INTRODUCTIONTop

The genus Ophioblennius comprises at least five highly related Atlantic blennies (see Muss et al. 2001Muss A., Robertson D.R., Stepien C.A., et al. 2001. Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55: 561-572.), one of which, Ophioblennius trinitatis Miranda-Ribeiro, 1919, is exclusively found on the Brazilian coast and its associated oceanic islands, a distinct biogeographic province (Floeter and Gasparini 2000Floeter S.R., Gasparini J.L. 2000. The southwestern Atlantic reef fish fauna: composition and zoogeographic patterns. J. Fish Biol. 56: 1099-1114., 2001Floeter S.R., Gasparini J.L. 2001. The Brazilian endemic reef fishes. Coral Reefs 19: 292.). Ophioblennius species are diurnally-active primary consumers, residing within restricted and permanent home ranges (i.e. territories), and are hostile in defending resources from intruder fishes (Nursall 1977Nursall J.R. 1977. Territoriality in redlip blennies, Ophioblennius atlanticus (Pisces: Blenniidae). J. Zool. 182: 205-223., Humann and DeLoach 2002Humann P., DeLoach N. 2002. Reef fish identification: Florida, Caribbean, Bahamas. New World Publications, Miami., Mendes 2006Mendes L.F. 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Rev. Bras. Zool. 23: 817-823.). Adults are primarily observed in shallow consolidated reef areas, whereas juveniles have been reported at depths of up to 53 m (Bath 1990Bath H. 1990. Blenniidae. In: Quero J.C., Hureau J.C., Karrer C. et al. (eds), Check-list of the fishes of the eastern tropical Atlantic (CLOFETA). SEI UNESCO, Lisboa, 1490 pp., Mendes 2007Mendes L.F. 2007. Ophioblennius trinitatis (Pisces: Blenniidae) from the oceanic archipelagos of São Pedro e São Paulo, Fernando de Noronha and Atol das Rocas. Braz. J. Oceanogr. 55: 63-65.).

Previous studies showed that Ophioblennius species contribute greatly to the overall abundance (Randall 1996Randall J.E. 1996. Caribbean reef fishes. T. F. H. Publications Inc., Hong Kong., Medeiros et al. 2010aMedeiros P.R., Grempel R.G., Souza A.T., et al. 2010a. Non-random reef use by fishes at two dominant zones in a tropical, algal-dominated coastal reef. Environ. Biol. Fish. 87: 237-246.) and biomass (Labelle and Nursall 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204.) of site-attached fishes on both coral and rocky reefs of the Atlantic Ocean. Furthermore, given their territorial habits, which potentially influence the distribution of other fishes, and their role in linking energy from primary producers to carnivores (Labelle and Nursall 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204.), they are of great ecological importance to the overall reef community.

In recent decades, due to a surge in the number of tropical reef studies carried out in the southwestern Atlantic, many species formerly recognized as Caribbean-equivalents have been resurrected from synonym (Guimarães and De Bacellar 2002Guimarães R.Z.P., De Bacellar A.C.L.H. 2002. Review of the Brazilian species of Paraclinus (Teleostei: Labrisomidae), with descriptions of two new species and revalidation of Paraclinus rubicundus (Starks). Copeia 2: 419-427., Moura et al. 2001Moura R.L., Figueiredo J.L., Sazima I. 2001. A new parrotfish (Scaridae) from Brazil, and revalidation of Sparisoma amplum (Ranzani, 1842), Sparisoma frondosum (Agassiz, 1831), Sparisoma axillare (Steindachner, 1878) and Scarus trispinosus (Valenciennes, 1840). Bull. Mar. Sci. 68: 505-524., Rocha and Rosa 2001Rocha L.A., Rosa R.S. 2001. Halichoeres brasiliensis (Bloch, 1791), a valid wrasse species (Teleostei: Labridae) from Brazil, with notes on the Caribbean species Halichoeres radiatus (Linnaeus, 1758). Aqua J. Ichthyol. Aqua. Biol. 4: 161-166., Rocha 2004Rocha L.A. 2004. Mitochondrial DNA and color pattern variation in three western Atlantic Halichoeres (Labridae), with the revalidation of two species. Copeia 2004: 770-782.), including O. trinitatis (Muss et al. 2001Muss A., Robertson D.R., Stepien C.A., et al. 2001. Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55: 561-572.). In fact, intraspecific variations in O. trinitatis along the Brazilian coast and oceanic islands suggest that this taxon needs a thorough revision. Although similarities in the ecology of related Caribbean and Brazilian fishes have been acknowledged in the past, more recent investigations suggest that the ecological and behavioural processes differ substantially between counterpart species from these two provinces (see Floeter and Gasparini 2000Floeter S.R., Gasparini J.L. 2000. The southwestern Atlantic reef fish fauna: composition and zoogeographic patterns. J. Fish Biol. 56: 1099-1114. for a review). Nonetheless, most of what is known nowadays on the ecological requirements and general habits of O. trinitatis is actually an extrapolation from what is known for O. atlanticus studied in the Caribbean (e.g. Nursall 1977Nursall J.R. 1977. Territoriality in redlip blennies, Ophioblennius atlanticus (Pisces: Blenniidae). J. Zool. 182: 205-223., 1981Nursall J.R. 1981. The activity budget and use of territory by a tropical blenniid fish. Zool. J. Linn. Soc. Lond. 72: 69-92., Rylander and Koster 1982Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115., Nursall 1989Nursall J.R. 1989. Buoyancy is provided by lipids of larval redlip blennies, Ophioblennius atlanticus (Teleostei: Blenniidae). Copeia 1989: 614-621, Marraro and Nursall 1983Marraro C.M., Nursall J.R. 1983. The reproductive periodicity and behaviour of Ophioblennius atlanticus (Pisces: Blenniidae) at Barbados. Can. J. Zool. 61: 317-325., Nursall and Turner 1985Nursall J.R., Turner L. 1985. The liver supports metamorphosis in the Caribbean reef blenniid, Ophioblennius atlanticus. Proc. 5th Int. Cor. Reef Symp. 5: 457-462., Labelle and Nursall 1985Labelle M., Nursall J.R. 1985. Some aspects of the early life history of red lip blenny, Ophioblennius atlanticus macciureii (Pisces: Blenniidae). Copeia 1985: 39-49., 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204., Muss et al. 2001Muss A., Robertson D.R., Stepien C.A., et al. 2001. Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55: 561-572., but see Mendes 2006Mendes L.F. 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Rev. Bras. Zool. 23: 817-823., 2007Mendes L.F. 2007. Ophioblennius trinitatis (Pisces: Blenniidae) from the oceanic archipelagos of São Pedro e São Paulo, Fernando de Noronha and Atol das Rocas. Braz. J. Oceanogr. 55: 63-65). Therefore, direct ecological and behavioural studies on O. trinitatis are an important means of supporting and/or contesting Caribbean-based findings.

In this paper, local patterns of abundance and microhabitat use, in addition to several behavioural traits (i.e. feeding behaviour, bite rate, territory size and agonistic interactions) were investigated for O. trinitatis at an oceanic archipelago of the southwestern Atlantic. Specifically, to test the ecological implications of spatial variation in fish density, we hypothesized that differences in spatial distribution are driven by differences in microhabitat characteristics. Regarding behavioural traits, the following hypotheses were tested, locally and spatially (i.e. among sites): 1) smaller individuals have higher bite rates due to a proportionally higher energy demand, typical of juveniles; 2) larger territories are observed at low-density sites due to the increased space availability and relaxed competition; 3) larger fish are able to defend larger territories; 4) potential competitors (i.e. fishes sharing feeding habits) are most likely to be involved in agonistic interactions than non-competitors; 5) larger individuals are more aggressive than smaller ones; and 6) agonistic interactions are higher at sites of high habitat complexity, given the increased competition for these optimal sites.

MATERIALS AND METHODS Top

Study area and sampling procedures

The study was conducted at Fernando de Noronha archipelago, an oceanic marine protected area of the southwestern Atlantic, located 360 km off the Brazilian coast (Fig. 1). The study was conducted between October and November 2009, always during the day, at four sites (Raquel, Sueste, Atalaia and Porto) (Fig. 1). General substratum characteristics of each site are as follows: Raquel is dominated by rocky pavements colonized by dense colonies of fleshy macroalgae and a high proportion of encrusting coralline algae. Sueste is dominated by reef flats with high proportions of sand and limestone, interspersed with rocky reefs, where turf algae and fleshy algae predominate. Atalaia is a small, protected reef area, where sandy bottoms blend with a reef terrace and somewhat high proportions of fleshy and coralline algae are observed. Porto is mainly a reef flat dominated by limestone and macroalgae, interspersed with rocky reefs where macroalgae and coralline are abundant (Eston et al. 1986Eston V.R., Migotto A.E., Oliveira-Filho E.C., et al. 1986. Vertical distribution of benthic marine organisms on rocky coasts of the Fernando de Noronha Archipelago (Brazil). Bol. Inst. Oceanogr. 34: 37-53.).

Density of O. trinitatis individuals was determined using underwater visual census (UVC) techniques on 2×2 m quadrates on consolidated substrates in each area (n=10 quadrates per site). All surveys were conducted at depths of less than 80 cm. Given the distinct depth distributions of the two recognized colour morphs (see Mendes 2006Mendes L.F. 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Rev. Bras. Zool. 23: 817-823., Rangel and Mendes 2009Rangel C.A., Mendes L.F. 2009. Review of blenniid fishes from Fernando de Noronha Archipelago, Brazil, with description of a new species of Scartella (Teleostei: Blenniidae). Zootaxa. 2006: 51-61.), observations of the present study included mostly, if not solely, O. trinitatis type 1 (typically the darker, adult individuals). Size of quadrates was chosen based on a previous study (i.e. Mendes 2007Mendes L.F. 2007. Ophioblennius trinitatis (Pisces: Blenniidae) from the oceanic archipelagos of São Pedro e São Paulo, Fernando de Noronha and Atol das Rocas. Braz. J. Oceanogr. 55: 63-65.). Each sample location was randomly chosen by dropping a lead weight to mark the centre of the quadrate. A one-minute period was left for the fish to get used to the diver’s presence and to return after possible initial disturbances and, subsequently, the diver spent 5 minutes counting all O. trinitatis individuals inside and within up to 0.5 m above the quadrate. Simultaneously, fishes wandering within the territory boundaries were also quantified in order to determine the composition and abundance of potential intruders. Care was taken to avoid quantifying the same individuals going in and out of the quadrate area.

Following fish counts, rugosity, depth and benthic composition were assessed in each quadrate. A 1-m-long chain was used to assess the physical complexity (rugosity) of the substrate (Luckhurst and Luckhurst 1978Luckhurst B.E., Luckhurst K. 1978. Analysis of the influence of substrate variables on coral reef fish communities. Mar. Biol. 49: 317-323.). The chain was positioned on the substrate and then adjusted, so it draped the substrate’s irregularities. Rugosity was determined at two non-overlapping locations within each quadrate and, subsequently, a rugosity index was estimated by calculating the ratio of the contoured chain to the linear horizontal distance (i.e. 1 m) and the mean value of the two replicates was used. Number of crevices was assessed by recording the number of holes located within the quadrate that were potentially used as temporary or permanent refuge sites (i.e. that were deeper than 5 cm and with a diameter <15 cm), and their length. Benthic composition was evaluated using photo-quadrats (Preskitt et al. 2004Preskitt L.B., Vroom P.S., Smith C.M. 2004. A rapid ecological assessment (REA) quantitative survey method for benthic algae using photoquadrats with scuba. Pac. Sci. 58: 201-209.) by taking a photograph in each quadrate area. Photographs were analysed by randomly plotting 50 points and estimating the relative proportions of six benthic categories (i.e. turf algae, macroalgae, coralline algae, live coral, sand and uncolonized pavement) using the coral point count with Excel extension software (CPCe 3.6) (Kohler and Gill 2006Kohler K.E., Gill S.M. 2006. Coral Point Count with Excel extensions (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput. Geosci. 32: 1259-1269.).

Feeding behaviour, agonistic interactions and territory size of O. trinitatis were quantified simultaneously using focal animal procedures (Lehner 1996Lehner P.N. 1996. Handbook of ethological methods. University Press, Cambridge.) for 40 individuals for 5 minutes each (10 focal adult individuals per site; 200 minutes of total observation). Density estimates and behavioural evaluations were made on separate events. Bite rate, that is, the number of times an individual bit on the substrate per minute, was quantified for each focal individual. During focal observations, benthic categories where bites were directed (same as described above) were distinguished, and size of each focal individual (total length: TL) was visually estimated. To test the effect of time on bite rate, focal observations were evenly spread between 10 am and 3 pm. For each focal individual we also recorded the number of agonistic interactions between the focal O. trinitatis (resident fish) and an intruder fish, and whether this was an intruder-directed interaction (i.e. the resident O. trinitatis attacking an intruder fish) or a resident-directed interaction (i.e. the resident O. trinitiatis being attacked by an intruder fish). Territory size was estimated by visually discerning and placing lead weights at the outermost locations visited by the focal fish to delimit its territory as a polygon. The longest diameter and the perimeter were measured and territory size was later calculated by drawing their positions and, using a compass and a protractor, drawing right-angle triangles (90º) inside the polygon, which had their areas calculated and combined to estimate overall territory size (Morgan and Kramer 2004Morgan I.E., Kramer D.L. 2004. The social organization of adult blue tangs, Acanthurus coeruleus, on a fringing reef, Barbados, West Indies. Env. Biol. Fish. 71: 261-273., Medeiros et al. 2010bMedeiros P.R., Souza A.T., Ilarri M.I. 2010b. Habitat use and behavioural ecology of the juveniles of two sympatric damselfishes (Actinopterygii: Pomacentridae) in the south-western Atlantic Ocean. J. Fish Biol. 77: 1599-1615.).

Data analysis

One-way ANOVAs (type III sum of squares) were used to verify spatial differences (i.e. among sites) of rugosity, number of crevices and fish density (log-transformed). Post-hoc Tukey HSD tests were used in case of significant F values. A one-way MANOVA (type III sum of squares; Pillai’s trace test statistic) followed by Tukey’s HSD test was used to verify spatial differences in the density of intruder fishes. Prior to running the analyses, normality and homogeneity of data were tested via Kolmogorov-Smirnov and Levene tests, respectively (Sokal and Rohlf 1995Sokal R.R., Rohlf F.J. 1995. Biometry. W.H. Freeman and Company, New York.), and when necessary data were transformed and re-tested.

The contribution of each benthic category to the substrate of each site was evaluated by a principal components analysis (PCA), using arcsine square root-transformed data of benthic proportions. The first two factors were interpreted (in all cases Eigenvalues>1.5) and the relative importance of each significant variable was inferred. Additionally, to test the effects of spatial variability and microhabitat covariates on density of O. trinitatis, factor scores from the PCA were used in a multivariate ANCOVA design (all effects model). In this analysis, density of O. trinitatis was entered as a dependent variable, study site as a categorical predictor and rugosity, number of crevices, depth, substrate diversity (Simpson’s index) and benthic composition (factor scores from principal components 1 and 2) as habitat covariates.

Spatial variation of behavioural traits (bite rate, territory size and agonistic interactions) were also assessed by means of one-way ANOVAs, similarly as described above. In order to determine feeding preferences relative to food availability in the environment, we used Ivlev’s electivity index (Ivlev 1961Ivlev V.S. 1961. Experimental ecology of the feeding of fishes. Yale University Press, New Haven.), E=(r_i− p_i)(r_i + p_i)^–1, where E is the electivity index and r_i and p_i are the relative proportions of the i category in the diet (r) and in the environment (p), respectively. This index ranges from –1 to 1, where positive values indicate a preference, negative values avoidance or inaccessibility, and values close to zero suggest an expected random feeding.

Simple linear regressions were used to test relationships between bite rate and fish size, territory size and fish size, rate of agonistic interactions and fish size, rate of agonistic interactions and territory size, and rate of agonistic interactions and rugosity. Finally, bite rate data were pooled across two periods (morning and afternoon) and a pairwise t-test was conducted. All statistical analyses were conducted on Statistica and Canoco softwares.

RESULTSTop

Relationship between fish density and habitat features

Number of Ophioblennius trinitatis individuals per m² pooled across the four study sites was (mean±SE) 1.14±0.86. A significant difference in density was observed among sites (ANOVA, F_3,36=11.79, p<0.0001), with Raquel and Atalaia showing higher values than Sueste and Porto (Fig. 2A).

Pooled across all sites, rugosity and number of crevices values were (mean±SE), respectively, 1.31±0.02 and 7.68±3.3, with no significant spatial differences observed (ANOVA, F_3,36=1.53; p>0.05) (ANOVA, F_3,36=1.12; p>0.05). Benthic composition was categorized and evaluated by a PCA (biplots shown in Fig. 3A). The first two PCA factors generated for Raquel cumulatively explained 71.5% of the variation in benthic composition. Factor 1 (37.4% of the variation) described an increasing proportion of macroalgae, coralline algae and uncolonized pavement, and a decreasing proportion of live coral. Factor 2 (34.1%) described an increasing proportion of turf algae and a decreasing proportion of live coral. At Sueste, the first two factors explained 67.8% of the variation. Factor 1 (42.2%) described an increasing proportion of coralline algae and live coral, and a decreasing proportion of sand. Factor 2 (25.6%) described an increasing proportion of turf algae and a decreasing proportion of sand. At Atalaia, the first two factors explained 69.8% of the variation. Factor 1 (43.9%) described an increasing proportion of turf algae, and a decreasing proportion of macroalgae and sand. Factor 2 (25.9%) described a decreasing proportion of live coral. At Porto, the first two factors explained 69.3% of the variation. Factor 1 (35.8%) described an increasing proportion of uncolonized pavement and live coral, and a decreasing proportion of sand. Factor 2 (33.5%) described an increasing proportion of macroalgae and live coral, and a decreasing proportion of turf algae.

ANCOVA results indicated that the density of O. trinitatis individuals, albeit marginally, was significantly affected by rugosity, number of crevices and substrate diversity (Simpson’s index), whereas water depth and PCA factors had no effect (Table 1).

Feeding behaviour

Turf algae, macroalgae and sand (Sueste only) were by far the most abundant benthic items (Fig. 3B). Coralline algae showed small percentages and live coral cover was somewhat high at Raquel and Sueste, but very low at Atalaia and Porto. Bite rates were mostly directed towards turf algae and, to a smaller extent, towards macroalgae (Fig. 3C), and regardless of differences in benthic composition among sites, turf algae were the only preferred food item by O. trinitatis at all sites, whereas the other items were completely avoided (Fig. 3B).

Bite rate averaged (mean±SE) 10.7±0.71 bites.min^–1 pooled across the four sites, but differed significantly among sites (ANOVA, F_3,39=3.73; p<0.05) due to differences between Raquel and Atalaia (Fig. 4A). Also, albeit weakly related (r²=0.14; p<0.05), bite rate decreased with an increase in the size of individuals, mostly due to higher bite rates being observed for individuals smaller than 5 cm TL compared with individuals with 6-9 cm TL (Fig. 4B). An increase in bite rate occurred during day hours, with peak rates from 1 to 2 pm (Fig. 4C). Further, with average bite rates of the morning and the afternoon periods pooled separately, a significant difference was observed (T-test; t-value=–2.15; df=38; p<0.05) (Fig. 4C).

Territory size and agonistic behaviours

Pooled across sites, territory size averaged (mean±SE) 0.79±0.09 m², and differed significantly among sites (ANOVA; F_3,39=4.80; p<0.01), with higher values observed in Sueste and Porto (Fig. 5A). Territory size showed a weak but significant positive relation with total length of individuals (r²=0.08; p<0.05), suggesting that larger individuals defended larger territories (Fig. 5B).

The most common intruders within territories of O. trinitatis at all sites were, in decreasing order of importance, the Noronha wrasse Thalassoma noronhanum (Boulenger, 1890) (mean abundance±SE, 4.45±3.71; relative abundance, 25.2%), the Rocas Gregory Stegastes rocasensis (Emery, 1972) (3.33±2.22; 18.8%), sailor’s grunt Haemulon parra (Desmarest, 1823) (2.53±2.21; 14.3%), Malacoctenus sp. (2.4±2.57; 13.6%), the sergeant major Abudefduf saxatilis (Linnaeus, 1758) (2.15±3.40; 12.2%) and the doctorfish Acanthurus chirurgus (Bloch, 1787) (1.95±3.02; 11.1%) (Fig. 6A). The remaining ten species accounted together for 4.8% of the recorded intruders: Halichoeres radiatus (Labridae), Sparisoma frondosum (Scaridae), Acanthurus coeruleus (Acanthuridae), Holocentrus adscensionis (Holocentridae), Sparisoma amplum (Scaridae), Sparisoma axillare (Scaridae), Bothus lunatus (Bothidae), Caranx latus (Carangidae), Chromis multilineata (Pomacentridae) and Pseudupeneus maculatus (Mullidae). Density of intruders varied significantly across sites (MANOVA; Pillai’s trace=1.76; F_45,72=2.26; p<0.001), and the two sites with higher densities of O. trinitatis showed higher abundances of A. saxatilis, Malacoctenus sp., S. rocasensis and T. noronhanum (Tukey’s HSD test; p<0.05) (Fig. 2B).

Rate of intruder-directed agonistic interactions (see Material and Methods) differed significantly among sites (ANOVA; F_3,39=3.71; p<0.05), being less common at Atalaia (Fig. 6A). Five intruder species were involved in agonistic interactions, and more than 85% of the attacks of resident O. trinitatis were directed towards conspecific intruders, Malacoctenus sp. and S. rocasensis (Fig. 6A). Within the rate of resident-directed agonistic interactions, no significant differences were observed among sites (ANOVA; F_3,39=0.23; p>0.05) Fig. 6B). In 97% of the occurrences, resident O. trinitatis received aggressive displays from S. rocasensis and conspecific individuals (Fig. 6B).

Neither intruder-directed (r²=0.03; p>0.05) nor resident-directed interactions (r²=0.01; p>0.05) correlated significantly with total length of individuals. Further, though intruder-directed interactions did not show a significant relation with territory size (r²=0.07; p>0.05), resident-directed interactions were more commonly observed inside larger territories (r²=0.18; p<0.01). Also, agonistic interactions (both types pooled) were lower at sites with higher structural complexity (r²=0.10; p<0.05).

DISCUSSION

Relationship between fish density and habitat features

The density of O. trinitatis observed in the present study concurs with densities reported for this species and for the related O. atlanticus on tropical rocky and coral reefs (e.g. Nursall 1981Nursall J.R. 1981. The activity budget and use of territory by a tropical blenniid fish. Zool. J. Linn. Soc. Lond. 72: 69-92., Mendes 2007Mendes L.F. 2007. Ophioblennius trinitatis (Pisces: Blenniidae) from the oceanic archipelagos of São Pedro e São Paulo, Fernando de Noronha and Atol das Rocas. Braz. J. Oceanogr. 55: 63-65.). The available literature suggests a high variability in the density of the latter species among different Caribbean sites, ranging from 0.29 ind. m^–2 at Punta de Betín (Rylander and Koster 1982Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115.) to 2.2 ind. m^–2 at Barbados (Labelle and Nursall 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204.). This somewhat high variability may be attributed to stochastic fluctuations in recruitment (Sale 1978Sale P.F. 1978. Coexistence of coral reef fishes, a lottery for living space. Env. Biol. Fish. 3: 85-102., Sale and Douglas 1984Sale P.F., Douglas W.A. 1984. Temporal variability in the community structure of fish on coral patch reefs and the relation of community structure to reef structure. Ecology 65: 409-422.), but also to geographical variations in the availability of space and suitable substrate (Labelle and Nursall 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204.). In the present study, local variation in fish density (i.e. among sites separated by few kilometres) was observed.

Local differences in the density of O. trinitatis among the four study sites may be attributed to differences in habitat characteristics, which eventually influenced territory size (see below). Although rugosity measures were similar across all sites, this factor had a significant positive effect on the distribution of this blenny, given that individuals were always observed near to, or associated with, small caves and crevices. In fact, presence of crevices seems to be a central habitat requisite for this species, and tight correlations between blennies and crevices are well documented (e.g. Rylander and Koster 1982Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115., Bath 1990Bath H. 1990. Blenniidae. In: Quero J.C., Hureau J.C., Karrer C. et al. (eds), Check-list of the fishes of the eastern tropical Atlantic (CLOFETA). SEI UNESCO, Lisboa, 1490 pp., Labelle and Nursall 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204., Mendes 2006Mendes L.F. 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Rev. Bras. Zool. 23: 817-823., 2007Mendes L.F. 2007. Ophioblennius trinitatis (Pisces: Blenniidae) from the oceanic archipelagos of São Pedro e São Paulo, Fernando de Noronha and Atol das Rocas. Braz. J. Oceanogr. 55: 63-65.). As complementary evidence, during two years of field experience in the study area, O. trinitatis was never observed at low-complexity unconsolidated sites, and was very rare even at the rocky reef-sand ecotone. A similar correlation was previously observed in a small shallow reef (Medeiros et al. 2010aMedeiros P.R., Grempel R.G., Souza A.T., et al. 2010a. Non-random reef use by fishes at two dominant zones in a tropical, algal-dominated coastal reef. Environ. Biol. Fish. 87: 237-246.), supporting the prominent habitat selectivity of this species.

Contrary to initial expectations, benthic composition was a somewhat poor determinant of O. trinitatis density (see PCA results), and though substrate diversity was significantly higher at sites with high fish density, only indirect assumptions on the influence of single benthic components are possible. For example, samples with a high contribution from turf and coralline algae showed higher fish densities, whereas samples with a high contribution from live coral and sand showed lower densities. Presence of turf algae inside the territories of these blennies is likely to be related to their feeding preferences (see below), but since this item is highly abundant at all sites (a common feature of south Atlantic reefs; e.g. Ferreira et al. 2004Ferreira C.E.L., Floeter S.R., Gasparini J.L., et al. 2004. Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J. Biogeogr. 31: 1093-1106., Floeter et al. 2005Floeter S.R., Behrens M.D., Ferreira C.E.L., et al. 2005. Geographical gradients of marine herbivorous fishes: patterns and processes. Mar. Biol. 147: 1435-1447., Medeiros et al. 2010aMedeiros P.R., Grempel R.G., Souza A.T., et al. 2010a. Non-random reef use by fishes at two dominant zones in a tropical, algal-dominated coastal reef. Environ. Biol. Fish. 87: 237-246.), it seems not to be a limiting factor on the abundance of O. trinitatis. Instead, as mentioned above, presence of crevices is particularly more important. An investigation on the required surface area of turf algae to supply each individual blenny is, however, necessary and should elucidate this (but see Nursall [1981]Nursall J.R. 1981. The activity budget and use of territory by a tropical blenniid fish. Zool. J. Linn. Soc. Lond. 72: 69-92., who suggested that the territory should include more resources than the minimum required for survival). Nonetheless, optimal sites seem to be those located in shallow depths (Rangel and Mendes 2009Rangel C.A., Mendes L.F. 2009. Review of blenniid fishes from Fernando de Noronha Archipelago, Brazil, with description of a new species of Scartella (Teleostei: Blenniidae). Zootaxa. 2006: 51-61.) with a complex rocky terrace covered by a sufficient percentage of turf cover, with a low vertical profile (low macroalgae cover), and low quantities of coral and sand. In fact, hiding places and high-quality food seem to be common prerequisites for all small territorial herbivores (e.g. Low 1971Low R.M. 1971. Interspecific territoriality in a pomacentrid reef fish, Pomacentrus flavicauda Whitley. Ecology 52: 648-654., Ebersole 1977Ebersole J.P. 1977. The adaptive significance of interspecific territories in the reef fish, Eupomacentrus leucostictus. Ecology 58: 914-920., Labelle and Nursall 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204., Letourneur 1992Letourneur Y. 1992. Spatial and temporal variability in territoriality of a tropical benthic damselfish on a coral reef (Réunion Island). Env. Biol. Fish. 57: 377-391., Haley and Müller 2002Haley M.P., Müller C.R. 2002. Territorial behaviour of beaugregory damselfish (Stegastes leucostictus) in response to egg predators. J. Exp. Mar. Biol. Ecol. 273: 151-159., Medeiros et al. 2010bMedeiros P.R., Souza A.T., Ilarri M.I. 2010b. Habitat use and behavioural ecology of the juveniles of two sympatric damselfishes (Actinopterygii: Pomacentridae) in the south-western Atlantic Ocean. J. Fish Biol. 77: 1599-1615.), given the disadvantageous net costs of defending low-quality territories (see reviews by Dill 1978Dill L.M. 1978. An energy-based model of optimal feeding-territory size. Theor. Popul. Biol. 14: 396 429. and Ebersole 1980Ebersole J.P. 1980. Food density and territory size: An alternative model and a test on the reef fish (Eupomacentrus leucostictus). Am. Nat. 115: 492-509.).

Feeding behaviour

Randall (1996)Randall J.E. 1996. Caribbean reef fishes. T. F. H. Publications Inc., Hong Kong. reported that turf algae were the only preferred benthic item of O. trinitatis and filamentous algae were the primary food item of O. atlanticus. Given the high abundance of turf algae at all study sites (covering a mean of 39.4% of the benthic surface), food is unlikely to be a limiting factor for this species. Roberts (1987)Roberts C.M. 1987. Experimental analysis of resource sharing between herbivorous damselfish and blennies on the Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 111: 61-75., studying Pacific blennies and damselfishes, also suggested that the presence of algae outside territories was evidence that food was not a limiting factor for these fishes. Our observations suggest that turf algae are also highly abundant in unoccupied interstitial spaces outside the territories of O. trinitatis and at the sand-reef ecotone, further supporting this hypothesis. On the other hand, crevice availability seems to be more limited. In fact, blennies were observed associated with substrate of high structural complexity with somewhat low turf cover, but never in turf-rich sites lacking crevices.

Confirming the hypothesis, bite rate decreased with an increase in size of blennies, suggesting an ontogenetic variation in energy demand, which is expected to be higher for developing juveniles (Hernaman et al. 2009Hernaman V., Probert P.K., Robbins W.D. 2009. Trophic ecology of coral reef gobies: interspecific, ontogenetic, and seasonal comparison of diet and feeding intensity. Mar. Biol. 156: 317-330.). Medeiros et al. (2010b)Medeiros P.R., Souza A.T., Ilarri M.I. 2010b. Habitat use and behavioural ecology of the juveniles of two sympatric damselfishes (Actinopterygii: Pomacentridae) in the south-western Atlantic Ocean. J. Fish Biol. 77: 1599-1615. studied the feeding habits of the juveniles of two territorial damselfishes and found similar evidence of ontogenetic shifts in the bite rate of these fishes, but these reports remain somewhat scarce and underreported for most reef fish families.

Feeding rate peaked between 1 and 2 pm and was concentrated in the afternoon. Nursall (1981)Nursall J.R. 1981. The activity budget and use of territory by a tropical blenniid fish. Zool. J. Linn. Soc. Lond. 72: 69-92., studying O. atlanticus, reported that individuals of this species also concentrated their feeding in the afternoon period and employed time-minimized strategies. Our observations support the findings of Mendes (2006)Mendes L.F. 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Rev. Bras. Zool. 23: 817-823., who stated that individuals alternate between fast foraging and resting inside the crevices, as a means of minimizing predation risk during feeding. Nursall (1981)Nursall J.R. 1981. The activity budget and use of territory by a tropical blenniid fish. Zool. J. Linn. Soc. Lond. 72: 69-92. also stated that O. atlanticus allocated 8.5% of its time to feeding. Interestingly, time estimates from unpublished video recordings of several individuals showed that O. trinitatis individuals allocated 8.83% of their time to feeding. Furthermore, these values are considerably lower than those recorded for other reef fishes (e.g. Jones and Norman 1986Jones G.P., Norman M.D. 1986. Feeding selectivity in relation to territory size in a herbivorous reef fish. Oecologia 68: 549-556., Bonaldo et al. 2005Bonaldo R.M., Krajewski J.P., Sazima I. 2005. Meals for two: foraging activity of the butterflyfish Chaetodon striatus (Perciformes) in southeast Brazil. Braz. J. Biol. 65: 211-215., Meekan et al. 2010Meekan M.G., Kuerthy C., McCormick M.I. et al. 2010. Behavioural mediation of the costs and benefits of fast growth in a marine fish. Anim. Behav. 79: 803-809.), supporting Nursall’s affirmation that Ophioblennius species are highly efficient time-minimizers.

Territory size and agonistic behaviours

Territory size of O. trinitatis (0.79 m²) was considerably smaller than those reported by Rylander and Koster (1982)Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115. (between 1.17 and 2.41 m²), but slightly larger than those reported for O. atlanticus by Nursall (1977)Nursall J.R. 1977. Territoriality in redlip blennies, Ophioblennius atlanticus (Pisces: Blenniidae). J. Zool. 182: 205-223. (0.5 m²). Territories defended by O. trinitatis showed local variation in size, being larger at sites with lower fish densities (compare Figs 2a and 5a). As hypothesized, these differences suggest that territory size increases at low-density sites (a density-dependent mechanism). In addition, though food does not seem to influence territory size (see above), it seems that fish need to compensate for residing on lower quality substrates by increasing their territory coverage. Although we found little evidence that food determined territory size, availability of hiding places seems to be a major determinant (see Rylander and Koster 1982Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115.). Therefore, we highlight the importance of structural heterogeneity for site-attached fishes, as also acknowledged for several other reef fishes (e.g. McCormick 1994McCormick M.I. 1994. Comparison of field methods for measuring surface topography and their associations with a tropical reef fish assemblage. Mar. Ecol. Prog. Ser. 112: 87-96., Friedlander and Parrish 1998Friedlander A.M., Parrish J.D. 1998. Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J. Exp. Mar. Biol. Ecol. 224: 1-30., Jones and Syms 1998Jones G.P., Syms C. 1998. Disturbance, habitat structure and the ecology of fishes on coral reefs. Aust. J. Ecol. 23: 287-297.). High-quality territories (sites of high structural complexity) are also important during reproduction, being a prerequisite during mate selection by females (Labelle and Nursall 1992Labelle M., Nursall J.R. 1992. Population biology of the redlip blenny, Ophioblennius atlanticus macclurei (sylvester) in Barbados. Bull. Mar. Sci. 50: 186-204.).

Larger individuals of O. trinitatis defended larger territories, as previously observed for other territorial fishes (Ebersole 1980Ebersole J.P. 1980. Food density and territory size: An alternative model and a test on the reef fish (Eupomacentrus leucostictus). Am. Nat. 115: 492-509., Rylander and Koster 1982Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115., Medeiros et al. 2010bMedeiros P.R., Souza A.T., Ilarri M.I. 2010b. Habitat use and behavioural ecology of the juveniles of two sympatric damselfishes (Actinopterygii: Pomacentridae) in the south-western Atlantic Ocean. J. Fish Biol. 77: 1599-1615.). Our findings suggest that territory size is driven by hierarchical and life-stage forces. Therefore, to achieve typical territorial adult habits, recruits need to first take up interstitial space (i.e. unoccupied area between territories) and gradually increase its area during their development (see Nursall 1977Nursall J.R. 1977. Territoriality in redlip blennies, Ophioblennius atlanticus (Pisces: Blenniidae). J. Zool. 182: 205-223., Robertson 1984Robertson D.R. 1984. Cohabitation of competing territorial damselfishes on a Caribbean coral reef. Ecology 65: 1121-1135.). Nonetheless, field experimental studies are necessary to elucidate these processes.

Regardless of the implications concerning local differences in territory size, optimal territories should be those with the smallest possible area, but including a sufficient food supply and suitable hideaway places. As acknowledged by Rylander and Koster (1982)Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115., these territories should increase the fitness of residents by reducing the risk of foraging away from shelter and the energy spent in territory defence.

Resident O. trinitatis individuals responded differently to fishes recorded inside their territories (i.e. intruders), given that common species such as H. parra, T. noronhanum, A. saxatilis and A. chirurgus were rarely or never attacked. On the other hand, S. rocasensis, Malacoctenus sp. and conspecific individuals were those most subjected to intruder-directed agonistic interactions. Stegastes rocasensis is a highly territorial species with microhabitat and food preferences similar to those of O. trinitatis (Souza et al. 2010Souza A.T., Ilarri M.I., Rosa I.L. 2010. Habitat use, feeding and territorial behavior of a Brazilian endemic damselfish Stegastes rocasensis (Actinopterygii: Pomacentridae). Env. Biol. Fish. 91: 133-144.). Malacoctenus sp., however, has different food habits but is highly site-attached, sharing substrates with O. trinitatis (Rangel and Mendes 2009Rangel C.A., Mendes L.F. 2009. Review of blenniid fishes from Fernando de Noronha Archipelago, Brazil, with description of a new species of Scartella (Teleostei: Blenniidae). Zootaxa. 2006: 51-61.), though sandy areas are also common microhabitats for these fish (author’s personal observation). Therefore, conspecifics, S. rocasensis and, to a smaller extent, Malacoctenus sp., were the most important competitors of O. trinitatis. Focusing agonistic displays towards potential intruders should be energy-efficient, given the unnecessary cost of territory defence towards non-competitive species, which are more often tolerated inside territories (Warner and Hoffman 1980Warner R., Hoffman S.G. 1980. Population density and the economics of territorial defense in a coral reef fish. Ecology 61: 772-780.).

Agonistic interactions towards resident O. trinitatis were mostly made by S. rocasensis and conspecific individuals. In general, for each agonistic attack directed towards an S. rocasensis individual, resident O. trinitatis received over 3.5 counterattacks. Thus, S. rocasensis is a far more aggressive species than O. trinitatis. Mendes (2006)Mendes L.F. 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Rev. Bras. Zool. 23: 817-823. and Nursall (1977)Nursall J.R. 1977. Territoriality in redlip blennies, Ophioblennius atlanticus (Pisces: Blenniidae). J. Zool. 182: 205-223. reported a low frequency of both intra- and interspecific agonistic interactions for O. trinitatis and O. atlanticus, respectively, but Rylander and Koster (1982)Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115. stated that interspecific agonistic interactions between O. atlanticus and two damselfishes were common.

Evidence of size-dependent territory dominance was not observed in the present study. In fact, among conspecifics, residents were more successful at defending territories than intruders were at overtaking them, regardless of individual size. A similar mechanism was acknowledged by Picciulin et al. (2006)Picciulin M., Sebastianutto L., Costantini M. et al. 2006. Aggressive territorial ethogram of the of the red-mouthed goby, Gobius cruentatus (Gmelin, 1789). Electron. J. Ichthyol. 2: 38-49., who stated that resident territorial gobies had a greater chance of maintaining their territories when attacked by an intruder conspecific, regardless of size.

Fish defending larger territories were subject to higher levels of aggressive interactions from intruders, supporting the findings of Rylander and Koster (1982)Rylander M.K., Koster F. 1982. Observations on the biology of the redlip blenny Ophioblennius trinitatis (Pisces: Blenniidae) on the Colombian coast of the Caribbean. An. Inst. Invest. Mar. Punta Betin. 12: 105-115.. Given the obvious dislocation constraints of defending distant borders, larger territories are more vulnerable to intruders. Furthermore, agonistic interactions are expected to be higher at complex sites due to higher fish densities (McCormick 1994McCormick M.I. 1994. Comparison of field methods for measuring surface topography and their associations with a tropical reef fish assemblage. Mar. Ecol. Prog. Ser. 112: 87-96.), but in the present study agonistic interactions were higher at low-complexity sites. This was due to the increased competition for refuge places (i.e. crevices), which are scarce at low-complexity sites.

Despite its aggressive territorial behaviour, O. trinitatis showed some degree of tolerance towards conspecifics. Densities of 2.5 and 3 ind. m^–2 were frequently observed and, in many cases, without intraspecific agonistic interactions, suggesting a possible intraspecific symbiotic sharing of territories (see Robertson and Polunin 1981Robertson D.R., Polunin N.V.C. 1981. Coexistence: symbiotic sharing of feeding territories and algal food by some coral reef fishes from the Western Indian Ocean. Mar. Biol. 62: 185-195.). Since food did not seem to be a limiting factor for the abundance of these blennies, the benefits of symbiotic sharing might overcome the net costs of co-habiting with potential competitors. These benefits appear to be the improved territory defence (given that the task is split among multiple individuals) and the underlying reduced energy cost of employing agonistic displays (Robertson and Polunin 1981Robertson D.R., Polunin N.V.C. 1981. Coexistence: symbiotic sharing of feeding territories and algal food by some coral reef fishes from the Western Indian Ocean. Mar. Biol. 62: 185-195., Norman and Jones 1984Norman M.D., Jones G.P. 1984. Determinants of territory size in the pomacentrid reef fish, Parma victoriae. Oecologia 61: 60-69., Foster 1985Foster S.A. 1985. Group foraging by a coral reef fish: a mechanism for gaining access to defended resources. Anim. Behav. 33: 782-792., Iguchi and Abe 2002Iguchi K., Abe S. 2002. Territorial defense of an excess food supply by an algal grazing fish, ayu. Ecol. Res. 17: 373-380.). Evidence of symbiotic sharing has been previously acknowledged for blennids (e.g. Roberts 1987Roberts C.M. 1987. Experimental analysis of resource sharing between herbivorous damselfish and blennies on the Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 111: 61-75., Townsend and Tibbetts 2004Townsend K.A., Tibbetts I.R. 2004. The ecological significance of the combtoothed blenny in a coral reef ecosystem. J. Fish Biol. 65: 77-90.). Furthermore, Mendes (2006)Mendes L.F. 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Rev. Bras. Zool. 23: 817-823. recorded, at several occasions, up to six ‘tolerating’ Ophioblennius individuals inhabiting a 1 m² area. Future studies, however, should elucidate whether territorial sharing is not simply a temporary sex-related process (i.e. sexual aggregation or harem formation).

ACKNOWLEDGEMENTSTop

We are indebted to A. M. A. Medeiros and R. G. Grempel for assistance during field work, and the staff of Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for providing logistic support and accommodation on the island. The Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) provided financial support.

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