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- Vocal behavior predicts reproductive success in a teleost fishPublication . Vasconcelos, Raquel O.; Carrico, Rita; Ramos, Andreia; Modesto, Teresa; Fonseca, Paul J.; Amorim, M. Clara. P.The relation between acoustic signaling and reproductive success is important to understand the evolution of vocal communication systems and has been well studied in several taxa but never clearly shown in fish. This study aims to investigate whether vocal behavior affects the reproductive success in the Lusitanian toadfish (Halobatrachus didactylus) that relies on acoustic communication to attract mates. We recorded 56 nest-holding (type I) males during the breeding season and analyzed the calling performance and acoustic features of the mate advertising sounds (boatwhistles) exhibited over circa 2 weeks. Hormonal levels of the subjects and the number of eggs (reproductive success) present in the respective nests were quantified. Nesting males attracted both females and other males, namely smaller type I males with significantly lower total length (TL), body condition, sonic muscle mass, gonad mass, and accessory glands mass. Calling rate (CR), calling effort (CE) (% time spent calling), and sound dominant frequency were significantly higher in nesting males with clutches than in those without clutches. Sex steroids (11-ketotestosterone and testosterone) were not correlated with vocal parameters or number of eggs. Maximum CR and CE were the best predictors of the number of eggs. In addition, these vocal variables were best explained by male's TL, condition, and sonic muscle mass. We provide first evidence that vocal behavior significantly determines reproductive success in a vocal fish and show that acoustic signaling at higher and constant rates can operate as an indicator of the male's size and body condition and probably of elevated motivation for reproduction.
- The swimbladder of the Lusitanian toadfish: sexual dimorphism and hormonal controlPublication . Modesto, Teresa; Canario, Adelino V. M.; Castanõ, J. P.; Malagon, M. M.; Garcia Navarro, S.The members of the family Batrachoididae produce sounds associated with courtship and agonistic interactions. While long mating calls are only produced by nesting males, agonistic short duration grunts have been recorded from toadfishes and midshipmen in both males (nesting or not) and females. Sound production results from the contraction of paired sonic muscles attached to the walls of the swimbladder, which cause a rapid variation in swimbladder volume and internal pressure. Both sonic muscle growth and sonic fibre morphology have been shown to be androgen sensitive in batrachoidids.
- Effect of dietary l-glutamine supplementation on the intestinal physiology and growth during Solea senegalensis larval developmentPublication . Matias, Ana Catarina; Viegas, Ana Rita; Couto, Ana; Lourenço-Marques, Cátia; Aragão, Cláudia; Castanho, Sara; Gamboa, Margarida; Candeias-Mendes, Ana; Soares, Florbela; Modesto, Teresa; Pousão-Ferreira, Pedro; Ribeiro, LauraThe maturation of the intestinal digestive and absorptive functions might limit the amount of absorbed nutrients to fulfil the high requirements of the fast-growing marine fish larva. Glutamine (Gln) has been described to improve intestinal epithelium functions, due to its involvement in energy metabolism and protein synthesis. The purpose of this study was to evaluate dietary 0.2% Gln supplementation on aspects of intestinal physiology, protein metabolism and growth -related genes expression in Senegalese sole larvae. Experiment was carried out between 12 and 33 days post hatching (DPH) and fish were divided into two experimental groups, one fed Artemia spp. (CTRL) and the other fed Artemia spp. supplemented with Gln (GLN). GLN diet had two times more Gln than the CTRL diet. Samples were collected at 15, 19, 26 and 33 DPH for biometry, histology, and digestive enzymes activity, and at 33 DPH for gene expression, protein metabolism and AA content determination. Growth was significantly higher for Senegalese sole fed GLN diet, supported by differences on protein metabolism and growth -related gene expression. Slight differences were observed between treatments regarding the intestinal physiology. Overall, GLN diet seems to be directed to enhance protein metabolism leading to higher larval growth.
- Boat noise impacts Lusitanian toadfish breeding males and reproductive outcomePublication . Amorim, M. 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 receiv-ing eggs, decreasing the number of live eggs and increasing the number of dead eggs, compared to control males. Treat-ment 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.
- 17a,20ß,21-trihydroxy-4-pregnen-3-one: the probable maturation-inducing steroid of the lusitanian toadfishPublication . Modesto, Teresa; Canario, Adelino V. M.17,20 ,21-Trihydroxy-4-pregnen-3-one (17,20 ,21-P) was identified as the major metabolite of incubations of Lusitanian toadfish Halobatrachus didactylus ovarian follicles with [3H]-17hydroxyprogesterone. The potency of several steroids in inducing germinal vesicle breakdown of follicle-enclosed oocytes of Lusitanian toadfish was systematically examined by using an in vitro germinal vesicle breakdown (GVBD) bioassay. 17,20 -Dihydroxy-4-pregnen-3-one (17,20 -P) and 17,20 ,21-P, two confirmed maturation-inducing steroids (MIS) in teleosts, were the most potent in inducing GVBD with ED50s ranging between 9 and 271 nM. Structure-activity relationships followed similar patterns to what has been observed in similar bioassays, i.e. a vital requirement for 17- and 20 -hydroxyl groups in C21 steroids and a reduction in activity of 14 and 5–6%, respectively, for 5-pregnene and 5 -pregnanes compared to 4-pregnenes. Corticosteroids, testosterone and 17 -oestradiol were ineffective. Folliculated oocytes stimulated by pituitary homogenate produced 17,20 ,21-P from endogenous substrates in amounts one order of magnitude higher than 17,20 -P. These results strongly support the hypothesis that 17,20 ,21-P is the likely MIS in this species.
- Molecular characterization and expression pattern of zona pellucida proteins in gilthead seabream (Sparus aurata)Publication . Modig, Carina; Modesto, Teresa; Canario, Adelino V. M.; Cerda, J.; Hofsten, Jonas von; Olsson, P. E.The developing oocyte is surrounded by an acellular envelope that is composed of 2–4 isoforms of zona pellucida (ZP) proteins. The ZP proteins comprise the ZP1, ZP2, ZP3, and ZPX isoforms. While ZP1 (ZPB) and ZP3 (ZPC) are present in all species, ZP2 (ZPA) is not found in teleost fish and ZPX is not found in mammals. In the present study, we identify and characterize the ZP1, ZP3 and ZPX isoforms of gilthead seabream. Furthermore, by analyzing the conserved domains, which include the external hydrophobic patch and the internal hydrophobic patch, we show that ZP2 and ZPX are closely related isoforms. ZP proteins are synthesized in either the liver or ovary of most teleosts. Only in rainbow trout has it been shown that zp3 has dual transcription sites. In gilthead seabream, all four mRNA isoforms are transcribed in both the liver and ovary, with zp1a, zp1b, and zp3 being highly expressed in the liver, and zpx being primarily expressed in the ovary. However, determination of the ZP proteins in plasma showed high levels of ZP1b, ZP3, and ZPX, with low or non-detectable levels of ZP1a. In similarity to other teleost ZPs, the hepatic transcription of all four ZP isoforms is under estrogenic control. Previously, we have shown that cortisol can potentiate estrogen-induced ZP synthesis in salmonids, and now we show that this is not the case in the gilthead seabream. The present study shows for the first time the endocrine regulation of a teleost ZPX isoform, and demonstrates the dual-organ transcriptional activities of all the ZP proteins in one species.
- Reproductive success in the Lusitanian toadfish: influence of calling activity, male quality and experimental designPublication . Amorim, M. Clara P.; Conti, Carlotta; Sousa-Santos, Carla; Novais, Bruno; Gouveia, Maria D.; Vicente, Joana R.; Modesto, Teresa; Gonçalves, Amparo; Fonseca, Paulo J.Acoustic signals are sexual ornaments with an established role on mate choice in several taxa, but not in fish. Recent studies have suggested that fish vocal activity may signal male quality and influence male's reproductive success but experimental evidence is lacking. Here we made two experiments to test the hypothesis that vocal activity is essential for male breeding success in a highly vocal fish, the Lusitanian toadfish. We first compared the reproduction success between muted and vocal males. In a second experiment we related male reproduction success with acoustic activity and male quality, including biometric, condition and physiological features. As a proxy for reproductive success we tallied both total number and number of sired eggs, which were correlated. Muting experiments showed that successful mating was dependent on vocalizing. In addition, the number of eggs was positively associated with the male's maximum calling rate. In the second experiment male's reproductive success was positively associated with male condition and negatively related with circulating androgen levels and relative gonad mass, but was not associated with vocal activity. Differences in results may be related with nest design which could have influenced mate choice costs and intra-sexual competition. In the muting experiment nests had a small opening that restrained the large nest-holder but allowed smaller fish, such as females, to pass while in the second experiment fish could move freely. These experiments suggest that a combination of factors, including vocal activity, influence reproductive success in this highly vocal species. (C) 2015 Elsevier Inc. All rights reserved.
- Hormonal control of swimbladder sonic muscle dimorphism in the Lusitanian toadfish, Halobatrachus didactylusPublication . Modesto, Teresa; Canario, Adelino V. M.The swimbladder and associated sonic muscle of the Lusitanian toadfish Halobatrachus didactylus increase in size throughout life and are, respectively, 25% and 30% larger in type I (nest-holder) males than females, which may generate sexual differences in sound production. Sexual dimorphism in swimbladder is also evident in the morphological features of sonic muscle fibers. During the breeding season, type I males have smaller myofibril contracting zones surrounded by larger sarcoplasm areas compared with females, possibly an adaptation to speed and fatigue resistance for the production of long mating calls. Type II (floater) males show characteristics that are intermediate, but statistically not significantly different, between type I males and females. Six weeks after castration and androgen (testosterone and 11- ketotestosterone) replacement in type I and type II males there were no alterations either in swimbladder mass or fiber morphology. However, 17b-estradiol induced a significant decrease in swimbladder mass and sarcoplasm area/myofibril area ratio. Six months after castration there was a clear reduction in the seasonal swimbladder hypertrophy in males and induction of sonic fiber morphological characteristics that resemble those occurring in females (low sarcoplasm area/myofibril area ratio). These results suggest that testicular factors are required to initiate sonic muscle hypertrophy and type I sonic fiber phenotype in H. didactylus, but a specific involvement of androgens has not been completely clarified.
- 16.P15. Branchial osmoregulatory response to salinity challenge in the Lusitanian toadfishPublication . Guerreiro, Pedro M; Laiz-Carrión, R.; Haond, Christophe; Modesto, Teresa; Fuentes, Juan; Mancera, J. M.; Canario, Adelino V. M.Halobatrachus didactylus, a marine teleost found in coastal lagoons and river estuaries is often exposed to important salinity changes. Despite its aglomerular kidney, it is able to survive in hypo-osmotic environments, likely via compensatory actions from gills and intestine. We aimed at evaluating the response of the branchial tissue of H. didactylus to salinity changes.
- Alloparental behavior in the highly vocal Lusitanian toadfishPublication . Ramos, Andreia; Fonseca, Paulo; Modesto, Teresa; Almada, V. C.; Amorim, Maria ClaraIn many fish species in which males guard nests with their eggs, parental care directed to genetically unrelated offspring may arise for example from nest takeovers or cuckoldry. Lusitanian toadfish (Halobatrachus didactylus) has exclusive male parental care and face intensive nest competition during the breeding season that may lead to care of foster eggs. Males of this species use visual displays and sounds when defending their nests frequently resulting in expulsion of the intruder without escalated confrontation. In this study we intended to investigate the existence of alloparental care in Lusitanian toadfish, a behavior whose adaptive significance is still poorly understood. Fish were randomly assigned to three different treatments: parental males in nests with their eggs, parental males with foster eggs and parental males without eggs. Nests with eggs with no nest holder or with females were used as controls. We performed three territorial intrusions over periods of 15 days and observed the acoustic and visual behaviors of residents and intruders. Egg survival was tallied from nests' photographs in all groups. Circulating steroid levels were measured in the three test groups and in another set of non-manipulated males. There were no differences in acoustic and visual territorial defense behaviors among treatments. Egg survival was similar between males (parental and alloparental) and significantly higher than in nests with no nest-tender. Females presented intermediate egg survival. All groups presented similar levels of testosterone and alloparental males showed higher 11-ketotestosterone levels but within the range of levels observed in non-manipulated males. Cortisol levels were similar in all male groups suggesting that experiments did not increase fish stress. The present results suggest the existence of alloparental care in this species.