Ecomorphological patterns of the lapilli of Paranoplatense Siluriforms (South America)

Fisheries Research 102 (2010) 160–165

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Ecomorphological patterns of the lapilli of Paranoplatense Siluriforms (South America) Alejandra V. Volpedo a,b,c,∗ , Daniela V. Fuchs b,d a

Centro de Estudios Transdisciplinarios del Agua (CETA), Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Av. Chorroarín 280, CP 1427 Buenos Aires, Argentina Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Universitaria, CP 1428 Buenos Aires, Argentina c CONICET, Argentina d División Zoología Vertebrados, Museo de La Plata, Paseo del Bosque s/n, CP 1900 La Plata, Argentina b

a r t i c l e

i n f o

Article history: Received 6 July 2009 Received in revised form 19 November 2009 Accepted 23 November 2009 Keywords: Paranoplatense fish Utricular otolith Ecomorphology Morphometry South America

a b s t r a c t The morphology and morphometry of lapillus otoliths were studied in bottom frequenters, intermediate and benthonic fishes. The shape, margins and type of sulcus of 3 groups of otoliths from 19 species were analyzed: group 1 (bottom frequenters, 11 spp), group 2 (intermediate, 5 spp) and group 3 (benthonic, 3 spp). The indices EL (maximum width of the lapillus (WOL)/maximum length of the lapillus (LOL) %) and S (sulcus area/otolith area %) were calculated for each species. The lapilli of bottom frequenters and intermediate groups showed, in their ventral face, similar morphological features, high shape variability (oblong shape, elongated shape and quadrangular shape) and a sulcus surface that represents 16–34% of otolith surface. The lapilli of the benthonic group are globosal or rounded with a sulcus surface that represents less than 12% of otolith surface. Statistical analyses showed significant differences in the EL and S indices between the benthonic group and the other two groups, but there were no differences between the otoliths of the bottom frequenters and intermediate groups. EL and S values could be used to characterize the lapilli of the paranoplatense fish and could be considered a useful tool for fish ecology studies. Published by Elsevier B.V.

1. Introduction Neotropical fishes richness includes 4475 valid species (representing 71 families). The order Siluriforms contributes with 1648 species (15 families) (Reis et al., 2003). The Paranoplatense zoogeographical province is the widest ichthylogical region in Argentina, occupying approximately the 75% of the country and it has the largest biodiversity (Menni, 2004; López and Miquelarena, 2005; López et al., 2008). In this region we find 83.5% of the Siluriform species from Argentina (162 out of 194) (López and Miquelarena, 2005; Liotta, 2006). Siluriforms, are predated by ichthiophagous birds and water mammals, such as Lutra longicaudis (Olfers, 1818) (vulnerable species) and Pteronura brasiliensis (Gmelin, 1788) (endangered species) (Parera, 1992, 1996).

∗ Corresponding author at: Centro de Estudios Transdisciplinarios del Agua (CETA), Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Av. Chorroarín 280, CP 1427 Buenos Aires, Argentina. Tel.: +54 11 4524 8423; fax: +54 11 4524 8499. E-mail address: [email protected] (A.V. Volpedo). 0165-7836/$ – see front matter. Published by Elsevier B.V. doi:10.1016/j.fishres.2009.11.007

The fish inner ear comprises three otolith systems with specific hair orientation patterns. These are semicircular canals (anterior, posterior and horizontal) and three otolithic end organs (saccule, lagena and utricle), which have related otoliths: sagittae, asterisci and lapilli. In particular in ostariophysian groups the lapilli is usually larger than the other two and appear to be more engaged in the sense of posture (Schellart and Popper, 1992; Assis, 2005) and have a very homogeneous structure among all vertebrates (Cordier and Dalcq, 1954; Popper and Coombs, 1982). Siluriform fish use the water column in different forms and these uses determine different ecological groups. These fish species have developed a wide range of feeding strategies, which allow them to utilize food resources in a variety of habitats (Abes et al., 2001; Fugi et al., 2001; Rossi, 2001; Viana et al., 2006; Fagundes et al., 2008). Otoliths allow the analysis of different aspects of fish biology and their environment (Morales-Nin, 1987; Gauldie, 1993; Torres et al., 2000; Volpedo and Echeverría, 2003). Environmental factors (Aguirre and Lombarte, 1999; Torres et al., 2000; Gauldie and Crampton, 2002; Volpedo and Echeverría, 2003; Volpedo et al., 2008), feeding habits (Nonogaki et al., 2007), ontogeny (Volpedo and Echeverría, 1999; Tombari et al., 2005), physiology, such as the hearing capabilities associated with specialization in acoustic communication (Popper and Fay, 1993; Paxton, 2000; Lombarte

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and Cruz, 2007), and phylogeny (Assis, 2003, 2005; Nolf and Tyler, 2006), could affect the morphology, the morphometry and the microstructure of otoliths (Campana et al., 1995; Volpedo and Fernández Cirelli, 2006; Volpedo et al., 2007). The aim of the present paper is to analyze whether the morphological features of Siluriform fish lapilli could be associated with water column use. 2. Materials and methods A total 462 lapilli were sampled from 19 fish species (Table 1) obtained from commercial and sport fisheries from paranoplatense rivers and lakes (Río de La Plata, Río Paraná, RíoUruguay, Río Salado, Río Sarmiento, Río Luján, Laguna de Chascomús, Laguna de Lobos, Laguna de Monte, Punta Lara, Santa Fé (Playa Municipal, Boca Cerrada) y Entre Ríos) (Fig. 1). Fish were assigned to three ecological groups, suggested by Ringuelet et al. (1967): (1) bottom frequenters (inhabit vegetated environments, soft bottom. Usually present well-developed barbels, and a forked caudal fin. They are omnivorous, they feed mainly on molluscs, crustaceans, insects, small fishes and organic matter present in mud bottom. The big catfishes are speedy swimmers while remaining fish of this group are less speed), (2) intermediate (inhabit vegetated environments, dark waters. Their feeding regime is omnivorous, including carrion; they also feed on fruits, insect larvae and aquatic insect adults. They swim to surface to breathe atmospheric air) and (3) benthonic (inhabit slow flowing water courses, with muddy and rocky bottoms, but some inhabit clear and fast water streams. Their body is entirely cover by bony plates, the ventral surface of the body is plane and the dorsal is curved or angled, so the body section is triangled. They have short barbels and an inferior mouth surrounded by wide lips. The feeding

Fig. 1. Map showing the sampling localities. 1 – Laguna de Lobos, 2 – Laguna de Monte, 3 – Laguna de Chascomús.

regime is detritivore-iliophagus. They usually rested on the substrate clinging by their mouth sucker). The criteria used to separate the fish into these groups were taken from literature: trophic habits, swimming style and habitat (Ringuelet et al., 1967; Ringuelet, 1975; Goulding, 1981; Cordiviola de Yuan and Pignalberi de Hassan, 1985; Burgess, 1989; Mills and Vevers, 1989; COMIP, 1994; Boujard et al., 1997; Le Bail et al., 2000; Hahn et al., 2002; Ferraris, 2003a,b;

Table 1 List of the studied species, including sizes, sampling locations and ecotype. Family/species

SL

Sampling locations

Ecological group

Author

6 1

130–440 108

a, b c

Bf Bf

1, 2, 5, 11 1, 2, 5, 11

2 17

60–110 29–63

d d, e

I I

1, 2, 14, 16 8, 14, 16

9 2

294–370 143–160

a, f f

I Bf

1, 2, 15, 16 1, 2, 15

Heptapteridae Pimelodella gracilis (Valenciennes, 1836) Pimelodella laticeps Eigenmann, 1917 Rhamdia quelen (Valenciennes, 1836)

13 53 43

86–130 23–107 94–320

f e. e, g, h, i

I I Bf

6, 7 18, 19 1, 2, 18

Loricariidae Hypostomus commersoni Valenciennes, 1836 Loricariichthys anus (Valenciennes, 1836) Paraloricaria vetula (Valenciennes, 1836)

12 41 7

195–330 89–445 320–422

b, e, k a, e, h a, l

B B B

1, 2, 12 1, 2, 12 1, 2, 12

9 28 127 49 4 21 18

76–240 105–970 51–240 38–345 105–150 44–235 24–142

a, c, m a, c, f, m, n a, e, g, m a, c, g, j, m a, m a, b, o b, c

Bf Bf (fast)a Bf Bf Bf Bf Bf (fast)a

1, 2, 4, 10, 13 1, 2, 3, 10, 13 1, 2, 9, 10, 13 1, 2, 3, 10, 13 1, 2, 19 1, 2, 4, 13 1, 2, 10, 13

Auchenipteridae Ageneiosus inermis (Linnaeus, 1766) Auchenipterus nuchalis** (Spix and Agassiz, 1829) Callichthyidae Callichthys callichthys (Linnaeus, 1758) Corydoras paleatus (Jenyns, 1842) Doradidae Pterodoras granulosus (Valenciennes, 1821) Rhinodoras dorbignyi (Kner, 1855)

Pimelodidae Iheringichthys labrosus Lütken, 1874 Luciopimelodus pati (Valenciennes, 1836) Parapimelodus valenciennis (Lütken, 1874) Pimelodus albicans (Valenciennes, 1840) Pimelodus argenteus Perugia, 1891 Pimelodus maculatus Lacepède, 1803 Sorubim lima (Bloch & Schneider, 1801)

N

** ED not shown because it is only one fish. Sampling locations: (a) Río de la Plata, (b) Punta Lara, (c) Río Paraná, (d) Provincia de Buenos Aires, (e) Laguna de Chascomús, (f) Río Uruguay, (g) Río Salado, (h) Laguna de Lobos, (i) Laguna de Monte, (j) Punta Lara, (k) Entre Ríos, (l) Playa Municipal (Santa Fe), (m) Río Sarmiento, (n) Boca Cerrada (Santa Fe), (o) Río Luján. (1) Ringuelet et al. (1967), (2) Ringuelet (1975) (3) Goulding (1981), (4) Cordiviola de Yuan and Pignalberi de Hassan (1985), (5) Burgess (1989), (6) Mills and Vevers (1989), (7) COMIP (1994), (8) Boujard et al. (1997), (9) Le Bail et al. (2000), (10) Hahn et al. (2002), (11) Ferraris (2003a), (12) Ferraris (2003b), (13) Lundberg and Littmann (2003), (14) Reis (2003), (15) Sabaj and Ferraris (2003), (16) Menni (2004), (17) Andrade and Braga (2005), (18) López et al. (2005), (19) Rosso (2006). SL: standard length (mm); SL: minimum and maximum values. (B) benthonic group, (Bf) bottom frequenters group, (I) intermediate group. a (fast) also found in fast in fast stream rivers.

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Lundberg and Littmann, 2003; Reis, 2003; Sabaj and Ferraris, 2003; Menni, 2004; Andrade and Braga, 2005; López et al., 2005; Rosso, 2006). The standard length (SL) of the fish was measured in millimeter. The lapilli were compared among groups 1–3. Group 1 included: Ageneiosus inermis (N = 6), Auchenipterus nuchalis (N = 1), Rhinodoras dorbignyi (N = 2), Rhamdia quelen (N = 43), Iheringichthys labrosus (N = 9), Luciopimelodus pati (N = 28), Parapimelodus valenciennis (N = 127), Pimelodus albicans (N = 49), Pimelodus argenteus (N = 4), Pimelodus maculatus (N = 21) and Sorubim lima (N = 18). Group 2 included: Callichthys callichthys (N = 2), Corydoras paleatus (N = 17), Pterodoras granulosus (N = 9), Pimelodella gracilis (N = 13) and Pimelodella laticeps (N = 53). Group 3 included: Hypostomus commersoni (N = 12), Loricariichthys anus (N = 41) and Paraloricaria vetula (N = 7). The lapilli were measured according to the methodology described by Volpedo and Echeverría (2000) and the morphological features of lapilli proposed by Mollo (1981) and Assis (2005). The following measurements were recorded from both lapilli (left and right): WOL (maximum width of the lapillus), LOL (maximum length of the lapillus), in mm with an error less than 0.01 mm, SS (sulcus area), OS (otolith area) in mm2 , with an error less than 0.01 mm2 (Fig. 2). There were no significant differences among width and length of right and left lapilli (t-test, P > 0.05). Four percentual indices were calculated, A, L, EL and S. The value of A (A = WOL/SL %) expresses the relative otolith width in relation to the SL and the value of L (L = LOL/SL %) expresses the relative otolith width in relation to the SL. The value of EL (EL = WOL/LOL %) expresses the tendency of the shape of the lapilli (circular or elongate), in the case of the circular otoliths the EL value is close to 80%, in the other hand the elongate ones has an EL value near of 50%. The value of S (S = sulcus area (SS)/otolith area (OS) %) expresses the percentage of the otolith surface that is occupied by the sulcus. This index was described by Gauldie (1988). The otolith and sulcus areas were measured using a digital image processing system, maximum width and length were measured with a digital caliber.

Fig. 2. Measurements recorded from the lapilli: WOL (maximum width of the lapillus), LOL (maximum length of the lapillus), in mm, SS (sulcus area), OS (otolith area) in mm2 . The scheme represents a right otolith, in view of the ventral face; A (anterior region), P (posterior region), L (lateral margin), M (medial margin).

The statistical analyses were based on the mean values of EL and S calculated for each species (Table 2). The data were transformed with logarithms. The mean values of E and S for fish groups were compared using analysis of the covariance (ANCOVA) with the standard length as covariable (Sokal and Rohlf, 1995) and multiple comparisons between fish groups (Zar, 1999). The software used in the statistical analyses was Statistica 6 (Statsoft). 3. Results The lapilli studied, showed high morphological and morphometric variability.

Table 2 A, L, EL and S indices of lapilli otoliths from the studied species. Family species

SL (mm)

A % X ± SD

L % X ± SD

EL % X ± SD

SS (mm2 ) X ± SD

OS (mm2 ) X ± SD

S % X ± SD

Auchenipteridae Ageneiosus inermis Auchenipterus nuchalisa

130–440 108

1 ± 0.13 2

1 ± 0.19 1

69 ± 4 65

0.50 ± 0.10 0.50

1.86 ± 0.65 2.52

28 ± 4 20

Callichthyidae Callichthys callichthys Corydoras paleatus

60–110 29–63

1 ± 0.11 2 ± 0.24

2 ± 0.19 3 ± 0.3

68 ± 1 64 ± 5

0.41 ± 0.21 0.26 ± 0.07

1.32 ± 0.68 0.84 ± 0.27

31 ± 0.25 34 ± 17

Doradidae Pterodoras granulosus Rhinodoras dorbignyi

294–370 143–160

1 ± 0.07 1 ± 0.10

1 ± 0.11 1 ± 0.11

55 ± 4 53 ± 4

1.60 ± 0.59 0.48 ± 0.12

7.1 ± 1.34 1.8 ± 0.13

22 ± 5 27 ± 5

86–130 23–107 94–320

2 ± 0.16 2 ± 0.21 1 ± 0.32

2 ± 0.20 3 ± 0.36 2±1

67 ± 6 73 ± 6 62 ± 3

0.72 ± 0.24 0.71 ± 0.42 2.32 ± 1.19

3.77 ± 1.14 4.35 ± 2.27 8.15 ± 3.68

19 ± 2 16 ± 3 27 ± 5

Heptapteridae Pimelodella gracilis Pimelodella laticeps Rhamdia quelen Loricariidae Hypostomus commersoni Loricariichthys anus Paraloricaria vetula

195–330 89–445 320–422

1 ± 0.08 1 ± 0.12 0.50 ± 0.04

1 ± 0.14 1 ± 0.12 1 ± 0.05

80 ± 4 83 ± 8 87 ± 7

0.21 ± 0.04 0.28 ± 0.11 0.24 ± 0.06

2.02 ± 0.70 3.47 ± 0.72 3.66 ± 0.45

11 ± 3 8±2 7±1

Pimelodidae Iheringichthys labrosus Luciopimelodus pati Parapimelodus valenciennis Pimelodus albicans Pimelodus argenteus Pimelodus maculatus Sorubim lima

76–240 105–970 51–240 38–345 105–150 44–235 24–142

1 ± 0.16 1 ± 0.48 1 ± 0.16 1 ± 0.17 1 ± 0.16 1 ± 0.21 2±2

1 ± 0.21 1 ± 0.50 2 ± 0.20 2 ± 0.19 2 ± 0.17 2 ± 0.21 2±3

69 ± 7 79 ± 7 64 ± 6 69 ± 7 75 ± 3 76 ± 6 65 ± 4

0.79 ± 0.44 2.24 ± 2.17 0.98 ± 0.58 0.92 ± 0.77 0.65 ± 0.25 1.10 ± 0.32 0.78 ± 0.40

2.85 ± 1.54 7.95 ± 7.35 3.83 ± 2.01 3.32 ± 2.98 2.27 ± 0.98 4.21 ± 1.60 2.47 ± 1.13

27 ± 3 29 ± 4 25 ± 4 29 ± 3 29 ± 2 27 ± 2 31 ± 3

SL: fish standard length; A: WOL/LS %; L: LOL/SL %; EL: WOL/LOL %; OS: otolith surface; S: SS/OS %; SS: sulcus surface; X: mean value; SD: standard deviation. a ED not shown because it is only one fish.

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Fig. 3. Ventral face of right lapilli of benthonic fishes. (a) Hypostomus commersoni, SL = 297 mm. (b) Loricariichthys anus, SL = 382 mm. (c) Paraloricaria vetula, SL = 415 mm. Scale bar: 1 mm. All specimens with lateral margin to the left of the page and anterior region to the top.

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The lapilli of bottom frequenter and intermediate groups showed similar morphological features in their ventral face (Figs. 4 and 5), such as high shape variability (oblong shape, elongated shape and quadrangular shape). The lapilli of benthonic group are globosal or rounded. In the benthonic group (group 3) lapilli shape was variable, being rounded in H. commersoni and L. anus and globosal in P. vetula (Fig. 3). In bottom frequenters (group 1) the lapilli showed three different shapes: quadrangular in A. inermis, R. quelen, P. albicans and P. argenteus; oblong in A. nuchalis, I. labrosus, L. pati, P. valenciennis, P. maculatus and S. lima and elongated in R. dorbignyi (Fig. 4). The intermediate group (group 2) showed variable shapes, oblong in C. callichthys and C. paleatus, elongated in Pterodoras granulosus, quadrangular in P. gracilis and rounded in P. laticeps (Fig. 5). Group 1 showed values of 53–79% (67 ± 8) in EL (WOL/LOL %) index, group 2 showed values between 55 and 73% (69 ± 8), and the species belonging to group 3 have the largest values among 80–87% (83 ± 8) (Table 2). Concerning the S index (SS/OS) group 1 showed values in the range 25–31% (28 ± 4), group 2 between 16 and 34% (25 ± 12) and group 3 showed the smallest values, 7–11% (9 ± 3) (Table 2). The statistical analysis (ANCOVA) showed significant differences among the EL and S values for the lapilli of benthonic fish, bottom frequenters fish and intermediate fish (EL index: F(2, 458) = 100,30, P < 0.05; S index: F(2, 92) = 40,6012, P < 0.05). The multiple comparisons among groups showed that the EL and S values between groups 1 and 2 did not show significant dif-

Fig. 4. Ventral face of right lapilli of bottom frequenter fishes. (a) Ageneiosus inermis, SL = 309 mm. (b) Auchenipterus nuchalis, SL = 108 mm. (c) Rhinodoras dorbignyi, SL = 160 mm. (d) Rhamdia quelen, SL = 300 mm. (e) Iheringichthys labrosus, SL = 240 mm. (f) Luciopimelodus pati, SL = 970 mm. (g) Parapimelodus valenciennis, SL = 227 mm. (h) Pimelodus albicans, SL = 270 mm. (i) Pimelodus argenteus, SL = 150 mm. (j) Pimelodus maculatus, SL = 235 mm. (k) Sorubim lima, SL = 300 mm. Scale bar: 1 mm. All specimens with lateral margin to the left of the page and anterior region to the top.

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Fig. 5. Ventral face of right lapilli of intermediate fishes. (a) Callichthys callichthys, SL = 110 mm. (b) Corydoras paleatus, SL = 50 mm. (c) Pterodoras granulosus, SL = 370 mm. (d) Pimelodella gracilis, SL = 86 mm. (e) Pimelodella laticeps, SL = 95 mm. Scale bar: 1 mm. All specimens with lateral margin to the left of the page and anterior region to the top.

ferences (EL: P = 0.1329; S: P = 0.2834), while the EL and S values indicate that group 3 presents significant differences in relation to the other groups (P < 0.0001). 4. Discussion In the studied species the lapilli width and length reach between 0.5–2% and 1–3% of standard fish length, respectively. In other species from the same order, such as Oxydoras kneri Bleeker, 1862, Heptapterus mustelinus (Valenciennes, 1835), Rhamdella jenynsi (Günther, 1864), Zungaro zungaro (Humboldt, 1821) (=Pseudopimelodus zungaro zungaro in Martínez and Monasterio de Gonzo, 1991), Megalonema platanum (Günther, 1880), Pseudoplatystoma corruscans (Agassiz, 1829), Trychomycterus borelli (Boulenger, 1897), Hoplosternum littorale (Hancock, 1829), Loricaria simillima (Regan, 1914) and Hypostomus cordovae (Günther, 1880) studied by Martínez and Monasterio de Gonzo (1991) similar results were found for these two indices. This could be attributed not only to the phylogenetic relations in the order, but also to adaptations to the environmental conditions of the water courses the fishes inhabit. The lapilli of Paranoplatense Siluriforms showed different morphological patterns related to environment. These differences are show in lapilli shape and in ventral face topography (Figs. 3–5). Benthonic fish showed rounded or globosal shape otoliths, so in these species the axis of deposition of calcium carbonate is lateromedial, different from the other groups where it is antero-posterior. This group does not show cisure, the sulcus area represent 12% to otolith area, and present variable sulcus shape. Bottom frequenters and intermediate fish show variable lapillus shape, rounded, quadrangular, oblongal and elongated. The presence of cisure is variable, the sulcus area represent 16–34% to otolith area, and present variable sulcus shape.

The present results support the hypothesis that the lapilli morphologic features in paranoplatense fish could be associated, to water column uses (ecomorphological type) among other factors. At least differences were found between bottom fish and the other groups; further studies might lead to a separation between the other two groups here proposed, but it has to be also considered that the phylogeny of the group might explain the lack of differences among them. If the function of the lapilli is related to equilibrium, the differences in its shape could correspond to the ecotypes, depending on the need of the fish to maintain the spatial position in the water column (Lombarte and Popper, 2004). The EL and S indices can be used to discriminate between lapilli of benthonic and the other fish groups. In future studies morphologic features could be related to physiological features as specialization in acoustic communication in deep waters in order, for example, to compensate for the reduction of light with depth (Popper and Fay, 1993; Lombarte and Cruz, 2007). Acknowledgements The authors would like to thank the Universidad de Buenos Aires (UBACyT X 504), Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) and CONICET for the financial support. We also thank Dr. C. Assis and the anonymous referee who contributed to the final version of the present report. References Abes, S.S., Agostinho, A.A., Okada, E.K., Gomes, L.C., 2001. Diet of Iheringichthys labrosus (Pimelodidae, Siluriforms) in the Itaipu Reservoir, Paraná River, BrazilParaguay. Braz. Arch. Biol. Technol. 44 (1), 101–105. Aguirre, H., Lombarte, A., 1999. Ecomorphologic comparisons of sagittae in Mullus barbatus and M. surmuletus. J. Fish Biol. 55, 105–114.

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