MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

https://doi.org/10.47193/mafis.3422021010605

ABSTRACT. This study aimed to determine the diet composition and feeding strategies of the

hairy conger eel Bassanago albescens in the Southwest Atlantic (35° S-45° S), from stomach con-

tents analysis of 222 specimens. The diet consisted mainly of cephalopods, followed by isopods,

amphipods, ophiuroids, brachyurous and polychaetes. Results showed significant differences in the

composition of the diet between sexes, regions and size classes that were reflected in the changes

in the foraging strategy. The consumption of squid Illex argentinus progressively increased with a

growing predator size, where the largest individuals showed specialization in the consumption of

this particular prey. We propose these dietary changes would be related to morphological limita-

tions and abilities associated with the body size of B. albescens, with larger individuals having

access to larger prey. Our results help to understand the biology of a species that has a sympatric

distribution with two key species in the Argentine fisheries: hake Merluccius hubbsi and I. argenti-

nus, with evidence of a strong trophic interaction between them. This new information on the

resources involved would allow an optimization of the fisheries management under an ecosystem-

based criterion.

Key words: Anguilliformes, ecosystem-based fishery management, feeding habits, ontogenetic

changes.

Ecología trófica del congrio de profundidad Bassanago albescens en el Atlántico Sudoccidental

y sus implicancias para el manejo ecosistémico de las pesquerías

RESUMEN. En el presente estudio se determina la composición de la dieta y estrategia alimen-

taria del congrio de profundidad Bassanago albescens en el Atlántico Sudoccidental (35° S-45° S),

a partir del análisis del contenido estomacal de 222 individuos. La dieta consistió de cefalópodos,

seguidos por isópodos, anfípodos, ofiuroideos, braquiuros y poliquetos. Los resultados mostraron

diferencias significativas en la composición de la dieta entre sexos, zonas y clases de tallas que se

vieron reflejadas en los cambios de la estrategia de forrajeo. Se registró un aumento progresivo en

el consumo de Illex argentinus con el aumento del tamaño de B. albescens, donde los individuos

más grandes mostraron una especialización en el consumo de esta presa. Estos cambios alimenta-

rios estarían relacionados a limitaciones morfológicas y habilidades asociadas al tamaño corporal

de B. albescens, teniendo los individuos más grandes acceso a presas de mayor tamaño. Nuestros

resultados ayudan a comprender la biología de una especie que tiene una distribución simpátrica

con dos especies clave en las pesquerías de la Argentina: Merluccius hubbsi e I. argentinus, con

181

*Correspondence:

gabriela_blasina@hotmail.com

Received: 26 February 2021

Accepted: 10 May 2021

ISSN 2683-7595 (print)

ISSN 2683-7951 (online)

https://ojs.inidep.edu.ar

Journal of the Instituto Nacional de

Investigación y Desarrollo Pesquero

(INIDEP)

This work is licensed under a Creative

Commons Attribution-

NonCommercial-ShareAlike 4.0

International License

Marine and

Fishery Sciences

MAFIS

ORIGINAL RESEARCH

Trophic ecology of hairy conger eel Bassanago albescens in the Southwest

Atlantic and its implications for the ecosystem-based fishery management

GABRIELA BLASINA1, 2, *, LUCIANO IZZO3, AGUSTÍN DEWYSIECKI4and DANIEL FIGUEROA3

1Instituto Argentino de Oceanografía (IADO), Universidad Nacional del Sur (UNS)-CONICET, Camino La Carrindanga km 7.5,

B8000FWB - Bahía Blanca, Argentina. 2Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur (UNS),

San Juan 670, B8000ICN - Bahía Blanca, Argentina. 3Laboratorio de Biología de Peces, Departamento de Ciencias Marinas, Facultad de

Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata (UNMdP), Funes 3350, B7602AYL - Mar del Plata, Argentina.

4Centro para el Estudio de Sistemas Marinos (CESIMAR), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),

Boulevard Brown 2915, U9120ACD - Puerto Madryn, Argentina

INTRODUCTION

The hairy conger eel Bassanago albescens

(Barnard, 1923) is an endemic species of the

Southern Hemisphere (Figueroa 1992; Anderson

2005; Buratti et al. 2020). It lives between 81 and

600 m deep (Reyes 2007) and presents a sym-

patric distribution with two key species in Argen-

tine fisheries, the Argentine hake (Merluccius

hubbsi) and Argentine squid (Illex argentinus)

(Haimovici et al. 1998; Arkhipkin et al. 2015). B.

albescens is an iteroparous species with a lepto-

cephalus larva (Figueroa and Ehrlich 2006),

marked sexual dimorphism (Blasina et al. 2018),

and benthic trophic habits (Figueroa 1999). In the

Argentine shelf, a large biomass has been record-

ed (García et al. 2010) as part of the bycatch of

the Patagonian scallop (Zygochlamys patagoni-

ca) fishery (Bremec et al. 2003) and commercial

catches of M. hubbsi (Renzi and Castrucci 1998).

Aquatic ecosystems are suffering alterations

due to the development of the fishing industry,

and these have been the focus of copious investi-

gations (Craing et al. 2009; FAO 2018). The

propagation of such impacts on ecosystems dif-

fers according to whether the food web is con-

trolled by apex predators (top-down control), by

lower levels (bottom-up control) or by dominant

species in medium trophic level (wasp-waist con-

trol) (Hill et al. 2020). Therefore, in recent

decades, a consensus has been reached on the

need to implement ecosystem-based fisheries

management (Pikitch et al. 2004; FAO 2018). In

this context, the complex interactions occurring

in an ecosystem must be considered to evaluate

the effects of fishing activities in an integrated

way (Branch et al. 2010). Such interactions are

key factors in the functioning, structure, compo-

sition and abundance of the species involved, and

in ecological processes such as predation and

competition for resources (Lercari et al. 2014).

Therefore, trophic ecology studies are essential to

understand the interrelationships and community

dynamics within an ecosystem (Amundsen and

Sánchez-Hernández 2019).

To understand the role that a species plays in a

biotope, it is necessary to describe the trophic

behaviour of the constituent species that compose

it, even those that have not been investigated due

to their lack of commercial importance (Stephens

et al. 2007; Brown et al. 2012). In this sense,

stomach content analysis is essential (Amundsen

and Sánchez-Hernández 2019). Few studies have

been conducted on the diet of B. albescens to

date, noting that its prey is represented mostly by

benthic invertebrates (Meyer and Smale 1991;

Figueroa 1999; Anderson 2005). The breadth of a

consumer’s trophic niche is determined by a vari-

ety of biological and environmental characteris-

tics (Hayden et al. 2019). Hayden et al. (2019)

have shown a latitudinal variation in the mean

trophic niche breadth of fish species, evidencing

that near the Equator they present a broader

trophic niche than those of the Arctic or Antarctic

seas. However, diet is also determined by a preda-

tor’s morphology, especially size, mobility, and

dentition that will determine what types of prey it

can capture (Stuart-Smith et al. 2013). Many

species show ontogenetic changes in habitat,

which are related to the type of prey and its size

(Griffiths 2020). Understanding these changes in

resource use is particularly important from an

ecological perspective because they can help

illustrate the integral functioning of the ecosys-

tem (Hooper et al. 2005; Brose et al. 2019). The

present work aims to: (1) quantify the composi-

182 MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

evidencias de una fuerte interacción trófica entre ellas. Esta nueva información sobre los recursos involucrados permitiría una optimi-

zación del manejo pesquero bajo un criterio ecosistémico.

Palabras clave: Anguilliformes, manejo ecosistémico de las pesquerías, hábitos alimentarios, cambios ontogenéticos.

tion of the diet of B. albescens, (2) determine the

feeding strategy through stomach content analy-

sis, and (3) investigate possible ontogenetic

changes in diet.

MATERIALS AND METHODS

The study area covered part of the Argentine

shelf between 36° S and 46° S and between 100

and 170 m deep. B. albescens specimens were

caught in two research surveys (EH-02/2009 and

EH-04/2009) carried out by the fisheries research

vessel ‘Dr. Eduardo L. Holmberg’ from the Insti-

tuto Nacional de Investigación y Desarrollo Pes-

quero (INIDEP), Argentina (Figure 1). In both

surveys, a bottom trawl gear was used for sam-

pling, and individuals were kept at -20 °C for pos-

terior analysis. Samples were thawed in the labo-

ratory at room temperature, and total length (LT),

weight without stomach (W) and sex were record-

ed in each specimen. Prey found inside stomachs

were separated and identified to the lowest possi-

183

BLASINA: TROPHIC ECOLOGY OF HAIRY CONGER EEL BASSANAGO ALBESCENS

Figure 1. Map of the study area showing fishing trawls where specimens of Bassanago albescens were caught. Black circles

indicate positive trawls for B. albescens from which diet samples were obtained. Grey triangles and crosses correspond

to the northern and southern region trawls.

69° 67° 65° 63° 61° 59° 57° 55° 53° 51°

55°

54°

53°

52°

51°

50°

49°

48°

47°

46°

45°

44°

43°

42°

41°

40°

39°

38°

37°

36°

35°

50 m

200 m

San Matías

Gulf

Malvinas Islands

Atlantic Ocean

Río de la Plata

San Jorge Gulf

Tierra del Fuego

Argentina

Uruguay

W

S

ble taxonomic level using taxonomic keys and

field guides (Bastida and Torti 1973; Boschi et al.

1992). The number, length (mm) and wet weight

(±0.01 g) of each prey were also recorded.

To determine the most important prey in the

diet of B. albescens, the Prey-Specific Index of

Relative Importance (%PSIRI, Brown et al. 2012)

was estimated as follows:

PSIRI =0.5 ×%FO ×(%Ni+%Mi)

where %FO is the percent frequency of occur-

rence of a particular prey (i.e. the number of

times a given prey is found in the total number of

stomachs with content, expressed as a percent-

age), %Niis the specific numerical abundance of

each prey (i.e. the percent numerical abundance

of a given prey found among the stomach sam-

ples), and %Miis the abundance of the specific

wet weight of the prey calculated for each prey.

PSIRI values were relativized to 100% (%PSIRI).

Cumulative prey curves were used to determine

whether an adequate number of stomachs had

been examined to describe the diet accurately.

The order in which stomachs were analysed was

randomized 100 times to minimize bias resulting

from the order of sampling. The asymptote of the

curve indicated the minimum sample size

required to adequately describe the diet (Ferry

and Cailliet 1996). To construct these curves, six

prey groups were considered: ophiuroids,

amphipods, isopods, polychaetes, cephalopods

and brachyurous, which together represented

more than 95% of the %PSIRI.

The variation in diet composition between

sexes, size classes (SC 1: <=540 mm LT, SC 2:

540-650 mm LT, and SC 3: >=650 mm LT) and

regions (north: 36° S-41° S, and south: 44° S-

47° S, corresponding to campaigns EH-04/2009

and EH-02/2009, respectively) were analysed.

The interaction between SC and regions were also

analysed through a non-parametric multivariate

analysis of variance (NP-MANOVA, Anderson

2001), using the number of prey and the Bray Cur-

tis distance measure with 10.000 permutations

(Zuur et al. 2007). All statistical analyses were

performed using R Software version 3.6.0 (R Core

Team 2019), with a significance level of 0.05.

To evaluate the feeding strategy of B.

albescens (as a generalist or specialist) and the

importance of prey (dominant or rare), we used

the graphic method proposed by Amundsen et al.

(1996). The method consists of plotting the spe-

cific abundance of the prey (Pi) against its fre-

quency of occurrence (%FO). Piis defined as the

percentage of the total number of prey idivided

by the number of all prey present in those individ-

uals that contained prey i. The analysis of the

feeding strategy was carried out considering the

main prey categories outlined above.

The relationship between the total length of B.

albescens and prey size was evaluated using the

width of the crabs’ shell, total length of

amphipods and isopods, disk width of echino-

derms, and standard length of teleosts. The

increase in the minimum, average and maximum

size of the prey consumed with the increase in the

total length of the predator was calculated, testing

the significance (P=0.05) of the slope of the

quantile regressions of 5, 50 and 95%, respective-

ly (Griffiths 2020).

The trophic position of B. albescens was deter-

mined by its trophic level (TL) for each size class

and area, applying the method proposed by

Cortés (1999) expressed as:

TL =1 +(∑ Pj×TLj)

where TLjis the trophic level of each prey item

(taken from Ebert and Bizarro 2007) and Pjis the

proportion of each prey item in the diet of B.

albescens.

To evaluate whether differences in the diet

composition and TL between regions were

reflected in the LT-W relationship of the individ-

uals, an estimation of it was carried out according

to the equation W =aLTbusing linear regression

after a logarithmic transformation of the vari-

184 MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

ables: log W =log a+blog LT(Froese 2006).

The degree of association between LTand W was

determined using the coefficient of determination

(r2). The hypothetical isometry values (b=3)

were tested by Student’s t-test with a 95% confi-

dence limit level (Zar 1999). An analysis of

covariance (ANCOVA, Zuur et al. 2007) was per-

formed to test for significant differences in

regression gradients between sexes (P=0.05).

RESULTS

Of the 222 stomachs analysed, 186 (83.78%)

presented some type of content. The sample from

the southern region consisted of 131 females rang-

ing 543-772 mm LT. No males were recorded. The

northern region was represented by 52 females

ranging 498-640 mm LT, and 39 males ranging

400-537 mm LT, which represented 16% of the

total sample and were all grouped within the SC 1.

A total of 34 prey items were identified. %PSIRI

values indicated that the main prey category in the

diet of B. albescens was cephalopods, followed by

isopods, amphipods, ophiuroids, brachyurous and

polychaetes (Table 1). The rest of the prey items

presented less than 5% of the %PSIRI (Table 1).

The most frequently consumed prey was the

squid I. argentinus, followed by the isopod

Cirolana spp., and the ophiuroid Ophiuroglypha

lymani (Table 1). Cumulative curves of the num-

ber of prey as a function of the sample size

revealed that the number of stomachs considered

185

BLASINA: TROPHIC ECOLOGY OF HAIRY CONGER EEL BASSANAGO ALBESCENS

Table 1. Frequency of occurrence (%FO), prey-specific number abundance (%Ni), prey-specific weight abundance (%Mi), Prey-

Specific Index of relative Importance (PSIRI), and percentage of PSIRI (%PSIRI) for the total sample of Bassanago

albescens.

Prey item %FO %Ni %Mi PSIRI %PSIRI

Teleostei 4.48

Patagonotothem sp. 2.19 30.77 37.52 74.78

Sebastes oculatus 0.54 33.33 20.48 14.53

Iluocoetes fimbriatus 0.54 50.00 99.83 40.45

No identificados 7.65 32.65 21.39 206.70

Chondrichthyes 0.16

Psammobatis sp. 0.55 33.33 9.73 11.84

Polychaeta 6.95

Questidae 0.54 50.00 79.31 34.91

Flabelligeridae 0.55 66.66 88.88 42.77

Eunicidae 1.09 45.45 79.68 68.20

Ophelidae 1.63 37.50 2.66 32.73

Lumbrineridae 3.28 3.28 6.63 16.25

Onuphidae 1.64 42.86 0.76 35.77

Capitellidae 0.55 20.00 6.85 7.38

Gliceridae 1.64 50.00 0.62 41.51

Not identified 12.02 31.82 8.48 242.20

186 MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

Table 1. Continued

Prey item %FO %Ni %Mi PSIRI %PSIRI

Mollusca

Cephalopoda 37.74

Illex argentinus 38.80 50.74 95.29 2,832.98

Gasteropoda 0.73

Marginella warrenii 0.54 50.00 42.86 25.07

Natica isabelleana 0.55 50.00 57.5 29.56

Bivalvia 0.78

Amiantis purpurata 1.09 7.41 8.22 8.52

Atrina seminude 0.54 96.97 87.62 49.84

Crustacea

Amphipoda 11.02

Gammaridae 13.66 57.00 2.83 408.64

Hyperiidae 7.10 80.7 37.14 418.33

Isopoda 15.16

Cirolana sp. 29.51 44.27 5.84 739.37

Serolis schythei 13.66 37.36 10.12 324.29

Serolis sp. 2.18 60.00 8.47 74.63

Brachyura 10.35

Sympagurus dimorphus 10.93 35.61 93.34 704.71

Not identified 2.73 11.36 41.45 72.09

Echinodermata

Ophiuroidea 10.91

Ophiuroglypha lymani 16.39 64.63 35.34 819.25

Cnidaria 1.41

Actinostola crassicornis 0.55 100.00 100.00 55.00

Tubo Hidrozoa indet. 3.28 25.8 5.23 50.89

Thaliacea 0.13

Iasis zonaria 0.54 7.14 28.09 9.51

Algae 0.18

Not identified 0.54 25.00 25.00 13.50

to describe and analyse the diet of B. albescens

were sufficient since the asymptote was reached

as a function of the number of samples for all the

groups considered (Figure 2).

Comparison of the composition of the diet

between the SC 1 individuals of both sexes did not

show significant differences (F =0.77; P=0.5405)

and were grouped for subsequent analyses. Results

of the two-way NP-MANOVA indicated that there

were significant differences in the composition of

the diet between SCs (F =15.29; P=0.0009) and

regions (F =47.27; P=0.0011), and also interac-

tion between the effects of both factors (F =3.89;

P=0.0001). Subsequent one-way NP-MANOVA

indicated significant differences between SC 2

and SC 3 in the southern region, and between all

SCs in the northern region versus those of the

southern region. On the contrary, no significant

differences were found in the composition of the

diet between the specimens of both SCs from the

187

BLASINA: TROPHIC ECOLOGY OF HAIRY CONGER EEL BASSANAGO ALBESCENS

Figure 2. Cumulative prey curves for Bassanago albescens as a function of stomach number (mean ±SD) from all specimens,

three size classes (SC) and both regions.

All specimens SC 1 ( 540 mm L )<T

SC 3 ( 650 mm L )>T

SC 2 (540-650 mm L )

T

Northern region Southern region

Number of stomachs

111213141516171 81 91 101 111

111213141516171

111213141516171 1 6 11 16 21 26 31 36 41 46 51 56 61 66 71

1 21 41 61 81 101 121 141 161 181 147101316192225283134

6

4

2

0

8

6

4

2

0

8

6

4

2

0

6

4

2

0

7

6

5

4

3

2

1

0

Cumulative number of preys

8

6

4

2

0

northern region (Table 2). Therefore, all the indi-

viduals from the northern region were grouped

for the following analyses. The specimens from

the northern region fed predominantly on

amphipods and ophiuroids, completing their

trophic spectrum with brachyurous and poly-

chaetes. As for the southern region, SC 2 speci-

mens consumed a higher proportion of isopods

and amphipods, while those corresponding to SC

3 consumed a higher proportion of cephalopods,

followed by isopods (Figure 3).

Taking into account the diet variation, the feed-

ing strategy was evaluated in general and for each

size class. The relationship between Piand %FO

indicated that the feeding strategy of B. albescens

tended towards generalist (Figure 4 A), but pre-

sented variations according to the size of the indi-

viduals. SC 1 specimens tended to specialize in

amphipods and those belonging to SC 2 presented

a generalist feeding strategy (Figures 4 B and C).

SC 3 individuals presented a specialization

towards cephalopods and isopods (Figure 4 D).

When analysing the relationship between sizes

of predator and prey, we see that the size of the

prey increases linearly with the size of the preda-

tor. However, the minimum prey size remained

constant, indicating that the largest B. albescens

individuals fed on both large and small prey,

while those with a smaller length fed only on

small prey (Table 3; Figure 5).

The TL of B. albescens varied by region and

between southern region size classes. Individuals

captured in the northern region presented an TL

of 3.78, whereas the specimens of classes SC 2

and SC 3 captured in the southern region showed

an TL of 3.89 and 4.11, respectively.

The LT-W relationship of B. albescens did not

differ significantly between regions (ANCOVA;

F =2.203; df =1; P=0.139), presenting positive

allometric growth in both (Table 4; joint Stu-

dent’s t-test: t =8.671; P=0.0002).

DISCUSSION

The study of the feeding habits of B. albescens

in the Argentine shelf indicated that the species is

a demersal-benthic predator. Its main prey is

cephalopods, followed by isopods, amphipods,

ophiuroids, brachyurous and polychaetes. The

percentage of empty stomachs was low (16.22%),

188 MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

Table 2. Non-parametric MANOVA testing differences in sex, size classes (SC) and region on the number and weight of main

prey items of Bassanago albescens. df: degrees of freedom.

Factor

Number Weight

df F P F P

North-SC 1 versus North-SC 2 1 0.50 0.7715 0.46 0.8537

North-SC 1 versus South-SC 2 1 19.01 *0.0001 8.51 *0.0001

North-SC 1 versus South-SC 3 1 24.59 *0.0001 15.60 *0.0001

North-SC 2 versus South-SC 2 1 20.93 *0.0001 10.50 *0.0001

North-SC 2 versus South-SC 3 1 24.59 *0.0001 19.90 *0.0001

South-SC 2 versus South-SC 3 1 7.17 *0.0002 3.84 *0.0036

*Significant differences.

189

BLASINA: TROPHIC ECOLOGY OF HAIRY CONGER EEL BASSANAGO ALBESCENS

Figure 3. Mean number (±SD) of prey consumed by Bassanago albescens grouped by size class (SC) and region.

Figure 4. Relationship between percent prey-specific abundance and frequency of occurrence (%FO) of Bassanago albescens

prey from all specimens and size classes (SC) considered.

Isopods

Amphipods

Polychaetes

Ophiuroids

Brachyurous

Cephalopods

North-SC 1 and 2 South-SC 2 South-SC 3

Mean number consumed

3.5

3.0

2.5

2.0

1.5

1.0

0.5

0.0

A

0

20

40

60

80

100

0 20406080100

All specimens

B

0

20

40

60

80

100

0 20406080100

SC 1 ( 540 mm L )<T

C

0

20

40

60

80

100

0 20406080100

Prey-specific abundance (%)

%FO

SC 2 (540-650 mm LT)

D

0

20

40

60

80

100

0 20406080100

%FO

SC 3 ( 650 mm L>T)

Ophiuroids Amphipods Isopods Polychaetes Cephalopods Brachyurous

190 MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

Table 4. Estimated parameters of length (LT)-weight (W) relationship and determination coefficient (r2) for Bassanago albescens

in the Southwest Atlantic shelf. N: number of individuals, min: minimum, max: maximum, a: intersection, b: slope.

LT(mm) W (g)

Region N Min Max Min Max a b r2

North 91 371 661 50 510 2 × 10-8 3.654 0.910

South 131 543 772 208 905 2 × 10-7 3.363 0.883

Table 3. Predator length-prey length relationship using the total length of Bassanago albescens and maximum size of prey.

Minimum (5% quantile regressions), mean (50% quantile regressions) and maximum (95% quantile regressions).

Maximum size of prey

Regression Intersection Slope P

Minimum -17.06 0.038 0.004

Mean -59.47 0.126 < 0.001

Maximum -361.90 0.853 < 0.001

Figure 5. Relationship between Bassanago albescens (predator) size and prey size. Dotted, dashed, and solid lines indicate

regression quartiles 5, 50, and 95%, respectively.

0

50

100

150

200

250

300

350

400 450 500 550 600 650 700 750 800 850

Prey (mm)size

Predator total length (mm)

with similar values reported by Meyer and Smale

(1991) and Figueroa (1999). On the contrary, in

related species that feed mainly on teleosts such

as the coastal conger eel, Conger orbignianus, the

proportion of empty stomachs is higher (71%,

Figueroa 1999). This is because the species that

feed mainly on small and medium invertebrates,

such as B. albescens, have a more frequent con-

sumption of prey than those species with a diet

based on fish (San Martín et al. 2007).

Results from diet composition in the present

work are in part consistent with previous studies.

In the coasts of Argentina, Figueroa (1999)

observed a diet consisting of ophiuroids with the

presence of crustaceans and polychaetes. In the

coasts of South Africa, Meyer and Smale (1991)

found sea pen cnidarians and brachyurous

Chaceon sp. as dominant and more numerous

preys over the ophiuroid Ophiura trimeni; many

of the prey were small crustaceans that included

isopods, tanaidaceans, and Macrura decapods.

Studies carried out by Anderson (2005) indicated

hagfish Myxine capensis and different species of

mesopelagic teleosts as dominant prey; the most

abundant fish in the diet were juveniles of hake

Merluccius spp. and other conger eels; the second

most important category consisted of at least six

species of ophiuroids. The rest of the prey were

benthic or benthopelagic species, except squid.

The differences found in the results of Meyer and

Smale (1991), Figueroa (1999) and Anderson

(2005) with respect to the present work, could be

related to the area from where the samples were

obtained in each study.

The diet of B. albescens varied according to

the study area. In the southern region, the most

important prey was I. argentinus, which would

be explained by a concentration of the South

Patagonian subpopulation of this prey that coin-

cided spatiotemporally with the southern sam-

pling survey (Ré 2007). Furthermore, the fact

that the survey is directed to the evaluation of

squid could generate a bias in the composition of

the diet of the SC 3 individuals. The SC 2 class,

the only class present in both areas, fed mainly

on isopods in the south, and wide-distributed

amphipods and ophiuroids in the north (Boschi et

al. 1992; Bremec et al. 2003). Differences in the

diet composition of B. albescens between differ-

ent regions would be attributed to differences in

the availability of prey species, and the size and

sex of the specimens captured in each one, possi-

bly driven by energy requirements of each sex

and ontogenetic stage (Livingston 2003). To

analyse the selective characteristics of this

species in detail, complementary studies should

be carried out in which the relative abundance of

prey is determined in these two regions of the

Argentine shelf.

The analysis indicated that the feeding strategy

changed during growth. SC 1 individuals (all

males are included here) showed a tendency to

specialize in the consumption of amphipods, SC

2 individuals had a generalist feeding strategy,

and SC 3 individuals (all mature females) pre-

sented a specialization towards cephalopods and

isopods. Transitions from one feeding stage to

another are generally related to the ontogenetic

development of the species (Livingston 2003).

Stuart-Smith et al. (2013) highlighted that feed-

ing progressions are associated with ontogenetic

changes regarding body morphology and corre-

lated with movement, teething and dimensions of

the mouth and guts. Figueroa (1999) mentioned

that in C. orbignianus, smaller specimens feed on

crustaceans and fish while older fish are exclu-

sively piscivorous, with prey of demersal-benthic

origin (sciaenids and flounder). On the contrary,

Anderson (2005) observed in the coasts of South

Africa that there was no relationship between the

predator size and the type of diet of B. albescens

and the southern conger Gnathophis capensis.

The ontogenetic and regional differences record-

ed in the present study, both in the diet composi-

tion and feeding strategy, suggested that a varia-

tion in the abundance of B. albescens in the

Southwest Atlantic has the potential to impact

various levels of the trophic chain of the region.

191

BLASINA: TROPHIC ECOLOGY OF HAIRY CONGER EEL BASSANAGO ALBESCENS

This observation is supported by the results of the

TL analysis, which varies according to the SC

and the distribution range of predators.

The relationship between B. albescens size and

the maximum prey size increased linearly, which

is consistent with the maximization of energy

intake, although the minimum prey size remained

constant. Small prey provides low benefits, while

relatively large prey has higher energy content,

but is potentially dangerous to attack (Griffiths

1980). Although the probability of an individual

prey being encountered by a predator may

increase with the body size of that prey (Mihalit-

sis and Bellwood 2017), predators could also

increase energy potential with ingestion as they

grow larger if they continue to eat small and easy-

to-catch prey (Griffiths 2020). This is why the

maximum prey size is roughly proportional to the

size of the predator in all habitats, but the mini-

mum prey size slopes may differ between habitats

since predators can change the type of prey they

ingest to keep elevated encounter rates (Floeter

and Temming 2003; Killen et al. 2007). The com-

bination of a high frequency of encounter, due to

a greater relative abundance, and a high probabil-

ity of capture could explain the continued inclu-

sion of small prey in the diet of B. albescens.

Blasina et al. (2018) found a sexual dimor-

phism in the size of B. albescens, where males

reached smaller size than females. This conclu-

sion is reflected in the ranges of SCs used in the

present work, in which all males were included in

SC 1 and located in the northern region. The feed-

ing strategy determined for this class indicated a

tendency to specialize in amphipods. The situa-

tion of SC 3 is different because is comprised of

larger female individuals distributed in the south-

ern region, and specialized in cephalopods and

isopods. Energy requirements for sperm produc-

tion are not the same as those required for the pro-

duction of oocytes, which after fertilization

results in leptocephali larvae that can exceed

200 mm (Figueroa and Ehrlich, 2006). This could

explain the greater size of females and their

southern distribution to access these resources.

Macchi et al. (2010) argued that large mature

female hake could travel long distances to deep

Patagonian waters in search of I. argentinus,

where it is found in large concentrations. This

cephalopod would be chosen for its high concen-

tration of fatty acids.

In the Argentine shelf, B. albescens presents

important biomass, recording catches of up to

12 t per trawl (Figueroa 1992, 1999). In the pres-

ent study, it was determined that one of the most

important prey items in the diet of B. albescens is

the squid I. argentinus. This species is also an

important trophic resource in the diet of the

Argentine hake, M. hubbsi (Belleggia et al.

2014), which could suggest a possible trophic

niche overlap that would be pertinent to assess in

the future. When two or more species coexist,

interspecific competitive interactions can develop

by exploiting a common resource that is scarce or

predates each other. These interactions can affect

the abundance and distribution of species in a

community (Hayden et al. 2019). Argentine hake

M. hubbsi represents one of the main species of

fish caught in Argentine trawl fisheries (Irusta et

al. 2016) and, together with squid I. argentinus,

are among the most important species in terms of

exportable quota from Argentina (MAGyP 2019).

Given the complexity of the interactions that can

occur in a marine community, the study of indi-

vidual trophic behaviour and the relationships of

the organisms that comprise it become essential

for the implementation of adequate management

of fishing resources under an ecosystem-based

approach (FAO 2018).

ACKNOWLEDGMENTS

We are grateful to INIDEP for the specimens

collected in research surveys and to Drs Ricardo

Bastida, Santiago Barbini, Cecilia Spath and

Mauro Belleggia for their collaboration in identi-

192 MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

fying prey items. We also thank the anonymous

reviewers for their corrections and suggestions

that have improved an earlier version of this work.

REFERENCES

AMUNDSEN PA, GABLER H, STALDVIK F. 1996. A

new approach to graphical analysis of feeding

strategy from stomach contents data modifica-

tion of the Costello (1990) method. J Fish

Biol. 48: 607-614.

AMUNDSEN PA, SÁNCHEZ-HERNÁNDEZ J. 2019.

Feeding studies take guts - critical review and

recommendations of methods for stomach

contents analysis in fish. J Fish Biol. 95: 1364-

1373.

ANDERSON ME. 2005. Food habits of some deep-

sea fish off South Africa’s west coast. 2. Eels

and spiny eels. Afr J Mar Sci. 27: 557-566.

ANDERSON MJ. 2001. Permutation test for uni-

variate o multivariate analysis of variance and

regression. Can J Fish Aquat Sci. 58: 629-639.

ARKHIPKIN AI, LAPTIKHOVSKY VV, BARTON AJ.

2015. Biology and fishery of common hake

(Merluccius hubbsi) and southern hake

(Merluccius australis) around the Falkland/

Malvinas Islands on the Patagonian shelf of

the Southwest Atlantic Ocean. In: ARANCIBIA

H, editor. Hakes, biology and exploitation.

Oxford: Wiley. p. 154-184.

BASTIDA R, TORTI M. 1973. Los isópodos

Serolidae en la Argentina. Clave para su reco-

nocimiento. Physis A. 32 (84): 19-46.

BELLEGGIA M, FIGUEROA DE, IRUSTA G, BREMEC

C. 2014. Spatio-temporal and ontogenetic

changes in the diet of the Argentine hake

Merluccius hubbsi. J Mar Biol Assoc UK. 94:

1701-1710.

BLASINA GE, IZZO L, FIGUEROA D. 2018. Sexual

dimorphism and length-weight relationship of

the hairy conger eel Bassanago albescens

(Anguilliformes: Congridae). J Ichthyol. 58

(3): 396-400.

BOSCHI E, FISCHBACH C, IORIO M. 1992. Catálogo

ilustrado de los crustáceos estomatópodos y

decápodos marinos de Argentina. Frente

Marít. 10: 7-94.

BRANCH TA, WATSON R, FULTON EA, JENNINGS S,

MCGILLIARD RC, PABLICO GT, RICARD D,

TRACEY SR. 2010. The trophic fingerprint of

marine fisheries. Nature. 468: 431-435.

BREMEC C, MARECOS A, SCHEJTER L, LASTA M.

2003. Guía técnica para la identificación de

invertebrados epibentónicos asociados a los

bancos de vieira patagónica (Zygochlamys

patagonica) en el Mar Argentino. Mar del

Plata: Instituto Nacional de Investigación y

Desarrollo Pesquero (INIDEP). 28 p.

BROSE U, ARCHAMBAULT P, BARNES AD, BERSIER

LF, BOY T, CANNING-CLODE J, CONTI E, DIAS

M, DIGEL C, DISSANAYAKE A, et al. 2019.

Predator traits determine food-web architec-

ture across ecosystems. Nat Ecol Evol. 3: 919-

927.

BROWN SC, BIZZARRO JJ, CAILLIET GM, EBERT

DA. 2012. Breaking with tradition: redefining

measures for diet description with a case study

of the Aleutian skate Bathyraja aleutica

(Gilbert 1896). Environ Biol Fish. 95 (1): 3-

20.

BURATTI C, DÍAZ DE ASTARLOA JM, FALABELLA V,

HÜNE M, IRIGOYEN A, LANDAETA M,

LINARDICH C, RIESTRA C, VIEIRA J, CAMPAGNA

C. 2020. Informe del Taller Regional de

Evaluación del Estado de Conservación de

Especies para el Mar Patagónico según crite-

rios de la Lista Roja de UICN: Peces óseos.

Foro para la Conservación del Mar Patagónico

y áreas de influencia. 117 p.

CORTÉS E. 1999. Standardized diet compositions

and trophic levels of sharks. ICES J Mar Sci.

56 (5): 707-717.

CRAING CM, HALPERN BS, BECK MW, KAPPEL

CV. 2009. Understanding and managing

human threats to the coastal marine environ-

ment. Ann NY Acad Sci. 1162 (1): 39-62.

193

BLASINA: TROPHIC ECOLOGY OF HAIRY CONGER EEL BASSANAGO ALBESCENS

EBERT DA, BIZZARRO JJ. 2007. Standardized diet

compositions and trophic levels of skates

(Chondrichthyes: Rajiformes: Rajoidei). Env-

iron Biol Fishes. 80: 115-131.

[FAO] FOOD AND AGRICULTURE ORGANIZATION OF

THE UNITED NATION. 2018. The state of world

fisheries and aquaculture. Rome: FAO. 227 p.

FERRY L, CAILLIET G. 1996. Sample size and data

analysis: are we characterizing and comparing

diet properly? In: MAC KINLAY D, SHEARER K,

editors. Feeding ecology and nutrition in fish.

San Francisco: American Fisheries Society. p.

71-80.

FIGUEROA D. 1992. Distribución geográfica y

estadísticas pesqueras de los congrios Conger

orbignyanus y Pseudoxenomystax albescens.

Frente Marít. 11 (A): 33-36.

FIGUEROA D. 1999. Estudio sobre la anatomía y

algunos aspectos de la biología de los congrios

que habitan el Mar Argentino y adyacencias

[PhD thesis]. Mar del Plata: Facultad de

Ciencias Exactas y Naturales, Universidad

Nacional de Mar del Plata. 108 p.

FIGUEROA DE, EHRLICH M. 2006. Systematics and

distribution of leptocephali in the western

south Atlantic. Bull Mar Sci. 78 (2): 227-242.

FLOETER J, TEMMING A. 2003. Explaining diet

composition of North Sea cod (Gadus

morhua): prey size preference vs. prey avail-

ability. Can J Fish Aquat Sci. 60: 140-150.

FROESE R. 2006. Cube law, condition factor and

weight-length relationships: history, meta-

analysis and recommendations. J Appl

Ichthyol. 22: 241-253.

GARCÍA M, JAUREGUIZAR A, PROTOGINO L. 2010.

Fish community ecology from Río de

la Plata to shelf slope. Lat Am J Aquat Res. 38

(1): 81-94.

GRIFFITHS D. 1980. Foraging costs and relative

prey size. Am Nat. 116: 743-752.

GRIFFITHS D. 2020. Foraging habitat determines

predator-prey size relationships in marine

fishes. J Fish Biol. 97 (4): 964-973.

HAIMOVICI M, BRUNETTI NE, RODHOUSE PG,

CSIRKE J, LETA RH. 1998. Illex argentinus. In:

RODHOUSE PG, DAWE EG, DOR RKO, editors.

Squid recruitment dynamics. The genus Illex

as a model, the commercial Illex species and

influence on variability. FAO Fish Tech Pap.

376. p. 27-58

HAYDEN B, PALOMARES MLD, SMITH BE, POELEN

JH. 2019. Biological and environmental driv-

ers of trophic ecology in marine fishes- a glob-

al perspective. Nat Sci Rep. 9: 11415.

HILL S, HINKE J, BERTRAND S, FRITZ L, FURNESS

R, IANELLI J, MURPHY M, OLIVEROS-RAMOS R,

PICHEGRU L, SHARP R, STILLMAN R, WRIGHT P,

RATCLIFFE N. 2020. Reference points for pred-

ators will progress ecosystem-based manage-

ment of fisheries. Fish Fish. 21 (2): 368-378.

HOOPER D, CHAPIN F, EWEL J, HECTOR A,

INCHAUSTI P, LAVOREL S, LAWTON J, LODGE D,

LOREAU M, NAEEM S, et al. 2005. Effects of

biodiversity on ecosystem functioning: a con-

sensus of current knowledge. Ecol Monogr. 75

(1): 3-35.

IRUSTA C, MACCHI G, LOUGE E, RODRIGUES K,

D’ATRI L, VILLARINO M, SANTOS B,

SIMONAZZI M. 2016. Biology and fishery of

the Argentine hake (Merluccius hubbsi). Rev

Invest Desarr Pesq. 28: 9-36.

KILLEN S, BROWN J, GAMPERL A. 2007. The effect

of prey density on foraging mode selection in

juvenile lumpfish: balancing food intake with

the metabolic cost of foraging. J Anim Ecol.

76: 814-825.

LERCARI D, VÖGLER R, VELASCO G. 2014.

Trophic models in the Southwestern Atlantic

Ocean: evaluating. Fish Cent Res Rep. 22 (3):

75 p.

LIVINGSTON R. 2003. Trophic organization in

coastal systems. Tallahassee: CRC. Florida

University. 388 p.

MACCHI G, LEONARDUZZI E, DIAZ M, RENZI M,

RODRIGUES K. 2013. Maternal effects on

fecundity and egg quality of the Patagonian

stock of Argentine hake (Merluccius hubbsi).

Fish Bull. 111 (4): 325-336.

194 MARINE AND FISHERY SCIENCES 34 (2): 181-195 (2021)

MACCHI G, MARTOS P, RETA R, DATO C. 2010.

Offshore spawning of the Argentine hake

(Merluccius hubbsi) Patagonian stock. Pan

Am J Aquat Sci. 5: 22-35.

MEYER M, SMALE M. 1991. Predation patterns of

demersal teleosts from the Cape south and

west coasts of South Africa. 2. Benthic and

epibenthic predators. S Afr J Mar Sci. 11: 409-

442.

MIHALITSIS M, BELLWOOD D. 2017. A morpholog-

ical and functional basis for maximum prey

size in piscivorous fishes. PLoS ONE:

e0184679.

[MAGYP] MINISTERIO DE AGRICULTURA,

GANADERÍA Y PESCA. 2019. [accessed 2021

February]. https://www.magyp.gob.ar/.

PIKITCH E, SANTORA C, BABCOCK E, BAKUN A,

BONFIL R, CONOVER D, DAYTON P, DOUKAKIS

P, FLUHARTY D, HENEMAN B, HOUDE E. 2004.

Ecosystem-based fishery management.

Science. 305 (5682): 346-347.

R CORE TEAM. 2019. R: a language and environ-

ment for statistical computing. R Foundation

for Statistical Computing. [accessed 2020

December]. http://www.r-project.org/index.html.

RÉME. 2007. Cefalópodos. Illex argentinus. In:

BOLTOVSKOY D, editor. Atlas de sensibilidad

ambiental de la costa y el Mar Argentino.

Ciudad Autónoma de Buenos Aires: Secretaría

de Ambiente y Desarrollo Sustentable. 5 p.

RENZI M, CASTRUCCI R. 1998. Análisis cuali-

cuantitativo de la fauna acompañante en la

pesquería de merluza (Merluccius hubbsi) al

norte de 41° S. Inf Téc Int DNI-INIDEP.

24/1998. 20 p.

REYES P. 2007. Peces abisales de la ‘Triple

Unión’, lugar de contacto de las placas

Antártica, Sudamericana y de Nazca (archi-

piélago patagónico noroccidental). Rev Biol

Mar Oceanogr. 42 (1): 37-47.

SAN MARTÍN M, BRACCINI L, CHIARAMONTE G,

PÉREZ J. 2007. Temporal and sexual effects in

the feeding ecology of the marbled sand skate

Psammobatis bergi Marini, 1932. Mar Biol.

151: 505-513.

STEPHENS D, BROWN J, YDENBERG R. 2007.

Foraging. Behavior and ecology. Chicago:

The University of Chicago Press. 608 p.

STUART-SMITH R, BATES A, LEFCHECK J, DUFFY J,

BAKER S, THOMSON R, STUART-SMITH J, HILL

N, KININMONTH S, AIROLDI L, et al. 2013.

Integrating abundance and functional traits

reveals new global hotspots of fish diversity.

Nature. 501: 539-542.

ZAR JH. 1999. Biostatistical Analysis, 4th ed.

New York: Prentice Hall. 663 p.

ZUUR A, IENO E, SMITH G. 2007. Analysing eco-

logical data. New York: Springer. 672 p.

195

BLASINA: TROPHIC ECOLOGY OF HAIRY CONGER EEL BASSANAGO ALBESCENS