Revista chilena de historia natural
versión impresa ISSN 0716-078X
Rev. chil. hist. nat. v.80 n.4 Santiago 2007
Revista Chilena de Historia Natural 80:431-437,2007
Trophic niche overlap between two Chilean endemic species of Trichomycterus (Teleostei: Siluriformes)
Sobreposición de nicho alimentario de dos especies endémicas chilenas de Trichomycterus (Teleostei: Siluriformes)
SERGIO SCOTT*, RODRIGO PARDO & IRMA VILA
Laboratorio de Limnología, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Santiago, Chile; *e-mail for correspondence: email@example.com
Trichomycterus areolatus and Trichomycterus chiltoni are endemic siluriform fishes of Chile. They are the only Chilean species of this genus that live in sympatry and coexist in the Biobio basin. High trophic niche overlap between both species was found. Horn's index varied from 0.668 to 0.885 among seasons, without significant differences, and Schoener's index varied from 0.639 to 0.912. Also the discriminant analysis showed no significant differences in prey item between the two species. Trophic composition of T. chiltoni and T. areolatus consisted mainly in chironomid larvae and other aquatic invertebrates. At all seasons T. chiltoni showed the greatest prey richness. Principal component analysis (PCA) showed a high similarity between diets of T. areolatus and T. chiltoni. These diet scores were significantly related with body size in T. chiltoni whereas T. areolatus showed a significant relationship with seasons. This may indicate a generalist strategy in T. areolatus by varying its diet in function of available prey items in each season, whereas T. chiltoni would be specialized in relation to individual size and intraspecific habitat partitioning.
Key words: diet, sympatry, Trichomycterus areolatus, Trichomycterus chiltoni.
Trichomycterus areolatus y Trichomycterus chiltoni son peces Siluriformes endémicos de Chile, siendo las únicas especies chilenas conocidas de este género que coexisten en simpatría. Se encontró alta sobreposición de nicho trófico entre estas dos especies. El índice de Horn varió de 0,668 a 0,885 entre estaciones, sin diferencias significativas, y el índice de Schoener varió de 0,639 a 0,912. Además el análisis discriminante no mostró diferencias significativas en las presas entre las dos especies. La composición de la dieta de T. chiltoni y T. areolatus consistió principalmente en larvas de chironómidos y otros invertebrados acuáticos. En todas las estaciones estudiadas T. chiltoni mostró una riqueza de presas mayor. El análisis de componentes principales (PCA) mostró una gran similitud entre las dietas de T. areolatus y T. chiltoni. Estos resultados se relacionaron significativamente con las medidas de tamaño corporal en T. chiltoni mientras que T. areolatus mostró una relación significativa con las estaciones. Esto podría indicar una estrategia generalista en T. areolatus, variando su dieta en función de las presas disponibles en cada estación, mientras que T. chiltoni estaría especializado en función del tamaño individual.
Palabras clave: dieta, simpatría, Trichomycterus areolatus, Trichomycterus chiltoni.
Early notions of ecological relations of closely related species indicate that these species cannot occupy the same habitat unless they differ in resource utilization (Dumas 1964). Most studies compare closely related taxa that occur in allopatry. Nevertheless in sympatry, the stabilizing forces that promote niche conservatism.
inhibiting niche shifts, may be countered by natural selection favouring ecological divergence to minimize the intensity of interspecific interactions (Losos et al. 2003). This agrees with the competitive exclusion principle that indicates that if two or more non-interbreeding populations compete for the same limited resources, then all but one of them will be driven to extinction (Hutchinson 1965). In this paper we examine trophic relationships of two congeneric freshwater fishes that inhabit the same basin.
In Chilean freshwater ecosystems sympatric coexistence of congeneric fishes is an unusual phenomenon (Vila et al. 1999, Dyer 2000, Vila & Pardo 2006), which may be explained in part by niche segregation through resource partitioning (i.e., diet, time and/or space, Schoener 1974). Habitat shift is a common mechanism for niche segregation in freshwater fishes (Werner & Hall 1977). However, niche partitioning may have an asymmetric effect among species, relegating the weakest competitor to marginal habitats (Nilson 1967, Werner & Hall 1976, 1977), where populations are more susceptible to local extinction (Zaret & Paine 1973).
Trichomycterus is a catfish genus including about 120 species, commonly found in neotropical headwater streams (Eigenmann 1918, Pouilly & Miranda 2003). In Chile, Trichomycterus is represented by five endemic species with a wide altitudinal and latitudinal distribution (Pardo et al. 2005). These species inhabit the rhithronic zone of freshwater systems and show the highest relative abundance among native fishes. Trichomycterus areolatus Valenciennes, inhabits rivers from Huasco (28° 27' S) to Chiloé island (41° 27'S), and Trichomycterus chiltoni (Eigenmann) endemic at Biobio basin (36° 49' S) (Dyer 2000, Habit et al. 2006, Vila et al. 2006). These two species overlap extensively in the Biobio basin, and they are the only species of this genus that live in sympatry in Chile (Arratia 1981). The morphological differentiation between them is slight, however adults of T. chiltoni reach a larger total length (maximun length 170 mm) than T. areolatus (maximun length 116 mm) (Eigenmann 1927). This similarity probably increases their potential competitive interactions, mainly due to the high morphological resemblance (Eigenman 1927) and the similar bottom-dwelling behaviour (Arratia 1990). Besides, T. areolatus and T. chiltoni may be classified as strict insectivores, feeding mainly on aquatic insects (Habit et al. 2005), and these fishes, as do other siluroids, scrape organisms from plant and rock surfaces (Aranhaetal. 1998).
The present study investigated the diet of Trichomycterus species from Biobio River, studying their mutual trophic interactions. The purpose was to infer the ecological process that could ameliorate the competitive interaction between these species, thereby sustaining their present coexistence.
MATERIALS AND METHODS
Biobio basin (36°43'-38°55' S, 70°49'-73° 10' W) has an Andean origin, and its drainage area of 24,029 km2 represents Chile's third largest river basin. It is a typical western Andean system characterized in having a length of ~380 km and a marked change in flow that varies between seasons from 300 to 1,200 m3 s_1. Local climatic conditions are Mediterranean with 1,308.2 mm of mean annual precipitation and a mean annual temperature of 12.4 °C (Niemeyer & Cereceda 1984).
In this basin 14 endemic species of fishes have been reported, corresponding to 31.8 % of the Chilean native species (Campos 1985, Ruiz etal. 1993, Vila et al. 1999).
From 1994 to 2000, bimonthly collections of T. areolatus and T. chiltoni specimens were made in the Biobio basin obtaining 452 specimens among which T. chiltoni was the most abundant (76.8 %). Fishes were captured using a Coffelt electrofishing backpack equipment and were preserved in 4 % buffered formalin. All esophagii and stomachs of captured specimens were analyzed and 70.4 % were empty, where T. areolatus shows the lowest proportion of empty stomachs (59.1 %), compared with T. chiltoni (79.2 %).
Prey items in the esophagus and stomach were analyzed under a dissecting microscope, and identified to order or family level whenever possible with available keys (Merritt & Cummins 1978, Lopretto & Tell 1995). Also, fishes were sexed and total body length measured with 0.1 mm precision. Total and eviscerated specimens were weighted with 0.01 g precision.
Horn's index of niche overlap (Krebs 1999) was calculated between T. areolatus and T. chiltoni on a seasonal basis. As a complement and due to the absence of quantitative data concerning the resources, Schoener's overlap index (Schoener 1970, Wallace 1981, Kahl 2006) was determined. The confidence intervals of Horn's index were estimated using the percentile method by bootstraping 10.000 individual diets (Manly 1997). A principal components analysis (PCA) was applied to individuals showing at least one prey item. For each species, the PCA scores of the first and second axes were related to date, body length, total and eviscerated weight, using Spearman's rank correlation (Zar 1996).
Also, to evaluate differences in trophic niche between T. areolatus and T. chiltoni, a Discriminant Analysis was performed, with a Jack-knifed classification matrix, that was complete using the first, second and third axis of PCA analysis of diet composition (Fisher, 1936).
Trophic composition of T. chiltoni and T. areolatus consisted mainly of chironomids in all seasons (Fig. 1). Ephemeroptera was almost absent in both species during winter, but represented almost 20 % of prey items the rest of the year. Prey organisms that represented less than five percent (Others), include the following insects: Coleóptera, Diptera, Baetidae, Tipulidae, Simulidae and Odonata; crustaceans: Decapoda and Amphipoda; Hirudinea and molluscs. Prey items of the class Others (Fig. 1) in T. areolatus were less diverse but more abundant. Trichomycterus chiltoni showed the greatest niche breadth.
Horn's trophic niche overlap between T. chiltoni and T. areolatus varied from 0.668 to 0.885, among seasons. Higher values were found during summer and spring, but 95 % bootstrap confidence interval overlapped between all seasons (Fig. 2), showing non-significant differences between them. On the other hand, Schoener's overlap index presented similar variation from 0.639 to 0.912 in summer and autumn, respectively. Intermediate values were found in winter (0.814) and spring (0.835).
The first two PCA factors, performed using the diet composition of T. areolatus and T. chiltoni at all seasons, explained over 85 % of the variance. That would indicate a strong similarity between diets of these species (Fig. 3). However, in T. areolatus the first PCA factor was correlated significantly with the sampling date, whereas the first and second factors of T. chiltoni showed a strong relationship with body size (Table 1). PCA was more effective in classifying T. chiltoni than T. areolatus (Table 2). The discriminant analyses showed no significant differences in prey items between the two species (Wilks' lambda = 0.98, F4 137= 0.75, P = 0.56).
Fig. 2: Horn's indices of niche overlap between T. chiltoni and T. areolatus calculated for all seasons. Error bars represent bootstrap 95 % confidence intervals.
Fig. 3: Plot representing the first two factors of a principal components analysis performed on the diet composition of T. chiltoni (A) and T. areolatus (+), between 1994 and 2000 in all seasons. Percentage of the total variance of each factor is shown in parenthesis.
According to previous works (Habit et al. 2005) and to our results, Trichomycterus areolatus and T. chiltoni are mainly benthic feeders, preying mostly on insect larval stages. Our estimates of resource partitioning between T. areolatus and T. chiltoni in the Biobio River, revealed high Schoener's niche overlap, which is consistent with Horn's overlap values in the trophic niche throughout the year. Also, the discriminant analysis does not show significant differences between these two species, indicating a greater discrimination by T. chiltoni individuals than by T. areolatus ones, showing the highest overlap at smaller sizes. These results led us to consider that these fishes should present mechanisms to avoid competitive interactions when the resources are scarce (Hutchinson 1965). Feeding results of T. areolatus and T. chiltoni suggest these two species may coexist mainly due to differences in their observed diet patterns. Trichomycterus areolatus correlates its diet with seasonal changes, and this would be related to the well described yearly changes shown by insect abundance and diversity (Fernández et al. 2001, Sabando 2004). We speculate that this implies generalist behaviour, associated to seasonal resource changes. On the other hand T. chiltoni shows a differential diet at different body sizes as intraspecific habitat partitioning (Arratia 1983). The prey items captured by T. chiltoni showed a greater taxa richness, what could be explained by the larger size that this fish reaches, allowing consumption of all preys eaten by T. areolatus plus bigger items such as decapods and dragonfly larvae that are absent in the stomach contents of T. areolatus. This widening in the trophic niche could be related with morphological characteristics such as mouth and body size that determine, in many cases, the types of prey consumed by fishes (Keeley & Grant 1997, Karpouzi & Stergiou 2003). Size range in these catfishes would have a constraining influence on the kind of trophic niche and therefore, on the feeding mechanism as well (Adriaens 2003). Thus, we suggest that the higher relative abundance of T. chiltoni in the Biobio river can be attributable to interspecific competition, with an asymmetric competitive feeding relationship that clearly favours T. chiltoni and suggests that T. areolatus is the weakest competitor. Future work should consider exclusion experiments that could support the suggested competitive relationship between T. chiltoni and T. areolatus described herein.
Rodrigo Pardo and S. Scott were supported by a MECESUP fellowship UCO-0214, Red Nacional de Programas de Doctorado en Ecología Sistemática y Evolución. We are very grateful to R. Medel for providing valuable criticism and the Centro de Ecología Aplicada (CEA) for providing the sampling.
ADRIAENS B (2003) Feeding mechanisms. In: Arratia G, BG Kapoor & M Chardon (eds) Catfishes: 221-248. Science Publishers, Inc., Enfield, Connecticut, USA. [ Links ]
ARANHA JMR, DF TAKEUTI & TM YOSHIMURA (1998) Habitat use and food partitioning of the fishes in a coastal stream of Atlantic forest, Brazil. Revista de Biología Tropical 46: 951-959.
ARRATIA G, G ROJAS & A CHANG (1981) Los peces de las aguas continentales de Chile. Publicación Ocasional del Museo Nacional Historia Natural (Chile) 34: 1-108.
ARRATIA G (1983) Preferencias de habitat de peces siluriformes de aguas continentales de Chile (Fam. Diplomystidae y Trichomycteridae). Studies of Neotropical Fauna and Environment 18: 217-237.
ARRATIA G (1990) The South American Trichomycterinae (Teleostei: Siluriformes), a problematic group. In: Peters G & R Hutterer (eds) Vertebrates in the tropics: 395-403. Museum Alexander Koenig, Bonn, Germany.
CAMPOS H (1985) Distribution of the fishes in the Andean rivers in the south of Chile. Archives Hydrobiologie 102: 169-191.
DUMAS PC (1964) Species-pair allopatry in the genera Rana and Phrynosoma. Ecology 45: 178-181.
DYER B (2000) Systematic review and biogeography of the freshwater fishes of Chile. Estudios Oceanológicos (Chile) 19: 77-98.
EIGENMANN C (1918) The Pygidiidae, a family of South American catfishes. Memoirs of the Carnegie Museum 7: 259-398.
EIGENMANN C (1927) The fresh-water fishes of Chile. Memoirs of National Academy Sciences, Washington (USA) 22: 1-63.
FERNÁNDEZ HR, F ROMERO, M PERALTA & L GROSSO (2001) La diversidad de zoobentos en ríos de montañas del noroeste de Argentina: comparación entre seis ríos. Ecología Austral (Argentina) 11: 9-16.
FISHER RA (1936) The use of multiple measurements in taxonomic problems. Annals of Eugenics 7: 179188.
HABIT E, P VICTORIANO & H CAMPOS (2005) Ecología trófica y aspectos reproductivos de Trichomycterus areolatus (Pisces, Trichomycteridae) en ambientes lóticos artificiales. Revista de Biología Tropical 53: 195-210.
HUTCHINSON GE (1965) The ecological theatre and evolutionary play. Yale University Press, New Haven, Connecticut, USA. 139 pp.
KAHL U & RJ RADKE (2006) Habitat and food resource use of perch and roach in a deep mesotrophic reservoir: enough space to avoid competition? Ecology of Freshwater Fish 15: 48-56.
KARPOUZI VS & KI STERGIOU (2003) The relationships between mouth size and shape and body length for 18 species of marine fishes and their trophic implications. Journal of Fish Biology 62: 1353-1365.
KEELEY ER & JWA GRANT (1997) Allometry of diet selectivity in juvenile Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 54: 1894-1902.
KREBS C (1999) Ecological methodology. Second edition. Benjamin/Cummings, Addison Wesley, Menlo Park, California, USA. 620 pp.
LOPRETTO E & G TELL (1995) Ecosistemas de aguas continentales. Ediciones Sur, La Plata, Argentina. 1.401 pp.
LOSOS JB, M LEAL, RE GLOR, K DE QUEIROZ, PE HERTZ, L RODRÍGUEZ- SCHETTINO, A CHAMIZO-LARA, TR JACKMAN & A LARSON (2003) Niche lability in the evolution of a Caribbean lizard community. Nature 424: 542-545.
MANLY B (1997) Randomization, bootstrap and Monte Carlo methods in biology. Second edition. CRC Press, Boca Roca, Florida, USA. 399 pp.
MERRITT RW & KW CUMMINS (1978) An Introduction to the Aquatic Insects of North America. Kendall/ Hunt Publishing. Iowa, USA. 441 pp.
NIEMEYER H & P CERECEDA (1984) Hidrografía. Geografía de Chile. Tomo VIII. Instituto Geográfico Militar, Santiago, Chile. 320 pp.
NILSSON NA (1967) Interactive segregation between fish species. In: Gerking SD (ed) The biological basis for fresh water fish production: 295-313. Blackwell Scientific Publications, Oxford, United Kingdom.
PARDO R, S SCOTT & I VILA (2005) Análisis de formas en especies chilenas del género Trichomycterus (Osteichthyes: Siluriformes) utilizando morfometría geométrica. Gayana (Chile) 69: 180-183.
POUILLY M & G MIRANDA (2003) Morphology and reproduction of the cavefish Trichomycterus chaberti and the related epigean Trichomycterus cf. barbouri. Journal of Fish Biology 63: 490-505.
RUIZ VH, MT LOPEZ, HI MOYANO & M MAN (1993) Ictiología del alto Biobío: aspectos taxonómicos, alimentarios, reproductivos y ecológicos una discusión sobre la hoya. Gayana Zoología (Chile) 57: 77-88.
SABANDO MC (2004) Análisis funcional de las comunidades bentónicas en un tramo altitudinal de Río Clarillo (Pirque). Memoria para optar al título de Licenciado en Educación en Biología y Pedagogía en Biología y Ciencias Naturales. Universidad de Ciencias de la Educación, Santiago, Chile. 81 pp.
SCHOENER TW (1974) Resource partitioning in ecological communities. Science 185: 27-39.
VILA I, L FUENTES & M CONTRERAS (1999) Peces límnicos de Chile. Boletín del Museo Nacional de Historia Natural (Chile) 48: 61-75.
VILA I, & R PARDO (2006) Peces límnicos. In: Biodiversidad de Chile: patrimonio y desafíos 306-311. Comisión Nacional del Medio Ambiente. Gobierno de Chile. Ocho Libros Editores Ltda., Santiago, Chile.
WALLACE RK (1981) An assessment of diet-overlap indexes. Transactions of the American Fisheries Society 110: 72-76.
WERNER EE & DJ HALL (1976) Niche shifts in sunfishes: experimental evidence and significance. Science 191: 404-406.
WERNER EE & DJ HALL (1977) Competition and habitat shift in two sunfishes (Centrarchidae). Ecology 58:869-876. ZAR J (1996) Biostatistical analysis. Third edition. Prentice-Hall, Englewood Cliffs, New Jersey, USA. 660 pp.
ZARET TM & TR PAINE (1973) Species introduction in a tropical lake. Science 182: 449-455.
Associate Editor: Brian Dyer
Received October 4, 2005; accepted May 4, 2007