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Latin american journal of aquatic research

On-line version ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.40 no.1 Valparaíso Mar. 2012

http://dx.doi.org/10.4067/S0718-560X2012000100010 

Lat. Am. J. Aquat. Res., 40(1): 102-112, 2012

Research Article

 

From coexistence to competitive exclusion: can overfishing change the outcome of competition in skates (Chondrichthyes, Rajidae)?

De la coexistencia a la exclusión competitiva: ¿Puede la sobrepesca cambiar el resultado de la competencia en rayas (Chondrichthyes, Rajidae)?

 

Natalia L. Ruocco12, Luis O. Lucifora13, Juan M. Díaz de Astarloa14, Roberto C. Menni15 Ezequiel Mabragaña1,5 & Diego A. Giberto1,2

1Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina.
2Instituto Nacional de Investigación y Desarrollo Pesquero, Paseo Victoria Ocampo s/n B7602HSA, Mar del Plata, Argentina.
3Instituto de Biología Subtropical, Universidad Nacional de Misiones, Centro de Investigaciones del Bosque Atlántico (CeIBA), P.O. Box 9, Puerto Iguazú, Misiones, Argentina.
4Universidad Nacional de Mar del Plata, Facultad de Ciencias Exactas y Naturales Departamento de Ciencias Marinas, Funes 3350, B7602AYL Mar del Plata, Argentina.
5Museo de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Argentina
.

Correspondencia a:


ABSTRACT. Competition for food could be a major force driving changes in the community structure of skates (Rajidae) subjected to fishing exploitation. Under this hypothesis, small skates are released from competition with larger skates after fishing has depleted the larger species. Here, we compare the abundance patterns of two sympatric skates with similar niches but different life histories, Bathyraja albomaculata (larger and slow-reproducing) and Bathyraja macloviana (smaller and faster-reproducing), before (1971, 1978) and after (1998-2004) a 108% increase in industrial bottom trawling on the southeastern South American shelf in order to test the prediction that B. macloviana should competitively exclude B. albomaculata after the increase in fishing mortality. In 1971 and 1978, there was no relationship between the abundance of both species, indicating that they coexisted over large scales. In 1998-2004, the relationship between the abundances of these skates was bell-shaped, indicating that both species increased in abundance at low densities until peaking, after which B. albomaculata decreased when B. macloviana became more abundant, consistent with resource competition. We tested whether food may be a potential limiting resource by comparing the diet of both species. The two species consumed mostly polychaetes, differing only in the consumption of polychaetes from the family Nephthyidae, which was much higher for B. macloviana. Bathyraja macloviana could replace B. albomaculata at high densities when food resources may become scarce. These results support the hypothesis that competition release is an important factor explaining the changes in skate communities in overexploited areas.

Keywords: Bathyraja albomaculata, Bathyraja macloviana, Rajidae, diet overlap, resource competition, elasmobranch fisheries, Argentina.


RESUMEN. La competencia por el alimento podría ser una fuerza importante detrás de los cambios en la estructura de las comunidades de rayas (Rajidae) bajo explotación pesquera. Según esta hipótesis, las rayas pequeñas son liberadas de la competencia por las rayas de mayor tamaño, al disminuir la abundancia de éstas últimas por la pesca. En este trabajo, se comparan los patrones de abundancia de dos rayas simpátricas con nichos similares pero con diferentes historias de vida, Bathyraja albomaculata (mayor y de reproducción lenta) y Bathyraja macloviana (más pequeña y de reproducción más rápida), antes (1971, 1978) y después (1998-2004) de un incremento del 108% en el arrastre de fondo industrial en la plataforma sudeste de América del Sur, para evaluar la predicción que B. macloviana excluiría competitivamente a B. albomaculata después del aumento en la mortalidad por pesca. En 1971 y 1978, no hubo relación entre las abundancias de ambas especies, indicando que, a escalas grandes, coexistían. En 1998-2004, la relación entre las abundancias de ambas especies tuvo forma de campana, indicando que ambas incrementaron su abundancia a densidades bajas hasta alcanzar un máximo, a partir del cual la abundancia de B. albomaculata disminuyó a medida que aumentaba la de B. macloviana, patrón consistente con la competencia por uso de recursos. Se evaluó si el alimento puede ser un recurso limitante mediante la comparación de la dieta de ambas especies. Ambas especies consumieron predominantemente poliquetos y difirieron sólo en el consumo de poliquetos Nephthyidae, mucho mayor en B. macloviana. B. macloviana remplazaría a B. albomaculata a altas densidades, cuando el alimento podría ser escaso. Estos resultados apoyan la hipótesis de que la liberación de la competencia es un factor importante en los cambios en las comunidades de rayas sobreexplotadas.

Palabras clave: Bathyraja albomaculata, B. macloviana, Rajidae, solapamiento de dieta, competencia por recursos, pesquerías de elasmobranquios, Argentina.


 

INTRODUCTION

Competitive interactions that structure communities are usually not accounted for in fisheries management. Fishing usually affects a number of species simultaneously, but fisheries are mostly managed focusing on the target population without taking into account species interactions or other community processes in which the target population plays a role (Pauly et al., 2002; Pikitch et al., 2004; Myers & Ottensmeyer, 2005) . As a result, unforeseen fishing effects usually spread throughout marine communities with serious consequences (Jackson et al., 2001; Jennings et al., 2001; Worm et al., 2006; Daskalov et al., 2007; Myers et al., 2007).

Skates (Rajidae), as a group, are highly affected by fisheries, but different species may differ in their response to fishery exploitation. Several species of skates have suffered large declines or even extirpation from large parts of their geographic range due to fisheries overexploitation (Brander, 1981; Casey & Myers, 1998; Graham et al., 2001; Devine et al., 2006) . It is apparent that they vary in their capacity to withstand exploitation and the abundance of smaller species increases after fishing removes larger species. This has been hypothesized to be a result of competition release, which allows the smaller, faster-reproducing species to replace the largest ones.

Walker & Heessen (1996), Walker & Hyslop (1998) and Dulvy et al. (2000) observed conspicuous shifts in the skate community of the North Sea, after decades of heavy fishing pressure. Dulvy et al. (2000) hypothesized that this shift was the result of competitive release, since small skate species replace the larger ones after fishing released small species from competition with large species, leading to shifts in community structure. Dulvy et al. (2000) suggested that food would be the limiting resource behind the competitive relationship of skates in the North Sea, since skates are all benthic feeders preying upon a variety of invertebrates and small fishes.

Competition is usually studied at small scales where experiments are feasible. Most of the best evidence for competition in vertebrate communities comes from small-scale experiments (in the scale of m2 or at most hectares) and from small-bodied organisms, such as small fishes (Schmitt & Holbrook, 1999), lizards (Petren & Case, 1996) and small mammals (Meserve et al., 1996). While controlled experiments provide the most unambiguous evidence for competition, their unfeasibility at large scales makes them impractical to study the importance of competition in large-scale communities (Connell, 1983).

As fisheries affect communities at a large scale (usually of hundreds or thousands of km2), where controlled experimentation is not possible, other approaches must be taken to study how competition may structure marine communities and how fishing may interact with competition to affect ecological processes desired to be maintained. These alternative approaches have been successfully applied in large-scale studies to infer the presence of competition in both terrestrial (Creel & Creel, 1996; Cooper et al., 2007) and marine (Ruggerone et al., 2003) species.

In this paper we use an alternative, non-experimental, modelling approach to study competition at a large scale. Our approach compares the relationship between the abundance of two skates before and after the hyper-development of industrial trawl fishing on the southeastern South American shelf, in order to test Dulvy et al.'s (2000) hypothesis. The theoretical basis for our rationale is as follows. Over large-scale communities, without human exploitation, the patterns of species abundance are more constant than at smaller scales (Sommer & Worm, 2003). At this large scale, species coexist, even though they may suffer local extinctions or colonize new places at smaller scales within the large-scale community as a result of competition (Ritchie, 2003). In this community, the abundances of both species do not show any particular relationship. On the other hand, if fisheries affect the competitive relationship between skates, as suggested by Dulvy et al. (2000), there should be a negative relationship between two competing skates, at least at high densities, when resources become scarcer (i.e. limiting).

The southeastern South American shelf, between 35° and 55°S, contains a diverse skate fauna (Menni & Stehmann, 2000; Cousseau et al., 2007) and is subjected to intense, unsustainable fishing exploitation by bottom trawlers since the early 1990s (Agnew et al., 1999; Campagna et al., 2006; Cañete, 2006). From 1990 to 1995 the fishing effort on this area increased by 108% (Campagna et al., 2006), and present levels of fishing effort in the area, as estimated from fuel consumption, are among the highest in the world (Tyedmers et al., 2005). This resulted in the overexploitation of many chondrichthyan and bony-fish populations (Carozza et al., 2004; Cordo, 2004; Massa et al., 2004; Wohler et al., 2004). Skates from this area are affected by at least four different bottom-trawl fisheries, both as a target and bycatch. The white-dotted skate, Bathyraja albomaculata, and the Patagonian skate, B. macloviana, are two common skates affected by these fisheries. Both species are targeted by the Islas Malvinas rajid fishery (Agnew et al., 2000) and as bycatch in finfish trawlers targeting Argentine hake, Merluccius hubbsi, southern blue whiting, Micromesistius australis, hoki, Macruronus magellanicus (Brickle et al., 2003), and red shrimp, Pleoticus muelleri (Cedrola et al., 2005).

Bathyraja albomaculata attains 99 cm in total length and starts to reproduce at 10 years (Henderson et al., 2004; Bücker, 2006). On the other hand, B. macloviana is the smallest species of the genus in the southwestern Atlantic, reaching 67 cm in total length and matures at 5-6 years (Bücker, 2006). Both species are specialized feeders, being polychaetes their dominant prey (Mabragaña et al., 2005; Scenna et al., 2006; Ruocco et al., 2009), which results in a high dietary overlap suggestive of a potential competitive interaction between them (Brickle et al., 2003). Thus, B. albomaculata and B. macloviana are a good model system to study the competitive release hypothesis in skates because both species suffer a similar fishing pressure, potentially overlap in the use of some resource (i.e. food) and have a large difference in age at maturity, with B. macloviana maturing at about half the age of B. albomaculata.

Here, we compare the abundance and diet of the white-dotted skate, B. albomaculata, and the Patagonian skate, B. macloviana, at a large scale -the southeastern South American shelf between 35 and 55°S- before and after a major increase in fishing effort in order to test the hypothesis that competition may occur between the two species.

MATERIALS AND METHODS

Pre-fishing abundance patterns

Pre-fishing abundance patterns were estimated using data from 241 stations trawled during two research cruises carried out in 1971 and 1978 that covered the area from 37.9° to 54°S, at depths between 30 and 450 m (Fig. 1). Standard commercial 42.7 and 60.9 m wide bottom trawl nets were used in the 1971 and 1978 cruises, respectively, which were conducted by the same vessel. All tows lasted 30 min at a speed of 4 knots.



Figure 1. Southeastern South American shelf showing the location of pre-fishing (1971 and 1978, black circles) and post-fishing (1998-2004, white circles) trawl stations used in the analyses.
Figura 1. Plataforma continental de América del Sur con las estaciones de muestreo utilizadas en el análisis antes (1971 y 1978, círculos negros) y después (1998-2004, círculos blancos), del desarrollo de la pesquería.

To explore the relationship between the abundance of B. albomaculata and B. macloviana, we constructed generalized linear models (GLM) with a log link and a negative binomial error distribution to account for the large number of zeros in the data and the dependance of the variance on the mean. All models included the number of individuals of B. albomaculata (NBa) as the dependent variable. NBa rather than the number of individuals of B. macloviana (NBm) was included as the dependent variable because Dulvy et al.'s (2000) hypothesis predicts that the larger and slower-reproducing species, in this case B. albomaculata, will be affected by the smaller and faster-reproducing species, in this case B. macloviana, after an increase in fishing pressure. All possible combinations of season (S; summer or winter), depth (D), latitude (L) and NBm were included as independent variables. To deal with nonlinear effects of D and NBm, models with quadratic terms (i.e. D + D2 and NBm + AW2) were also fitted. We could not include log(swept area) as an offset variable (see below) for the pre-fishing analysis because we did not have that information for these cruises. However, as the data come from research cruises, all tows were performed in a standardized fashion, with swept area not expected to vary substantially between trawl stations.

Akaike's Information Criterion (AIC) were computed for each model. The most parsimonious model (i.e. hypothesis) was chosen as that with the lowest AIC (Franklin et al., 2001; Johnson & Omland, 2004).

Post-fishing abundance patterns

A total of 452 trawling stations from 7 research cruises conducted between 1998 and 2004, from 35° to 55°S, at depths between 46 and 380 m were used in this analysis (Fig. 1). A 59 m Engel-type bottom-trawl net, with a stretched mesh size of 200 mm in the wings and 103 mm in the codend, a vertical height of 4 m, and a horizontal opening of 15 m was used in all research cruises. Each haul lasted 30 min and trawling speed was 3.6 knots. The surveys were aimed at the assessment of Argentine hake, Merluccius hubbsi, southern blue whiting, Micromesistius australis, hoki, Macruronus magellanicus, and Argentine squid, Illex argentinus.

As for the pre-fishing analyses, GLMs with a log link and a negative binomial distribution were used. All models included the number of B. albomaculata caught per trawl (NBa) as the dependent variable and the log of the swept area as an offset variable. All possible combinations of number of B. macloviana caught per trawl (NBm), latitude (l), depth (D), sin, cosine, 2 χ sin and 2 χ cosine of Julian day (d) were included as independent variables. Models with quadratic terms (i.e. D + D and NBm + NBm2) were also fitted. The best hypothesis was chosen using information theory in the same way as with the pre-fishing analyses, as the model with the lowest AIC.

Measurement error

In both pre- and post-fishing situations, the abundance of both B. macloviana and B. albomaculata were measured with error. This situation violates the assumption of GLMs that explanatory variables are measured without error. To deal with this situation, we reestimated the parameters for NBm in the cases when the best model included the terms NBm or NBm + NBm2. We did this by using the simex method (Cook & Stefanski, 1994). Simex reestimates the parameters of the model through an iterative procedure that inflates the measurement error by a factor λ, creating several estimates (one for each value of λ) and extrapolating the estimation to the case of no measurement error. As the measurement error was unknown (no repeated sampling at the same time and place was performed), we repeated the simex procedure for a range of levels of measurement error extending over 4 orders of magnitude (i.e. standard error = 1, 10, 100 and 1000).

Dietary analysis

To evaluate if feeding habits were a possible overlapping resource between the two species, we analyzed the stomach contents of 89 specimens of B. albomaculata and 88 of B. macloviana caught in scientific surveys in the southwestern Atlantic between 37° and 55°S, over a depth range of 43-440 m, between 2000 and 2003. The net and trawl specifications were the same as for the analysis of post-fishing abundance. For each specimen, total length and sex were recorded. The stomachs were removed, frozen and subsequently analyzed in the laboratory. Prey were identified to the lowest possible taxonomic level, counted and weighted to the nearest 0.01 g. Only 12 stomachs of B. albomaculata were empty. Sample sufficiency was assessed by constructing accumulation curves for the number of prey species as a function of the number of skates examined for stomach contents, after randomizing the sampling order 1000 times. Sample size was judged to be sufficient if the curves reached an asymptote.

The number of each prey group consumed by each individual was modeled as a function of species, sex, total length, latitude, depth and year in order to test for differences between species while controlling for the effects of the other variables. For each prey, a generalized linear model with a log link and a negative binomial error distribution was constructed (Lucifora et al., 2009a, 2009b; Barbini & Lucifora, 2011). Afterwards, the best minimum model (BMM) was chosen by minimization of the AIC. Differences in diet between species were considered important if the variable species was included in the BMM. The magnitude of inter-specific differences in the consumption of a given prey was quantified by the BMM coefficient for the variable "species".

RESULTS

Pre-fishing abundance patterns

There was no relationship between the abundances of B. albomaculata and B. macloviana during 1971 and 1978, well before the development of intense industrial fishing (Fig. 2a). The best model explaining the abundance of B. albomaculata included the variables S, D and D2, but not abundance of B. macloviana, indicating that both species coexisted at all densities of B. macloviana. The best model had the following parameters: intercept = -6.841, S(winter relative to summer) = 0.662, D = 0.054, D2 = -0.0001 (AIC = 241.8).



Figure 2. Relationship between the abundance of the skate Bathyraja albomaculata as a function of the abundance of B. macloviana on the southeastern South American shelf. a) Pre-fishing situation between 1971 and 1978, b) post-fishing situation between 1998 and 2004. White circles are fitted values for the best models in each situation. The solid line in (b) is the relationship estimated from a generalized linear model with a negative binomial error distribution and a log link. A small amount of jitter was added to the data in the plots (not in the analyses), to improve visualization of overlapping data points.

Figura 2. Abundancia de la raya Bathyraja alboma-culata en función de la abundancia de la raya B. macloviana en la plataforma del sudeste de América del Sur. a) Situación pre-pesca entre 1971 y 1978, b) situación post-pesca entre 1998 y 2004. Los círculos blancos son valores ajustados por los mejores modelos de cada situación. La línea continua en (b) es la relación estimada por el modelo lineal generalizado con distribución binomial negativa y enlace logarítmico. Para mejorar la visualización debido a la superposición de puntos, se movieron muy levemente algunos puntos (sólo para visualización, no para el análisis).

Post-fishing abundance patterns

Between 1998 and 2004 there was a change in the interaction between B. albomaculata and B. macloviana, as compared to the pattern in 1971 and 1978. The abundance of B. albomaculata increased at low densities of B. macloviana, reached a peak and decreased at high densities of B. macloviana (Fig. 2b).

The best model describing the relationship of the abundance of B. macloviana and B. albomaculata included L, 2 χ sin (d), cos (d), D, D2, NBm and NBm2. The parameters of the model were: intercept = 0.321, L = -0.088, 2 χ sin (d) = -0.846, cos (d) = -0.571, D = 0.067, D2 = -0.0001, NBm = 1.346, NBm2 = -0.157 (AIC = 552.55).

Application of the simex procedure did not lessen the effect of NBm and NBm2, as their coefficients remained high. For each level of measurement error tried (1, 10, 100 and 1000), the coefficients for both parameters were 2.573 and -0.310, 1.588 and -0.226, 2.943 and -0.461, and 3.019 and -0.471, for NBm and NBm2, respectively.

Dietary analysis

The most important prey found in both species were polychaetes, amphipods and isopods, while cirripeds, crabs, cumaceans, brittlestars and mollusks were the less consumed prey; for this reason these prey were grouped together for analysis as "other prey". Accumulation curves reached an asymptote for both species, indicating that sample size was sufficient to describe diet in each species (Fig. 3).



Figure 3. Accumulation curves for prey species of the skates Bathyraja albomaculata and B. macloviana on the southeastern South American shelf, as a function of number of skates examined for stomach contents. The solid line represents the mean number of prey species for a given sample size and the shaded area is ± 1 standard error, after 1000 permutations of the sampling order. The asymptote reached indicates that a sufficient number samples was examined.

Figura 3. Curvas acumulativas de especies presa de las rayas Bathyraja albomaculata y B. macloviana en la plataforma suroriental de América del Sur, en función del número de estómagos examinados. La línea continua representa el número medio de especies presa para un tamaño muestral determinado y el área sombreada corresponde a ± 1 error estándar, después de 1000 permutaciones del orden de muestreo. El alcance de una asíntota indica que se examinó un número suficiente de muestras.

Diet was very similar in the two species; it only differed in the consumption of polychaetes of the family Nephthyidae which was 38 times higher in B. macloviana. The only two other prey with a different consumption among skate species were unidentified polychaetes (3 times as common in B. macloviana as in B. albomaculata) and other prey (0.4 times as common in B. macloviana as in B. albomaculata) (Fig. 4).


Figure 4. Comparative consumption of 11 prey groups by the skates Bathyraja albomaculata and B. macloviana on the southern South American shelf. Values are standardized by sex, total length, latitude, depth and year of sampling. Prey marked with an asterisk were consumed in significantly different amounts by the two species. Bold line: median; box: interquartile range; whiskers: range (1.5 times the interquartile range); circles: outliers.

Figura 4. Comparación del consumo de 11 grupos de presas de las rayas Bathyraja albomaculata y B. macloviana en la plataforma del suroriental de América del Sur. Los valores están estandarizados por sexo, longitud total, latitud, profundidad y año de muestreo. Las presas marcadas con un asterisco fueron consumidas en cantidades significativamente diferentes por las dos rayas. Línea gruesa: mediana; límites del recuadro: rango intercuartil; líneas: rango (1,5 veces el rango intercuartil); círculos: valores extremos.

DISCUSSION

Our results are consistent with the hypothesis that competitive release allows fast-reproducing skate species to exclude slow-reproducing ones producing a shift in skate community structure after heavy fishing pressure (Dulvy et al., 2000). In a non-equilibrium community, such as one subjected to a high fishing pressure, a medium-sized but smaller, faster-reproducing skate, B. macloviana, outcompetes a larger, slow-reproducing species, B. albomaculata, as proposed by Dulvy et al. (2000). This situation contrasts with the coexistence of both species at all densities observed during 1971 and 1978, well before the hyper-development of industrial fishing in the early 1990s that persists at present (Campagna et al., 2006).

Coexistence is the rule in natural communities of mobile animals, even when competition occurs (Ritchie, 2003). Exclusive resources- i.e. those resources used solely by one of the competitors- allow species to coexist, even when both species compete for many other shared resources (Ritchie, 2003). Due to the lack of biological data during the pre-fishing years, we can only speculate about which resources were exclusively used by B. macloviana or B. alboma-culata that may have allowed coexistence of both species during the pre-fishing years. The almost exclusive use of Nephthyid polychaetes by B. macloviana suggests that they could have been used as an unshared resource, assuming that diet composition has not changed substantially from the pre-fishing to the post-fishing ecosystem state.

We propose that intense fishing pressure shifted the balance in favor of B. macloviana because of its earlier sexual maturation as compared to B. albomaculata. Given its earlier age at maturity -an important determinant of population growth and recovery in many marine fishes (Myers et al., 1997; Heppell et al., 1999; Cortés, 2002; Reynolds et al., 2005)- B. macloviana may cope better with fishing mortality than B. albomaculata. By having a higher productivity, B. macloviana may have a higher recolonization rate than B. albomaculata and replace it, once B. albomaculata was removed from a given area by fishing.

Resource competition, rather than interference competition, is consistent with the bell-shaped relationship between the abundance of B. alboma-culata and B. macloviana after the hyper-development of industrial fisheries on the southeastern South American shelf. At low densities, when resources are not limiting, the abundance of both species is positively correlated due to their similarity in resource use, i.e. both species increase in sympatry because the shared resource is not limiting, since both species are at low densities. On the other hand, at high densities, when resources become scarcer, B. macloviana outcompetes B. albomaculata. The dominance of B. macloviana is due to their faster population dynamics which is explained by its earlier maturity (Bücker, 2006). Then, under a similar fishing pressure, the faster growing population dominates over the slower growing one. The dominance of B. macloviana (the smallest species) over B. albomaculata suggests that, as proposed by Dulvy et al. (2000), resource competition rather than interference competition is operating, since in interference competition usually the larger species dominates over the smaller one (Fedriani et al., 2000; Valeix et al., 2007).

Information on composition and distribution of benthic communities from the southeastern South American shelf is scarce and precluded any analysis of the potential effects of prey availability on the relationship between the abundances of B. macloviana and B. albomaculata. The only study that covered all our study area found three areas differing in their benthic assemblages (considering only mollusks, bryozoans and echinoderms): 36°-43°S and 43°-55°S below the 100 m isobath, and 39°-55°S beyond the 100 m (Bastida et al., 1992). Information on polychaete distribution is available only for the southern (Bremec et al., 2000; Montiel et al., 2005 and references therein) and the northern (Bremec & Giberto, 2006) extremes of the study area. In those areas, polychaetes have an heterogeneous distribution, with some regions of low faunistic similarity due to differences in sediment composition and ocea-nographic conditions. The main prey of both B. macloviana and B. albomaculata, Opheliid poly-chaetes, are uncommon in some regions of the shelf, contributing with less than 5% of the total individuals sampled by Bremec et al. (2000) and Bremec & Giberto (2006). However, there is no comparable data of the density of these polychaetes that could be used to estimate the food availability for the skates. The potential effects of differences in spatial availability of prey on our results should be considered in future studies.

Other ecological processes, such as the negative effects of shared enemies (apparent competition; Bonsall & Hassell, 1997; Morris et al., 2004), might contribute to explain the pattern between the abundance of both species observed as well. If B. macloviana is more resilient to some shared predator or parasite than B. albomaculata, when both species are in sympatry, these enemies will affect B. alboma-culata more heavily than B. macloviana, resulting in the apparent exclusion of B. albomaculata by B. macloviana. This might occur, for instance, if both species differ in the ability to detect predators, as observed in stingrays (Semeniuk & Dill, 2006). Nothing is known on the effect of predators, parasites or other potential natural enemies on populations of species of Bathyraja, which precludes any evaluation of this hypothesis. However, although apparent competition might play some role in producing the observed pattern, the high similarity in diet of both species suggests that, at high densities, food can become a limiting resource, and then competition may operate.

We described an example of change in the relationship of abundances of two ecologically similar skate populations after intense exploitation. This example may indicate that intense industrial fishing pressure may produce shifts in competitive interactions that may lead to shifts in skate community structure. The pattern found for B. albomaculata and B. macloviana supports the hypothesis that skate communities may experience shifts in structure due to competitive release (Dulvy et al., 2000), and give further reasons for an ecosystemic management of fisheries (Pauly et al., 2002; Pikitch et al., 2004; Myers & Ottensmeyer, 2005). Management of fisheries that affect skates should focus on the most sensitive species instead of the target species (Myers & Ottensmeyer, 2005) in order to avoid fishery-driven changes in skate communities and marine ecosystems.

The high speed of the changes in species interactions after overfishing -only 8-14 years after the commencement of large-scale industrial fishing in 1990- in a previously near-pristine region (Bortolus & Schwindt, 2007) calls for rapid action to avoid large-scale changes in ecosystem functioning.

ACKNOWLEDGEMENTS

N.L. Ruocco was supported by a scholarship from CONICET (Argentina). Research cruises in 1971 and 1978 were carried out by RV "Walther Herwig" of the Hamburg Fisheries Institute (Germany). Research cruises in 1998-2004 were carried out by RVs "Capitán Oca Balda" and "Dr. Eduardo Holmberg" of the National Institute of Fisheries Research and Development (INIDEP, Argentina). This study was partially supported by funds from CONICET (PIP 5009). We thank Francesco Ferretti for comments on the manuscript and Wade Blanchard for advice on statistical procedures.

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Received: 17 February 2010; Accepted: 5 January 2011.

Corresponding author: Luis O. Lucifora (luis.lucifora@gmail.com)