electrophysiological technique extensively used in vertebrates & mdash;the electro-olfactogram & mdash;to record from the osphradium in the Pacific oyster, Magallana gigas. This technique was validated using amino acids as stimulants. The osphradium proved to be sensitive to most proteinogenic l-amino acids tested, evoking tonic, negative, concentration-dependent 'electro-osphradiogram' (EOsG) voltage responses, with thresholds of detection in the range of 10(-)(6) to 10(-)( 5) M. Conversely, it was insensitive to l-arginine and l-glutamic acid. The current study supports the hypothesis that the osphradium is, indeed, a chemosensory organ. The 'electro-osphradiogram' may prove to be a powerful tool in the isolation and characterization of pheromones and other important chemical cues in bivalve biology.
- Bile acids as putative social signals in Mozambique tilapia (Oreochromis mossambicus)Publication . Ashouri, Samyar; Da Silva, José Paulo; Canario, Adelino; Hubbard, PeterChemical cues provide potential mates with information about reproductive status and resource-holding potential. In the Mozambique tilapia (Oreochromis mossambicus), males can distinguish female reproductive status through chemical cues, and accessibility of males to females depends on their position in the hierarchy, determined in part by chemical cues. Here, we hypothesized that tilapia faecal cues are attractive to conspecifics once released into the water. C18 solid-phase extracts of faeces from dominant males and pre-ovulatory females evoked stronger olfactory epithelium electrical responses (EOG) than, respectively, subordinate males and postspawning females. Mass spectrometry of the reverse-phase C18 high-performance liquid chromatography fractions of these extracts with highest EOG, identified by amino acids and bile acids. Faeces from pre-ovulatory females contain significantly higher concentrations of cholic acid (CA) and taurocholic acid (TCH) than both post-spawning females and males. A pool of amino acids had no effect on aggression or attraction in males. However, males were attracted to the scent of pre-ovulatory female faeces, as well as CA and TCH, when applied separately. This attraction was accompanied by increased digging behaviour compared to the odour of postspawning females. CA and TCH exert their action through separate receptor mechanisms. These findings are consistent with a role for faeces - and bile acids therein - in chemical communication in this species, acting as an attractant for males to reproductive females.
- Extracellular multi-unit recording from the olfactory nerve of teleostsPublication . Hubbard, Peter; Velez, ZéliaRecent studies have shown that ocean acidification affects olfactory-driven behavior in fish. This may be due in part to a reduction in olfactory sensitivity in high PCO2/low pH water. To assess the effects of ocean acidification, or olfactory sensitivity in marine fish in general, we propose that extracellular multi-unit recording from the olfactory nerve is the method of choice. Although invasive, it is sensitive, robust, reproducible and independent of external salinity (unlike the electro-olfactogram [EOG], for example). Furthermore, it records a primary sensory input into the CNS, prior to any central processing. We show that this method can show a reduction in olfactory sensitivity that is both temporary and odorant-dependent, using a range of amino acids to construct concentration-response curves and calculate the thresholds of detection.
- Anatomy of the olfactory system and potential role for chemical communication in the sound‐producing lusitanian toadfish, halobatrachus didactylusPublication . Modesto, Teresa; Gregório, Beatriz Neves; Marcelino, Gonçalo; Marquet, Nathalie; Costa, Rita; Guerreiro da Costa Guerreiro, Pedro Miguel; Velez, Zélia; Hubbard, PeterThe current study investigated the structure and function of the olfactory system of the Lusitanian toadfish, Halobatrachus didactylus, using histology and electrophysiology (electro-olfactogram [EOG]), respectively. The olfactory system consists of a digitated anterior peduncle, of unknown function, containing the inhalant nostril. This then leads to a U-shaped olfactory chamber with the olfactory epithelium-identified by G(alpha olf)-immunoreactivity-on the ventral surface. A large lacrimal sac is connected to this tube and is likely involved in generating water movement through the olfactory chamber (this species is largely sedentary). The exhalent nostril lies by the eye and is preceded by a bicuspid valve to ensure one-way flow of water. As do other teleosts, H. didactylus had olfactory sensitivity to amino acids and bile acids. Large-amplitude EOG responses were evoked by fluid from the anterior and posterior testicular accessory glands, and bile and intestinal fluids. Anterior gland and intestinal fluids from reproductive males were significantly more potent than those from non-reproductive males. Male urine and skin mucus proved to be the least potent body fluids tested. These results suggest that chemical communication-as well as acoustic communication-may be important in the reproduction of this species and that this may be mediated by the accessory glands and intestinal fluid.
- Minimizing the time to evaluate pheromone‐mediated reduction of aggressive behavior in Mozambique tilapia (Oreochromis mossambicus)Publication . Ashoori, Samyar; Hubbard, Peter; Canario, Adelino