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  • Vocal repertoire and consistency of call features in the meagre Argyrosomous regius (Asso, 1801)
    Publication . Bolgan, Marta; Pereira, Beatriz P.; Crucianelli, Aurora; Mylonas, Constantinos C; Pousão-Ferreira, Pedro; Parmentier, Eric; Fonseca, Paulo J.; Amorim, Maria Clara P
    Passive Acoustic Monitoring (PAM) is a non-intrusive and cost-effective method capable of providing high-resolution, long-term information on the status and health of vocal populations and communities. To successfully monitor the same species over wide geographical and temporal scales, it is necessary to characterise the range of sound variability, as well as the consistency of sound features between populations. The meagre (Argyrosomus regius, Asso 1801) is an interesting case study because recent investigations suggest a wider vocal repertoire than previously described. In this study, meagre vocalizations were recorded and analysed from a variety of settings, ranging from rearing facilities to wild populations to provide a comprehensive characterisation of its vocal repertoire, while investigating the consistency of spawning sound features between populations. All sounds presented a similar acoustic structure in their basic unit (i.e. the pulse), while an important variability was found in the number of pulses; the meagre can emit sounds made of one single pulse or many pulses (up to more than 100). High level of overlap in the Principal Component Analysis made difficult to differentiate sound type clusters. Despite this, two sound types were identifiable: knocks (sounds from 1 to 3 pulses) and long grunts (sounds with more than 29 pulses). Discriminant Analysis carried out on PCA residuals showed that knock had the highest proportion of correct placement (92% of the observations correctly placed) followed by long grunts (80%). All other previously described sound types (intermediate grunt, short grunt and disturbance sounds) could not be separated and presented low levels of correct placement, suggesting that care should be taken when defining these as independent sound types. Finally, acoustic features consistency was found in meagre grunts emitted by different populations during spawning nights; statistical differences could be explained by recording settings and fish conditions. The results of this study provide important information for fostering PAM programs of wild meagre populations, while contributing to the discussion around the definition of fish sound types in vocal fish communities. Studies of this kind, which evaluate both variability and consistency of sound features, are of fundamental importance for maximising PAM efforts in the wild, at both the specific and the community level.
  • Chorusing Behaviour in the Lusitanian Toadfish: Should I Match My Neighbours' Calling Rate?
    Publication . Jordão, Joana; Fonseca, Paulo; Amorim, Maria Clara P
    Choruses have been described mostly in birds, anurans and insects but have been poorly studied in fish. Research in batrachoidid (toadfishes) species suggest vocal facilitation among neighbouring males, but whether chorusing fish present more complex interactions is unknown. In this study, we test the hypothesis that chorusing fish males compete actively to increase attractiveness to females. We first describe vocal interactions in natural choruses of Lusitanian toadfish males. Our analysis found positive correlations between the calling rates of neighbouring males in several occasions. However, we also found that males that showed an overall low vocal activity throughout the observation period exhibited peaks of increased calling activity when neighbours decreased their calling rate, suggesting an opportunistic maximisation of attractiveness. We further test with playback experiments how toadfish males adjust calling activity relative to their neighbours’. We observed that males silent at the time of the playbacks but who had an overall high vocal performance tended to start calling when exposed to playbacks in contrast to low-activity males. Playback experiments further showed that males initially calling at a high rate adjust their calling rate according to the neighbour’s vocal activity level, that is, they increased calling rate when exposed to a high calling rate and decreased it when confronted with a low calling rate. However, males calling at a low rate did not significantly alter their calling rate when presented with a low (similar) or higher calling rate, probably due to temporary physiological and/or ecological constraints. We argue that Lusitanian toadfish males tend to optimise calling effort in relation to their neighbours when they are actively advertising. Further studies are necessary to better understand vocal behaviour with increased chorus size.
  • Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish
    Publication . Vasconcelos, Raquel Ornelas; Amorim, Maria Clara Pessoa; Ladich, Friedrich
    Underwater noise pollution is an increasing environmental problem which might affect communication, behaviour, fitness and consequently species' survival. The most common anthropogenic noises in aquatic habitats derive from shipping. In the present study we investigated the implications of noise pollution from a ship on the sound detectability, namely of conspecific vocalizations in the Lusitanian toadfish, Halobatrachus didactylus. Ambient and ferry-boat noises were recorded in the Tagus River estuary (Portugal), as well as toadfish sounds, and their sound pressure levels determined. Hearing sensitivities were measured under quiet lab conditions and in the presence of these masking noises at levels encountered in the field, using the auditory evoked potentials (AEP) recording technique. The Lusitanian toadfish is a hearing generalist, with best hearing sensitivity at low frequencies between 50 and 200 Hz (below 100 dB re. 1 microPa). Under ambient noise conditions, hearing was only slightly masked at lower frequencies. In the presence of ship noise, auditory thresholds increased considerably, by up to 36 dB, at most frequencies tested. This is mainly because the main energies of ferry-boat noise were within the most sensitive hearing range of this species. Comparisons between masked audiograms and sound spectra of the toadfish's mating and agonistic vocalizations revealed that ship noise decreased the ability to detect conspecific acoustic signals. This study provides the first evidence that fishes' auditory sensitivity can be impaired by ship noise and that acoustic communication, which is essential during agonistic encounters and mate attraction, might be restricted in coastal environments altered by human activity.
  • Mating sounds in the two-spotted goby, Pomatoschistus flavescens: Effects of water temperature on acoustic features
    Publication . Millot, Morgane; Faria, Ana M.; Clara P Amorim, Maria
    Acoustic signals in teleost fishes play a fundamental role in reproduction. As fish are ectothermic animals, temperature has the potential to change their signal production and detection, with further implications for mating interactions. In this study, we describe the mating sounds made by the two-spotted goby, Pomatoschistus flavescens, for the first time and further investigate the effect of temperature on the acoustic features. Courtship sounds of 15 two-spotted goby males were recorded at three different temperatures: 16C, 19C, and 21C. As seen for other marine gobies, two-spotted goby produced two courtship sounds: drums and thumps. Drums showed similar acoustic features to other Pomatoschistus species already studied. Calling rates for both kinds of sound were not affected by the increases in temperature. However, pulse rate increased from 16Cto19C and stabilised between 19C and 21C, suggesting that two-spotted gobies reached their physiological limits at 19C. Spectral features were also affected by temperature, presenting higher values at 19C. Whether or not the observed changes in acoustic features with temperature lead to changes in mating remains to be addressed. Studies like the present one are fundamental to better comprehend how reproduction will be affected by global warming in soniferous fishes.
  • Predicting the effects of anthropogenic noise on fish reproduction
    Publication . Jong, Karen De; Forland, Tonje Nesse; Amorim, Maria Clara Pessoa; Rieucau, Guillaume; Slabbekoorn, Hans; Sivle, Lise Doksæter
    Aquatic animals use and produce sound for critical life functions, including reproduction. Anthropogenic noise is recognized as a global source of environmental pollution and adequate conservation and management strategies are urgently needed. It becomes therefore critical to identify the reproductive traits that render a species vulnerable to acoustic disturbances, and the types of anthropogenic noise that are most likely to impact reproduction. Here, we provide predictions about noise impact on fish reproduction following a two-step approach: first, we grouped documented effects of noise into three mechanistic categories: stress, masking and hearing-loss, and test which type of noise (continuous vs intermittent and regular vs irregular) was most likely to produce a significant response in each category with either ametaanalysis or a quantitative review, depending on data availability. Second, we reviewed existing literature to predictwhich reproductive traits would render fish most sensitive to stress, masking and hearing-loss. In step one, we concluded that continuous sounds with irregular amplitude and/or frequency-content (e.g. heavy ship traffic) were most likely to cause stress, and continuous sounds were also most likely to induce masking and hearing-loss. From step two we concluded that the vulnerability of a species to noise-induced stress will mainly depend on: (1) its potential to reallocate reproduction to more quiet times or locations, and (2) its vulnerability to masking and hearing-loss mainly on the function of sound communication in its reproductive behaviour. We discuss in which stages of reproduction fish are most likely to be vulnerable to anthropogenic noise based on these findings.
  • Sound production in the Meagre, Argyrosomus regius (Asso, 1801): intraspecific variability associated with size, sex and context
    Publication . Pereira, David; Vieira, Manuel; Pousão-Ferreira, Pedro; Candeias-Mendes, Ana; Barata, Marisa; Fonseca, Paulo; Amorim, Maria Clara Pessoa
    Many fish taxa produce sound in voluntary and in disturbance contexts but information on the full acoustic repertoire is lacking for most species. Yet, this knowledge is critical to enable monitoring fish populations in nature through acoustic monitoring.
  • Fish sounds and boat noise are prominent soundscape contributors in an urban European estuary
    Publication . Vieira, Manuel; Fonseca, Paulo; Amorim, Maria Clara P
    Passive acoustic monitoring is a valuable tool for non-intrusive monitoring of marine environments, also allowing the assessment of underwater noise that can negatively affect marine organisms. Here we provide for the first time, an assessment of noise levels and temporal soundscape patterns for a European estuary. We used several eco-acoustics methodologies to characterize the data collected over six weeks within May 2016 - July 2017 from Tagus estuary. Biophony was the major contributor dominated by fish vocalizations and the main driver for seasonal patterns. Maritime traffic was the major source of anthropogenic noise, with daily patterns monitored using 1584 Hz third-octave band level. This indicator avoided biophony and geophony, unlike other indicators proposed for the EU Marine Strategy Framework Directive. Furthermore, the frequency overlap between anthropophony and biophony demands precautionary actions and calls for further research. This study provides an assessment that will be useful for future monitoring and management strategies.
  • Detection of invasive fish species with passive acoustics: Discriminating between native and non-indigenous sciaenids
    Publication . Amorim, Maria Clara P; Wanjala, Joan A.; Vieira, Manuel; Bolgan, Marta; Connaughton, Martin A.; Pereira, Beatriz P.; Fonseca, Paulo J.; Ribeiro, Filipe
    Invasive alien species have been rising exponentially in the last decades impacting biodiversity and ecosystem functioning. The soniferous weakfish, Cynoscion regalis, is a recent invasive sciaenid species in the Iberian Peninsula and was first reported in the Tagus estuary in 2015. There is concern about its possible impacts on native species, namely the confamiliar meagre, Argyrosomus regius, as there is overlap in their feeding regime, habitat use, and breeding behaviour. Here, we characterised the sciaenid-like sounds recently recorded in the Tagus estuary and showed that they are made by weakfish as they have similar numbers of pulses and pulse periods to the sounds made by captive breeding weakfish. We further demonstrate that breeding grunts from weakfish and the native sciaenid, recorded either in captivity or Tagus estuary, differ markedly in sound duration, number of pulses and pulse period in the two species, but overlap in their spectral features. Importantly, these differences are easily detected through visual and aural inspections of the recordings, making acoustic recognition easy even for the non-trained person. We propose that passive acoustic monitoring can be a cost-effective tool for in situ mapping of weakfish outside its natural distribution and an invaluable tool for early detection and to monitor its expansion.
  • Assessment of fighting ability in the vocal cichlid Metriaclima zebra in face of incongruent audiovisual information
    Publication . Amorim, Maria Clara Pessoa; Fonseca, Paulo; Mathevon, Nicolas; Beauchaud, Marilyn
    Information transfer between individuals typically depends on multiple sensory channels. Yet, how multi-sensory inputs shape adaptive behavioural decisions remains largely unexplored. We tested the relative importance of audio and visual sensory modalities in opponent size assessment in the vocal cichlid fish, Metriaclima zebra, by playing back mismatched agonistic sounds mimicking larger or smaller opponents during fights of size-matched males. Trials consisted in three 5-min periods: PRE (visual), PBK (acoustic+visual) and POST (visual). During PBK agonistic sounds of smaller (high frequency or low amplitude) or larger (low frequency or high amplitude) males were played back interactively. As a control, we used white noise and silence. We show that sound frequency but not amplitude affects aggression, indicating that spectral cues reliably signal fighting ability. In addition, males reacted to the contrasting audio-visual information by giving prevalence to the sensory channel signalling a larger opponent. Our results suggest that fish can compare the relevance of information provided by different sensory inputs to make behavioural decisions during fights, which ultimately contributes to their individual fitness. These findings have implications for our understanding of the role of multi-sensory inputs in shaping behavioural output during conflicts in vertebrates.
  • Boat noise impacts Lusitanian toadfish breeding males and reproductive outcome
    Publication . Amorim, Maria Clara P; Vieira, Manuel; Meireles, Gabriela; Novais, Sara C; Lemos, Marco F.L.; Modesto, Teresa; Alves, Daniel; Zuazu, Ana; Lopes, Ana F.; Matos, André B.; Fonseca, Paulo J.
    Anthropogenic noise is a growing threat to marine organisms, including fish. Yet very few studies have addressed the impact of anthropogenic noise on fish reproduction, especially in situ. In this study, we investigated the impacts of boat noise exposure in the reproductive success of wild Lusitanian toadfish (Halobatrachus didactylus), a species that relies on advertisement calls for mate attraction, using behavioural, physiological and reproductive endpoints. Two sets of artificial nests were deployed in the Tagus estuary and exposed to either ambient sound or boat noise during their breeding season. Toadfish males spontaneously used these nests to breed. We inspected nests for occupation and the presence of eggs in six spring low tides (in two years) and assessed male vocal activity and stress responses. Boat noise did not affect nest occupation by males but impacted reproductive success by decreasing the likelihood of receiving eggs, decreasing the number of live eggs and increasing the number of dead eggs, compared to control males. Treatment males also showed depressed vocal activity and slightly higher cortisol levels. The assessment of oxidative stress and energy metabolism-related biomarkers revealed no oxidative damage in noise exposed males despite having lower antioxidant responses and pointed towards a decrease in the activity levels of energy metabolism-related biomarkers. These results suggest that males exposed to boat noise depressed their metabolism and their activity (such as parental care and mate attraction) to cope with an acoustic stressor, consistent with a freezing defensive response/behaviour. Together, our study demonstrates that boat noise has severe impacts on reproductive fitness in Lusitanian toadfish. We argue that, at least fishes that cannot easily avoid noise sources due to their dependence on specific spawning sites, may incur in significant direct fitness costs due to chronic noise exposure.