Buoyancy of sub-Antarctic notothenioids including the sister lineage of all other notothenioids (Bovichtidae)

Daniel A. Fernndez, Santiago G. Ceballos, Gabriela Malanga, Claudia C. Boy & Fabin A. Vanella
Polar Biology ISSN 0722-4060 Polar Biol DOI 10.1007/ s00300-011-1037-7

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Polar Biol DOI 10.1007/s00300-011-1037-7

ORIGINAL PAPER

Buoyancy of sub-Antarctic notothenioids including the sister lineage of all other notothenioids (Bovichtidae)
ndez Santiago G. Ceballos Daniel A. Ferna Gabriela Malanga Claudia C. Boy n A. Vanella Fabia

Received: 4 February 2011 / Revised: 26 April 2011 / Accepted: 17 May 2011 Springer-Verlag 2011

Abstract The radiation of notothenioid shes (Perciformes) in Antarctic waters was likely the result of an absence of competition in the isolated Antarctic waters and key traits such as the production of antifreeze glycoprotein and buoyancy modications. Although notothenioids lack a swim bladder, the buoyancy of Antarctic species, ranging from neutrally buoyant to relatively heavy, corresponds to diverse life styles. The buoyancy of South American notothenioids has not been studied. Static buoyancy was measured in adult notothenioids (n = 263, from six species of the sub-order Notothenioidei, families Bovichtidae, Eleginopidae, Nototheniidae, and Harpagiferidae) from the Beagle Channel. Measurements were expressed as percentage buoyancy (%B). Buoyancy ranged from 3.88 to 6.96% (median, 4.06.7%), and therefore, all species could be considered benthic consistent with previous studies that found that neutral buoyancy in notothenioids is rare. Harpagifer bispinis, Patagonotothen cornucola, and Cottoperca gobio were signicantly less buoyant than Paranotothenia magellanica. The buoyancy values of most species were concordant with known habitat preferences. These data, especially the data of C. gobio (sister lineage of all other nototehnioids) and E. maclovinus (sister lineage of the Antarctic clade of notothenioids), could be useful for

understanding the diversication of this feature during the notothenioid radiation. Keywords Beagle channel Buoyancy Fish Notothenioids Sub-Antarctic region

Introduction Buoyancy of shes relies on both a passive component, related to body composition (static lift), and an active component, related to the activity of the species (dynamic lift). Static lift is the difference between the weight of a sh in air and its weight in water and varies according to the species life style (e.g., pelagic, benthic, and semi-pelagic). Neutrally buoyant sh have no weight to support in water and, therefore, do not devote energy from forward locomotion to provide hydrodynamic lift. Thus, neutral buoyancy can be seen as an adaptive advantage for sh living in the water column. To facilitate buoyancy, most teleost sh have a special organ called the swim bladder (also called gas bladder), which accounts for *5% of the shs total volume (Marshall 1979). Because volume is approximately equal to weight, a marine sh that lacks a swim bladder must support *5% of its weight in air when it is in the water column. However, in environments where buoyancy regulation may be unnecessary or even disadvantageous, such as benthic habitats (Steen 1970) or deep-sea environments (Marshall 1960), the absence of a swim bladder has been considered adaptive. As a result, the swim bladder has been lost independently in 425 families of living teleosts that inhabit benthic or deep-sea environments (McCune and Carlson 2004). Notothenioids (Perciformes) are the most abundant and species-rich teleost clade in the Southern Ocean. The ancestral notothenioids, as well as extant species, lack a

ndez (&) S. G. Ceballos D. A. Ferna C. C. Boy F. A. Vanella cas Centro Austral de Investigaciones Cient (CADIC-CONICET), 200 Bernardo Houssay, V9410CAB Ushuaia, Tierra del Fuego, Argentina e-mail: dfernandez@cadic-conicet.gob.ar G. Malanga Physical Chemistry-PRALIB, School of Pharmacy and Biochemistry, University of Buenos Aires, Junin 956, 1113 Buenos Aires, Argentina

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swim bladder and are primarily a benthic group. Nevertheless, some Antarctic notothenioids have buoyancy modications that have allowed them to expand their range in the water column during a radiation they underwent in Antarctic waters about 14 million years ago (Mya) (see Eastman and De Vries 1982, 1985; Eastman 1993; Eastman and Sidell 2002; Near et al. 2007). For example, pelagic notothenioid species, such as Dissostichus mawsoni and Pleuragramma antarcticum, have buoyancy values of 0.01% wtwater/wtair and 0.57% wtwater/wtair, respectively. The diversication in Antarctic waters, which resulted in notothenioids lling ecological niches occupied by taxonomically diverse sh in temperate waters, was possible, given the reduced competition and isolation of Antarctica where they evolved (Eastman 1993; Clarke and Johnston 1996). At least 28 notothenioid species are found outside the Antarctic Convergence with 18 found in the Beagle pez et al. 1996; Eastman 2005). Eleven of Channel (Lo these species belong to early diverging families that evolved outside the Antarctic, while the rest (or their ancestors) belong to families that have re-colonized subAntarctic waters from Antarctica. Most are in the family Nototheniidae, but there are also species from Harpagiferidae (Harpagifer bispinis) and Channichthydae (Cham pez et al. 1996; Eastman 2005). The psocephalus esox) (Lo sub-Antarctic notothenioids evolved in the presence of sh groups that are absent or uncommon in Antarctic waters. Therefore, these lineages likely experienced more competition over their evolutionary history compared with the Antarctic notothenioids, limiting the occupation of niches distinct from the original benthic one. We hypothesized that some sub-Antarctic notothenioids, like some Antarctic species, would exhibit buoyancy that allows them to occupy a wide range of habitats from the ancestral benthic to pelagic. To gain insight into the role of buoyancy in niche diversication of sub-Antarctic notothenioids, we measured the static lift of six species belonging to four families, two primarily non-Antarctic (only one Antarctic species) and two primarily Antarctic. This analysis of buoyancy should reveal the degree of ecological diversication in sub-Antarctic notothenioids and the importance of competition in niche occupation. Additionally, it could provide information about vertical segregation in the water column, swimming behavior, and potential interactions of the sh with other components of the ecosystems (Eastman 1993).

Bridges Islands and Lapataia Bay) using trammel nets, gill nets, traps, and by hand (Fig. 1). Two hundred and sixty-three sh from six species were included in the study: Cottoperca gobio (n = 11), Eleginops maclovinus (n = 40), Paranotothenia magellanica (n = 98), Patagonotothen tessellata (n = 63), Patagonotothen tessellata gravid (n = 25), Patagonotothen cornucola (n = 14), and H. bispinis (n = 12). Buoyancy Buoyancy was measured in heavily anaesthetized sh or sh that had recently died in the nets. Using an Ohaus Adventurer scale with a capacity of 2,100 g and accuracy of 0.01 g, individuals were weighed in air and in seawater at the same temperature when they were caught. To measure the weight in seawater, a hook on the scale was attached to a nylon line (0.30 mm) with a hook on the other end that was inserted in the operculum. Air bubbles were removed manually from the oral and branchial cavities, and the weight was recorded when the scale display stabilized. Fish were not sexed since they were used for other

Materials and methods Fish During the summers of 2007 and 2008, sh were captured in three locations in the Beagle Channel (Ushuaia Bay,
Fig. 1 Notothenioids were collected in the Beagle Channel waters located south of Isla Grande de Tierra del Fuego, southern South America. Sampling sites were Ushuaia Bay, Bridges Island, and Lapataia Bay

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experiments afterward. Nevertheless, gravid females of just one species (P. tessellata) were available. They were used in this study in order to compare non-gravid and gravid sh. Buoyancy values were expressed as percentage buoyancy. For example, a sh with a buoyancy of 2% had a weight in seawater that was 2% of its weight in air, indicating it was negatively buoyant. %B Wwater =Wair 102 Skeleton analysis To determine the possible sources of variation in static buoyancy, we measured the skeletal weight and the ash content of the skeleton in most of the species studied. Fish were boiled in water until the esh began to fall off the bones. Bones were separated from the esh with tweezers. To remove any remaining esh, the bones were digested with commercial enzymatic soap powder for several hours until they look clean (rinsing them with water every 2 h). Clean bones were dried in an oven at 60C until constant weight was obtained. Using this constant weight as the skeletal weight, the percent of skeletal weight from total weight was calculated. Skeletons were then burned in an oven at 450C for 36 h. The ashes were weighed to calculate the skeletal ash content. We also calculated the ashed skeleton values as follows: % ashedskeleton skeletalashcontent=total weight 102 Proximate muscle composition The water content of the muscles was measured after drying the esh in an oven at 60C until constant weight was obtained. Total protein content was measured following hydrolysis with 0.5 N NaOH, using 1 mg ml-1 BSA as a standard following the method of Lowry et al. (1951). Glycogen was extracted from tissues by boiling with 30% (p/v) KOH and was determined as total carbohydrates using the Anthrone reagent (Seifter and Dayton 1950; Carroll et al. 1956). Glycogen was quantied after precipitation with 99% (v/v) ethanol, using a standard 20 lg ml-1 glucose solution. Lipids were measured by a gravimetric method (Bligh and Dyer 1959). The results were expressed as mg biochemical component per gram (g) of tissue ash-free dry weight (AFDW). Ash was measured using the methodology already explained for the skeletons. Statistical analysis Due to the heteroscedasticity of the data buoyancy, skeletal weight proportion, ash content, water content, and proximate composition of muscles were analyzed using

KruskalWallis nonparametric ANOVAs. Dunns post hoc tests were performed for all pairs of species. Regression analysis of buoyancy versus total length (TL) and total weight (TW) were also performed for the more abundant species (P. magellanica, P. tessellata, and E. maclovinus).

Results The buoyancy values (mean and median), length and weight ranges, and ecological characteristics of all species are shown in Table 1. Average buoyancy ranged from 3.88 to 6.96% (Fig. 2). Notothenioid species could be ordered from the most buoyant to the least buoyant as follows: P. magellanica [ P. tessellata [ E. maclovinus [ C. gobio [ P. cornucola [ H. bispinis. Nonparametric ANOVA analysis (KruskalWallis) showed highly signicant differences in buoyancy values among species (P \ 0.0001, KW = 70.266) due to the signicant differences between the most buoyant P. magellanica and the less-buoyant P. tessellata, E. maclovinus, C. gobio, P. cornucola, and H. bispinis (Dunns post hoc test). Gravid P. tessellata were more buoyant than non-gravid specimens (Fig. 2), but the difference was not signicant. The least buoyant species (P. cornucola and H. bispinis) were signicantly heavier than gravid P. tessellata (Table 2). In P. tessellata and P. magellanica, regression analysis of buoyancy revealed that buoyancy was not associated with length or weight. However, in E. maclovinus, bigger sh were signicantly less buoyant than smaller sh (r2 = 0.37; P \ 0.0001 for TL and r2 = 0.23; P \ 0.0019 for TW). The percent of skeletal weight from total weight was signicantly different among species (KW = 16.208, P = 0.0028) being signicantly lower in P. magellanica than that of H. bispinis (Dunns post hoc test, P \ 0.01, Table 3). The skeletal ash content was signicantly different among species (KW = 12.227, P = 0.0157) being signicantly lower in H. bispinis than in P. tessellata (Dunns post hoc test, P \ 0.05, Table 3). The ashed skeleton values were signicantly different between species (KW = 20.651; P = 0.0004) being signicantly lower in P. magellanica than that of C. gobio or H. bispinis. Glycogen and lipid content of the muscle were signicantly different among P. magellanica, E. maclovinus, and P. tessellata (Table 4). Glycogen content was signicantly higher in P. tessellata than in E. maclovinus, and the lipid content was signicantly higher in E. maclovinus than in P. tessellata. The ash content was signicantly different among species, but no pairwise comparison was signicant (Table 4).

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Polar Biol Table 1 Buoyancy values and basic data on all the studied species (including total length, total weight, habit and preferred depth) Families/species Buoyancy (% SD) Nototheniids Bovichthydae Cottoperca gobio Eleginopidae Eleginops maclovinus Notothenidae Patagonotothen cornucola Patagonotothen tessellata Patagonotothen tessellata Paranotothenia magellanica Harpagiferidae Harpagifer bispinis

(median/range)

TL range (cm)

TW range (g)

Scope of activity

Habitat

Depth

4.58 (0.2) 4.43 (0.8) 5.35 (1.0) 4.33 (0.7) 4.14 (0.6) 3.88 (0.7)

4.6 (4.14.8) 4.4 (2.35.9) 5.0 (3.87.4) 4.3 (3.26.0) 4.1 (3.15.9) 4.0 (1.85.9)

20.037.6 13.549.0 6.412.1 16.637.0 17.521.4 11.241.3

104.5769.8 19.31,134.0 2.520.5 40.2222.7 63.2109.2 20.91,243.9

11 40 14 63 25 98

Sluggish Active Sluggish Sluggish Sluggish Very active

Benthic Benthopelagic Benthic Benthic Benthic Semi-Pelagic

Deep Coastal Intertidal resident Coastal/intertidal Coastal/intertidal Kelp-forest

6.96 (2.1)

6.7 (3.810.5)

6.07.8

3.26.6

12

Sluggish

Benthic

Intertidal resident

ndez et al. 2000; Johnston et al. 2003) Data on habit and depth are based on our personal observations and from previous work (Ferna gravid P. tessellata

Fig. 2 Box plots of the buoyancy values (B%). The boxes show the 25th and 75th percentiles of buoyancy for each species. The bars indicate 10th and 90th percentiles. The line inside the box is the median. Because the data were heteroscedastic and did not conform to the assumptions of the standard probability model, we used nonparametric percentile values for B%

Discussion Buoyancy and ecology of the sh species The buoyancy observed in the sub-Antarctic notothenioids corresponds to known values for benthic species (Eastman 1993). Nevertheless, there was a signicant difference

between the buoyancy of P. magellanica (most buoyant) and all other notothenioids (except gravid P. tessellata); between P. tessellata versus P. cornucola and H. bispinis (less-buoyant species); and between E. maclovinus and H. bispinis. Gravid P. tessellata females were more buoyant than non-gravid P. tessellata individuals. Although this intraspecic comparison was not statistically signicant,

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Polar Biol Table 2 Dunns post hoc tests showing pairwise comparisons of the buoyancy values of the different species Pm P. magellanica P. tessellata P. tessellata E. maclovinus C. gobio P. cornucola H. bispinis

Pt

Pt

Em

Cg

Pc

Hb

*** ** ** *** *** ** *** * *

Species are ordered from more buoyant to less buoyant. Species names in the columns are abbreviated for the sake of space gravid P. tessellata * P \ 0.05 ** P \ 0.01 *** P \ 0.001 Table 3 Analysis of the skeleton of the different species Species C. gobio E. maclovinus P. tessellata P. magellanica H. bispinis Skeleton weight from total weight* (%) 3.3 0.3 2.7 1.9 1.8 0.2 1.3 0.3*L 3.9 0.6*H Skeletal ash content** (%) 59.0 2.9 47.5 13.7 63.2 2.0 60.6 4.7 47.3 4.8 Ashed skeleton*** (%) 2.0 0.1*H 1.1 0.6 1.2 0.1 0.8 0.1*L 1.8 0.2*H # 6 5 4 5 7

Pairwise statistical signicant differences in the percent of skeletal weight from total weight and ashed skeletons between species are pointed out (*Hsignicantly higher; *Lsignicantly lower, Dunns test) * Skeleton weight/total weight 9 102 ** Ash weight/skeleton weight 9 102 *** Skeletal ash content/total weight 9 102 Table 4 Proximate analysis results of axial muscle for three common species in Beagle Channel waters (P. magellanica, E. maclovinus, and P. tessellata), including percentage values for carbohydrates, lipids, proteins, ash, and water content P. magellanica Glycogen* pids* L Proteins* Ashes* Water content** # 0.8 0.8 4.2 1.1 77.1 14.0 6.7 0.3 78.8 4.2 11 E. maclovinus 0.3 0.1 5.3 0.8 87.3* 6.3 0.3 76.1 3.9 6 P. tesellata 0.6 0.3 3.8 1.0 76.2 6.7 6.3 0.7 78.4 2.7 8 KruskalWalliss test P = 0.044/KW = 6.247 P = 0.0384/KW = 6.52 ns P = 0.0378 ns Dunns test Em vs. Pt (P \ 0.05) Em vs. Pt (P \ 0.05)

KruskalWallis test was used to compare each tissue, and signicant values were also determined in pairwise comparisons using Dunns post hoc test * Percentage of dry weight ** Percentage of wet weight

we found statistically signicant differences when comparing the buoyancy of these gravid females and nongravid individuals from other notothenioid species. For example, P. magellanica was signicantly more buoyant than non-gravid P. tessellata individuals but did not differ signicantly from gravid females of P. tessellata.

In spite of observed interspecic differences, all buoyancy values were similar to those from benthic Antarctic notothenioids (Eastman and De Vries 1982, 1985; Eastman 1993; Eastman and Sidell 2002). Thus, all species in this study should be considered benthic, consistent with previous studies that found that neutral buoyancy in

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notothenioids is rare (Eastman and Sidell 2002; Eastman 2005), although P. magellanica could also be considered benthopelagic. The ecological background knowledge we have on the habits of the different species analyzed correlates well with the buoyancy values measured in most of the species. Our previous knowledge is derived from more than 10 years of working on notothenioids in the Beagle Channel and more specically from a study we have made on the kelp forest of the area, distinguishing shes that live in the water column or are associated with the bottom (Vanella et al. 2007). H. bispinis and P. cornucola are benthic species found in the intertidal zone and the kelp holdfast (Moreno and Jara 1984; Vanella et al. 2007). At low tide, they can be found under rocks with H. bispinis furthest from the water ndez unpublished results). P. cornucola eggs level (Ferna have been found inside the holdfast of Macrocystis pyrifera (Vanella et al. 2007), and H. bispinis egg masses are regularly found in Beagle Channel shores around Ushuaia Bay ndez, pers. com). The position of these species (Ferna among notothenioids, as the least buoyant, is therefore consistent with our ecological knowledge. The variability found in the buoyancy values for H. bispinis was due to the low weight of the individuals, resulting in larger errors around the buoyancy measurements. Similarly, we found that C. gobio had low buoyancy, and it is a known benthic species living at a depth of 10270 m (Lloris and Rucabado 1991) and associated with the kelp holdfast (Vanella et al. 2007). With intermediate buoyancy, P. tessellata is found throughout the water column in a kelp forest but not in the kelp holdfast (Vanella et al. 2007). Although it is not a resident species of the intertidal zone, P. tessellata uses this habitat for reproduction during summer and winter (Rae ndez 2006). Also and Calvo 1995a, b; Ceballos and Ferna with intermediate buoyancy, E. maclovinus is active and moves daily along the coast, entering estuaries probably for spawning (Gosztonyi 1980; Calvo et al. 1992; Veas 1998; Licandeo et al. 2006). In captivity, this species primarily remains on the bottom of the tank or swims slowly using the pectoral ns. When being chased or pursuing a prey, it swims with rapid caudal propulsion (fast starts) and gliding with the pectoral ns after being propelled by the tail beats ndez et al. 2002). (Ferna The most buoyant species was P. magellanica. This species has been associated with kelp fronds and the upper portion of the water column (Moreno and Jara 1984; Vanella et al. 2007) and swims into the kelp forest to ndez et al. unpubforage (Moreno and Jara 1984; Ferna lished results). In captivity, they swim continuously and slowly in the water column using their pectoral ns. When chased, they swim fast using subcarangiform locomotion ndez et al. unpublished results). (Ferna

Skeletons, tissues, and energy The ashed skeleton values corresponded well with the buoyancy of the different species. P. magellanica had the lowest ash skeleton value and the highest buoyancy, while C. gobio and H. bispinis had high skeleton ashed values and lowest buoyancy. These differences could be explained for the percent of skeletal weight from total weight of the different species but not for differences in the skeletal ash content (Table 3). In general, the ashed skeleton values of the sub-Antarctic notothenioids were higher than those of Antarctic Notothenioids taken from the literature (Eastman and De Vries 1982), but the difference was not signicant. None of the sub-Antarctic species had values as low as the pelagic Antarctic species (\0.59). The proximate composition was studied in three of the more abundant species of notothenioids in the Beagle Channel: the coastal/intertidal benthic species (P. tessellata), one that inhabits the kelp forest with a more pelagic habitat (P. magellanica) and one coastal benthic species with a wide latitudinal distribution (E. maclovinus). In terms of buoyancy, the most important variable of the proximate composition is the lipid content (Eastman and De Vries 1982; Clarke et al. 1984; Friedrich and Hagen 1994; Phleger et al. 1999), which differed signicantly among species, being signicantly higher in E. maclovinus versus P. tessellata both intermediate buoyancy shes. The carbohydrates (glycogen) were also signicantly different among species, being higher in P. tessellata than in. E. maclovinus. However, the difference in total carbohydrates may include depletion in carbohydrate storage from struggling in the net after being captured and therefore should be taken with caution. Overall, proximate composition did not add valuable information to understand buoyancy differences between these three sub-Antarctic notothenioid species. Physiology related to dynamic lift In sub-Antarctic notothenioids, static buoyancy, metabolic rate, and the inuence of temperature reect known differences in habitat and behavior of the species. Species adapted to an active lifestyle have higher buoyancies, higher metabolic rates, and a lower temperature effect on their aerobic capacities. The latter correlates well with the nding that volume density of mitochondria increases substantially in demersal and moderately active sh but not in active species with temperature variation (Johnston et al. 1998). The intertidal resident species H. bispinis has low routine metabolic rates (0.96 mmol O2 h-1 kg-1), low mobility (in aquaria), and high Q10 for both routine metabolic rate (7.6) and postprandial metabolic rate (specic dynamic action, SDA) (Vanella and Calvo 2005; Vanella

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et al. 2010). Although there is no metabolic data for P. cornucola, data for the congener P. sima, an ecologically similar species, shows a similar pattern (0.21 mmol O2 h-1 kg-1 for routine metabolic rate and a Q10 value of 7.04 for routine metabolic rate). The coastal species E. maclovinus and P. magellanica have high routine metabolic rates (1.33 and 1.36 mmol O2 h-1 kg-1, respectively). Q10 of routine metabolic rate is high (6.91) for E. maclovinus and low (3.81) for P. magellanica (Vanella and Calvo 2005). The metabolism of P. tessellata has not been studied. Thus, more buoyant species are also more active, and therefore, dynamic lift could be reinforcing static buoyancy. We reject the hypothesis that the sub-Antarctic notothenioids have diverse static buoyancy values that allow them to occupy different places in the water column, like Antarctic notothenioids. However, we did detected signicant differences in the static buoyancy values of notothenioids, implying that some species, such us as P. magellanica and possibly E. maclovinus, may occupy more pelagic habitats as evidenced by their active behavior. By contrast, the notothenioids that inhabit the intertidal zones have low static buoyancy. Buoyancy values of sub-Antarctic notothenioids do not show a biogeographic signal since the two species that belong to the extra-Antarctic families, C. gobio and E. maclovinus (Bovichtidae and Eleginopidae, respectively) do not show a similar value different from the rest of the species. While the static buoyancy accurately predicts the habit of most sub-Antarctic notothenioids, buoyancy has both static and dynamic components. In cases where static buoyancy and habitats are not in agreement, it will be important to investigate the role of dynamic buoyancy.
s Chalde, FacAcknowledgments We would like to thank Toma undo Llompart, Eliana Tetamanzi and Eugenia Di Fiore for sampling assistance. We would like to thank Daniel Aureliano, Sonia Rimbau, Marcelo Gutierrez, Mariela Victorio and Eliana Gonzales for lab assistance. We would like to acknowledge Dr. Jorge Calvo for his intellectual input into the project. We would like to thank Joe Eastman, Tom Near and an anonymous reviewer for constructive comments on the original manuscript. Sheryl Macnie and Sandy Becker provided English editorial assistance. Funds for the project were provided by Agencia PICT 38152 and PICT 906, and CONICET PIP 6187.

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