INTRODUCTIONTop

Fish inhabiting artificial reefs have demonstrated reproductive success similar to or better than that of those living in natural reefs, probably due to the greater protection offered by environments of anthropogenic origin (Granneman and Steele 2014Granneman J.E., Steele M.A. 2014. Fish growth, reproduction, and tissue production on artificial reefs relative to natural reefs. ICES J. Mar. Sci. 71: 2494-2504. ). Maricultures are examples of artificial environments that offer protection and foraging resources for fish (Goodbrand et al. 2013Goodbrand L., Abrahams M.V., Rose G.A. 2013. Sea cage aquaculture affects distribution of wild fish at large spatial scales. Can. J. Fish. Aquat. Sci. 70(9): 1289-1295.).

Mariculture structures alter the environment, resembling a reef environment. This enables the occurrence of species formerly absent at the site (Freitas and Velastin 2010Freitas M.O., Velastin R. 2010. Ictiofauna associada a um cultivo de mexilhão Perna perna (Linnaeus, 1758) Norte Catarinense, Sul do Brasil. Acta Sci. Biol. Sci. 32(1): 31-37.). In addition to cryptic fish species, other organisms such as corals, bryozoans, sponges and echinoderms are attracted to these new consolidated environments. They are mostly suspensivores, thus changing the suspended material and consequently the turbidity (Thrush and Dayton 2002Thrush S.F., Dayton P.K. 2002. Disturbance to marine benthic habitats by trawling and dredging: Implications for Marine Biodiversity. Annu. Rev. Ecol. Syst. 33: 449-473.).

Hypleurochilus fissicornis (Quoy and Gaimard, 1824) is a small-sized cryptic marine species that inhabits consolidated environments such as coral and rocky reefs. The species is distributed in the western Atlantic from Vitória (Espírito Santo State, Brazil) to Mar del Plata (Argentina) and in the northeast Atlantic in the Azores (Portugal) (Menezes and Figueiredo 1985Menezes N.A., Figueiredo J.L. 1985. Manual de peixes marinhos do sudeste do Brasil – V Teleostei (4). Museu de Zoologia. Univ. São Paulo. São Paulo, pp. 54-55., Santos et al. 1997Santos R.S., Porteiro F.M., Barreiros J.P. 1997. Marine fishes of the Azores: annotated checklist and bibliography. Bull. Univ. Azores Suppl: 1: 1-244., Floeter et al. 2003Floeter S.R., Gasparini J.L., Rocha L.A., et al. 2003. Brazilian reef fish fauna: checklist and remarks (updated Jan. 2003). Brazilian Reef Fish Project: www.brazilianreeffish.cjb.net.). As in other Blenniidae fish, males take care of the nest where females spawn oocytes. The preferential sites for nests of H. fissicornis are rock crevices, empty shells, barnacles and even experimental fouling panels (Menezes and Figueiredo 1985Menezes N.A., Figueiredo J.L. 1985. Manual de peixes marinhos do sudeste do Brasil – V Teleostei (4). Museu de Zoologia. Univ. São Paulo. São Paulo, pp. 54-55., Omena and Souza 1999Omena E.P., Souza M.M. 1999. Efeito da predação no desenvolvimento inicial da comunidade incrustante na região da Urca, Baía de Guanabara, R.J. Oecol. Bras. 7: 213-227.).

Small organisms such as blennies have the potential to dominate resources and control the functions of the system in which they live in high abundances, performing a fundamental role in the trophic chain of reef environments (Ackerman and Bellwood 2000Ackerman J.L., Bellwood D.R. 2000. Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar. Ecol. Prog. Ser. 206: 227-237.). In natural coastal reefs and in artificial ones designed to increase local diversity, H. fissicornis is usually found in low abundances from northern Rio de Janeiro State to the south-central coast of Santa Catarina State (Brotto et al. 2007Brotto D.S., Krohling W., Zalmon I.R. 2007. Comparative evaluation of fish assemblages census on an artificial reef. Rev. Bras. Zool. 24(4): 1157-1162., Luiz-Jr. et al. 2008Luiz-Jr O.J., Carvalho-Filho A., Ferreira C.E.L., et al. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, Southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations, and conservation. Zootaxa 1807: 1-25., Alves and Pinheiro 2011Alves J.A., Pinheiro P.C. 2011. Peixes recifais das ilhas costeiras do Balneário Barra do Sul – Santa Catarina – Brasil. R. CEPSUL Biodiv. Conserv. Mar. 2(1): 10-21.). On the other hand, in mariculture, the species is found in high abundances (Gerhardinger et al. 2004Gerhardinger L.C., Hostim-Silva M., Barreiros J.P. 2004. Empty mussel shells on mariculture ropes as potential nest places for the blenny Hypleurochilus fissicornis (Perciformes: Blenniidae). J. Coast. Res. SI39: 1202-1204., Freitas and Velastin 2010Freitas M.O., Velastin R. 2010. Ictiofauna associada a um cultivo de mexilhão Perna perna (Linnaeus, 1758) Norte Catarinense, Sul do Brasil. Acta Sci. Biol. Sci. 32(1): 31-37.), indicating that H. fissicornis probably reproduces more successfully in artificial sheltered environments than in natural coastal habitats.

Aiming to determine the strategy used by H. fissicornis in an artificial environment, the present study intended to (1) characterize the maturity stages of females and males from the development of germ cells (oogenesis and spermatogenesis), (2) identify the reproductive tactics to check for the reproductive success, and (3) investigate the use of cultivation structures in the reproductive process.

MATERIALS AND METHODSTop

Guaratuba Bay (Fig. 1) has an area of 50.19 km² situated on the coastal plain of southern Brazil. The climate of the region is humid mesothermal. Data of air temperature and rainfall, furnished by the technological institute SIMEPAR, were used to characterize the study period. The highest mean monthly temperatures were recorded in January (25.8°C), February (26.1°C) and March (24.1°C), and the lowest in July (15.9°C) and August (16.3°C). The mean annual temperature was 21.0°C. Cumulative rainfall was 2020.6 mm, with the largest volume in June (220.2 mm) and the smallest in August (77.4 mm).

Monthly samplings were conducted between May 2013 and May 2014, in an oyster (Crassostrea brasiliana (Lamarck, 1819)) farm in the Pinheiros River (25°26’S; 49°17’W), near the mouth of the bay. Oysters were placed in mesh tubes, which were attached to a main cable held above the water by floats. These mesh tubes were covered with a cylindrical net (mesh 1 mm) by means of diving in order to prevent the escape of organisms, and brought to the surface following the methodology used by Freitas and Velastin (2010)Freitas M.O., Velastin R. 2010. Ictiofauna associada a um cultivo de mexilhão Perna perna (Linnaeus, 1758) Norte Catarinense, Sul do Brasil. Acta Sci. Biol. Sci. 32(1): 31-37.. Shells on which spawn was laid were also collected, as well as water temperature, pH, dissolved oxygen (DO) and salinity data (obtained using a multiparameter probe).

In the laboratory, measurements of total length (TL in cm) and total weight (TW in g) of specimens of H. fissicornis were taken. Gonads were removed, weighed (GW in g) and identified macroscopically for sex and gonadal development (according to Vazzoler 1996Vazzoler A.E.M. 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. EDUEM. Maringá, 169 pp. and Brown-Peterson et al. 2011Brown-Peterson N.J., Wyanski D.M., Saborido-Rey F., et al. 2011. A Standardized Terminology for Describing Reproductive Development in Fishes. Mar. Coast. Fish. Dynam. Manag. Ecosys. Sci. 3(1): 52-70.). Some gonads were subjected to routine histological analysis (fixed in ALFAC for 18h and embedded in Paraplast). Slides were stained with hematoxylin-eosin and analysed under a light microscope to characterize the maturity stage of females and males and to confirm the macroscopic identification of gonadal stages. The characterization of the development of female germ cells was based on Lowerre-Barbieri et al. (2013)Lowerre-Barbieri S.K., Brown-Peterson N.J., Murua H., et al. 2013. Emerging issues and methodological advances in fisheries reproductive biology. Mar. Coast. Fish. Dynam. Manag. Ecosys. Sci. 3(1): 32-51., while the maturity stage for females and males was prepared according to Vazzoler (1996)Vazzoler A.E.M. 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. EDUEM. Maringá, 169 pp. and Brown-Peterson et al. (2011)Brown-Peterson N.J., Wyanski D.M., Saborido-Rey F., et al. 2011. A Standardized Terminology for Describing Reproductive Development in Fishes. Mar. Coast. Fish. Dynam. Manag. Ecosys. Sci. 3(1): 52-70.. The sex ratio (monthly and by length classes) was analysed by a χ² test, with a degree of freedom of 1 and a significance of 0.05 (χ²> 3.84), according to Vazzoler (1996)Vazzoler A.E.M. 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. EDUEM. Maringá, 169 pp.. The length classes (seven classes with a 1-cm range) were established in accordance with Sturges (Sokal and Rolf 1981Sokal R.R., Rohlf F.J. 1981. Biometry. W. H. Freeman. New York, 859 pp.).

The individual gonadosomatic index (GSI), expressed by the formula GSI=(GW/TW)100, was calculated to analyse gonadal development. To determine the maturation curve, the monthly mean GSI was calculated from the individual GSI of females and males, including juveniles of both sexes. After histological analysis of gonads, the distribution of the monthly percentage frequencies of gonadal development and the frequencies of young and adult individuals were estimated.

The weight-length relationship was calculated by TW=aTL^b, in which a is the linear coefficient and b is the slope (both determined using the least squares method) (Le Cren, 1951Le Cren E.D. 1951. The length-weight relationship and seasonal cycle in gonad and conditions in the perch Perca fluviatilis. J. Anim. Ecol. 20(2): 201-219.). From this, the total and somatic condition factors were calculated, expressed by K=TW/TL^b and K’=BW/TL^b, respectively (BW= body weight of the specimen subtracting the gonad weight).

Length at first maturity (L₅₀) was calculated by Fr=1–(℮^–aLmb) (Fr= relative frequency of adult individuals; ℮= base of the Napierian logarithm; a and b are coefficients estimated by the least squares method, transforming the variables involved; and L_m=midpoint of the length classes), according to Fávaro et al. (2003)Fávaro L.F., Lopes S.C.G., Spach H.L. 2003. Reprodução do peixe-rei, Atherinella brasiliensis (Quoy & Gaimard) (Atheriniformes, Atherinidae), em uma planície de maré adjacente à gamboa do Baguaçu, Baía de Paranaguá, Paraná, Brasil. Rev. Bras. Zool. 20: 501-506. and Oliveira and Fávaro (2011)Oliveira E.C., Fávaro L.F. 2011. Reproductive biology of the flatfish Etropus crossotus (Pleuronectiformes: Paralichthyidae) in the Paranaguá Estuarine Complex, Paraná State, subtropical region of Brazil. Neotrop. Ichth. 9: 795-805. in reproductive studies on estuarine fish.

Abiotic variables were summarized by a principal component analysis (PCA). Axes with higher eigenvalues were used to relate with gonadal development stages through Spearman correlation (α=0.05). The broken-stick method was used to select the most important axes. The seasons of the year were defined as autumn (April to June), winter (July to September), spring (October to December) and summer (January to March). These analyses were run using the R 3.1.0 software.

RESULTSTop

A total of 519 specimens were collected from May 2013 to May 2014 (205 females, 228 males and 86 of unidentified sex, including juvenile and adults with TL ranging from 1.2 to 5.4 cm). No specimens were collected in February and March 2014. TL varied from 2.0 to 7.8 cm (4.78±1.06 cm) and from 2.0 to 8.5 cm (5.64±1.50 cm) for females and males, respectively.

There were no significant differences in the sex ratio between the months, except January, when a larger number of males was found (χ²=4.89; df=1; p<0.05). The analysis of sex ratio by size classes showed differences between the sexes. Intermediate classes (3.2-4.2 and 4.3-5.3 cm) were dominated by females (χ²=5.12 and χ²=8.57; df=1; p<0.05) and the larger classes (6.5-7.5 and 7.6-8.6 cm) by males (χ²=27.55 and χ²=30.11; df=1; p<0.05) (Fig. 2).

Histological description of the gonads

There were six developmental stages of ovarian follicles. Oogonia are the smallest germ cells, with a large nucleus and scant cytoplasm. The primary growth (PG) oocyte is characterized by increased cytoplasmic volume and basophilia. In the next stage, called cortical alveolar (CA), oocytes have vesicles in the cytoplasm. Subsequently, primary, secondary and tertiary vitellogenic oocytes (Vtg) have, in addition to these vesicles, yolk granules in the cytoplasm. In the next stage, oocytes with germinal vesicle migration (GVM) have larger diameter and cytoplasm filled by yolk granules. Then, pre-ovulatory hydration promotes the fusion of yolk granules, characterizing the hyalinization process and the germinal vesicle breakdown oocytes (GVBD). Follicle cells are squamous in the PG oocytes, which become cylindrical at the end of oogenesis. The yolk membrane is observed from CA.

The development of sperm cells begins with the spermatogonia (larger volume cell). These cells lose cytoplasmic volume during the mitotic and meiotic cell division, which creates smaller cells with more condensed nuclei that are highly basophilic at each cell division. This results in the formation of spermatozoa (smallest cells from spermatogenesis). Each cell type is arranged radially into clusters, forming the wall of the seminiferous tubules, with the spermatozoa located in the lumen. Testes are located peripherally, surrounding a central portion, the testicular gland.

The gonadal maturity scale (five stages for each sex) was determined from the characterization of the oogenesis and spermatogenesis (Tables 1 and 2, Figs 3 and 4). Partial spawning for the species was characterized by observation of partially-spawned gonads through histological analysis.

Reproduction analysis

The maturation curve showed a synchronized trend for females and males, characterizing an extensive reproductive period of eight months (May to December) (Fig. 5). Winter was the period with the highest reproductive activity, showing the highest frequencies of spawning-capable gonads (Fig. 6). Partially-spawned individuals were sampled throughout the period, except in January and May 2014, months with smaller mean GSI values and higher frequencies of gonads in the post-spawning and developing stages, respectively. Young individuals were recorded in almost the entire sampling period, but in higher abundance in December, January and May (Fig. 7).

Corroborating the maturation curve and the frequency of gonadal stages, the total (K) and somatic (K’) condition factors confirmed the extensive period of investment in gonads, especially for females (Fig. 8). In turn, for males, graphic analysis evidenced no difference, given the small variation in testis weight over the period.

The use of empty oyster shells for spawning was observed from June to November. Shells with spawns were under the care of a single male of the species, and each nest contained several egg development stages, indicated by their colour (Fig. 9).

The L₅₀ of females was 2.12 cm and the L₁₀₀ was 6.07 cm (Fig. 10A). The estimate for males was L₅₀=2.02 cm and L₁₀₀=5.71 cm (Fig. 10B).

Relationship between abiotic factors and reproduction

From June to August, values of water and air temperatures were the lowest, accompanied by the highest DO values. In the study period, salinity varied from 13 to 30 and pH from 7.05 to 8.19. Only the first PCA axis was sufficient to represent the data distribution. This axis was very positively influenced by the water and air temperatures and very negatively by DO (Fig. 11; Table 3).

For both female and male individuals, the spawning-capable stage was strongly negatively correlated with the first PCA component, indicating that individuals probably reach maturity at lower temperatures (Table 4).

DISCUSSIONTop

Females showed an ovarian maturity scale in agreement with the pattern found in other teleosts, while males of H. fissicornis had a testicular gland associated with the testis, making the determination of male gonadal development more complex.

Unlike most teleosts, H. fissicornis have testes limited to a reduced peripheral part of the testicular gland, so the developing, spawning-capable and partially-spawned stages were difficult to characterize because these stages have all types of sperm cells (differing slightly in number of spermatozoa). This partial release of gametes is an important reproductive tactic because it reduces the probability of larval loss due to environmental fluctuations (Santos 1995Santos R.S. 1995. Anatomy and histology of secondary sexual characters, gonads and liver of the rock-pool blenny, Parablennius sanguinolentus parvicornis, (Pisces: Blenniidae) of the Azores. Arquipel. Life Mar. Sci. 13(A): 21-38.).

The extensive reproductive period was also found for Coryphoblennius galerita on the Portuguese coast (Almada et al. 1996Almada V.C., Carreiro H., Faria C., et al. 1996. The breeding season of Coryphoblennius galerita in Portuguese waters. J. Fish Biol. 48: 295-297.). However, Blenniidae species on the coast of Portugal and Spain showed a reproductive peak in summer (Almada et al. 1994Almada V.C., Gonçalves E.J., Santos A.J., et al. 1994. Breeding ecology and nest aggregations in a population of Salaria pavo (Pisces: Blenniidae) in an area where nest sites are very scarce. J. Fish Biol. 45: 819-830., Almada et al. 1996Almada V.C., Carreiro H., Faria C., et al. 1996. The breeding season of Coryphoblennius galerita in Portuguese waters. J. Fish Biol. 48: 295-297., Carrassón and Baú 2003Carrassón M., Baú M. 2003. Reproduction and gonad histology of Aidablennius sphynx (Pisces: Blenniidae) of the Catalan Sea (northwestern Mediterranean). Sci. Mar. 67(4): 461-469), whereas H. fissicornis, in southern Brazil, reaches greater reproductive activity in winter, as gonadal maturity is intimately related to the drop in water temperature. This difference in the reproduction period may be used by the species to avoid potential predators, since as youth of piscivorous fishes (as Epinephelidae) were found in the study area only in summer (personal observation). Other piscivorous fish species, such as Centropomus parallelus and Cynoscion sp., have been found in the surroundings of the study area (Gomes and Chaves 2006Gomes I.D., Chaves P.T. 2006. Ictiofauna integrante da pesca de arrasto no litoral sul do estado do Paraná. Bioikos 20(1): 9-13., Vendel et al. 2010Vendel A.L., Bouchereau J.L., Chaves P.T. 2010. Environmental and subtidal fish assemblage relationships in two different Brazilian coast estuaries. Braz. Arch. Biol. Technol. 56(6): 1393-1406.). In addition, the disappearance of H. fissicornis specimens in February and March demonstrates that the bivalve farming is used by the species only as a reproductive site. Therefore, after reproduction, the individuals leave the area, as described for Salaria pavo (Almada et al. 1994Almada V.C., Gonçalves E.J., Santos A.J., et al. 1994. Breeding ecology and nest aggregations in a population of Salaria pavo (Pisces: Blenniidae) in an area where nest sites are very scarce. J. Fish Biol. 45: 819-830.). In addition, this behaviour of H. fissicornis also avoids predation in summer.

On the other hand, in colder waters such as those of Argentina, the reproductive period of H. fissicornis is in summer (Delpiani et al. 2012Delpiani S.M., Bruno D.O. Díaz De Astarloa J.M., et al. 2012. Development of early life stages of the blenny Hypleurochilus fissicornis (Blenniidae). Cybium. 36(2): 357-359.), and this situation may indicate that the ideal temperature range for gonadal development and larval development is found in winter in warm waters and in summer in cold waters. Temperature influences the maturation and growth rate of Parablennius ruber, which are accelerated with increasing temperature (Azevedo and Homem 2002Azevedo J.M.N., Homem N. 2002. Age and growth, reproduction and diet of the red blenny Parablennius ruber (Blenniidae). Cybium. 26(2): 129-133.). The relationship of temperature, latitude and reproductive period was also demonstrated by Fávaro et al. (2007)Fávaro L.F., Oliveira E.C., Verani N.F. 2007. Estrutura da população e aspectos reprodutivos do peixe-rei Atherinella brasiliensis (Quoy & Gaimard) (Atheriniformes, Atherinopsidae) em áreas rasas do complexo estuarino de Paranaguá, Paraná, Brasil. Rev. Bras. Zool. 24(4): 1150-1156. for Atherinella brasiliensis.

With regard to the use of empty shells, several egg development stages were observed in the same shell, indicating that more than one female may have used the same nest in different periods, spawning batches of ovarian follicles under the care of a single male. This strategy is used by Rhabdoblennius nitidus females, which choose their partners by preferentially repeating the choice of another female, in order to reduce the probability of desertion of the male (Matsumoto and Takegaki 2013Matsumoto Y., Takegaki T. 2013. Female mate choice copying increases egg survival rate but does not reduce mate-sampling cost in the barred-chin blenny. Anim. Behav. 86: 339-346.). Considering that the ability of the male to care for the eggs is directly related to the probability of larval survival, subjecting spawns to several partners is advantageous (Santos 1995Santos R.S. 1995. Anatomy and histology of secondary sexual characters, gonads and liver of the rock-pool blenny, Parablennius sanguinolentus parvicornis, (Pisces: Blenniidae) of the Azores. Arquipel. Life Mar. Sci. 13(A): 21-38.). Since the males need to defend their nests, their parental care may explain the longer length observed in males.

The species H. fissicornis was abundant in the bivalve farming studied, and the presence of young individuals for several months is indicative that the species has been reproductively successful at the site. In marine reef environments, the species is present in low abundances (Luiz-Jr. et al. 2008Luiz-Jr O.J., Carvalho-Filho A., Ferreira C.E.L., et al. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, Southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations, and conservation. Zootaxa 1807: 1-25., Hackradt and Félix-Hackardt 2009Hackradt C.W., Félix-Hackradt F.C. 2009. Assembléia de peixes associados a ambientes consolidados no litoral do Paraná, Brasil: Uma análise qualitativa com notas sobre sua bioecologia. Pap. Avulsos de Zool. 49(31): 389-403., Alves and Pinheiro 2011Alves J.A., Pinheiro P.C. 2011. Peixes recifais das ilhas costeiras do Balneário Barra do Sul – Santa Catarina – Brasil. R. CEPSUL Biodiv. Conserv. Mar. 2(1): 10-21.), which may indicate that the farms, more sheltered in the estuary, offer greater protection during the reproductive cycle. However, since the samplings of the works cited above were carried out using visual censuses, cryptic and small-sized species can be underestimated (Ackerman and Bellwood 2000Ackerman J.L., Bellwood D.R. 2000. Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar. Ecol. Prog. Ser. 206: 227-237.).

The highest frequency of young individuals was recorded in December, coinciding with the end of the reproductive season. The largest number of males in relation to females in January possibly indicates that females leave the breeding site earlier, as only males display parental care for the offspring.

The determination of length at first maturity for H. fissicornis pointed out that individuals with much reduced length enter into the reproductive process. Based on the L₅₀/L_max ratio, the values were 0.27 for the females and 0.23 for the males. This is characterized as an early first maturity, since the value of the L₅₀/L_max ratio is generally between 0.4 and 0.9 for different species (Beverton and Holt 1959Beverton R.J.H., Holt S.J. 1959. A review of the lifespans and mortality rates of fish in nature, and their relation to growth and other physiological characteristics. In: Wolstenholme G. E. W., Oconnor M. (eds), Ciba Foundation Colloquia on Ageing. 5: 142-180.).

Our results demonstrate that H. fissicornis has a variety of tactics to protect its offspring (e.g. batch spawning, long reproductive period, parental care, small length at first maturity and low-temperature reproductive period). Thus, the oyster farm is used as a breeding site by H. fissicornis in winter, ensuring the reproductive success of the species.

ACKNOWLEDGEMENTSTop

We thank Hamilton de Moura Kirchner for allowing this study in his mariculture, Augusto L. Ferreira Junior for making the map, and Diego Zanlorenzi, Thiago B. Mayer, Gisleine Hoffman, Wanessa P. D. Carmo and all who helped with the sampling. We also thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the postgraduate scholarship and the Instituto SIMEPAR for the environment data provided.

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