ORIGINAL ARTICLE

Food preferences and rhythms of feeding activity of twoco-existing demersal fish, the longspine snipefish,Macroramphosus scolopax (Linnaeus, 1758), and theboarfish Capros aper (Linnaeus, 1758), on theMediterranean deep shelfPaolo Carpentieri1, Natalia Serpetti2, Francesco Colloca3, Alessandro Criscoli1 & GiandomenicoArdizzone1

1 Department of Environmental Biology, “La Sapienza” University of Rome, Rome, Italy

2 Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, UK

3 Istituto per l’Ambiente Marino Costiero, Consiglio Nazionale delle Ricerche (IAMC – CNR), Mazara del Vallo, Italy

Keywords

Boarfish; feeding; longspine snipefish;

Mediterranean Sea.

Correspondence

Paolo Carpentieri, Department of

Environmental Biology, “La Sapienza”

University of Rome, Viale dell’Universit�a 32,

00185 Rome, Italy.

E-mail: paolo.carpentieri@uniroma1.it

Accepted: 18 December 2014

doi: 10.1111/maec.12265

Abstract

The feeding behaviour of two potentially competing species, the longspine snipe-

fish,Macroramphosus scolopax, and the boarfish Capros aper was examined. While

both species are very abundant along the Mediterranean coast and are regularly

caught by demersal trawlers, they are of no commercial value. The diets of boar-

fish and longspine snipefish were investigated from samples collected between

January 2001 and May 2002. Variations in the diet with fish size and season, as

well as diet overlap and diversity were explored. Mysid shrimps, amphipods and

gastropods were the most important food items in the diet of longspine snipefish.

During ontogenetic development, M. scolopax occupies different trophic levels:

the diet shifts from being predominantly composed of mysids (Anchialina agilis,

Lophogaster typicus, Erythrops sp., Leptomysis spp.) in the smaller longspine snipe-

fish [<6.5 cm total length (TL)] towards decapods (Anapagurus laevis) and am-

phipods (Leucothoe incisa, Eusirus longipes, Hyperidea) in the larger individuals

(>6.5 cm TL). Crustacean decapods and copepods were the most important prey

in the stomachs of boarfish. Mysids (Lo. typicus), euphausiids and nematodes

were present in the larger individuals (>8 cm TL). A more generalist diet, still

containing copepods, crustacean decapods, gastropods (Limacina retroversa) and

a large variety of amphipods (e.g. Phtysica marina, Stenotoe bosphorana) and mys-

ids (e.g. A. agilis, Leptomysis spp., Erythrops sp.), dominated the diet of C. aper

between 2 and 8 cm TL. Diet overlap between longspine snipefish and boarfish

was very low and the differences in stomach species diversity were explained by

season and fish size.

Introduction

Interspecific competition can be one of the major factors

determining the trophic niche width of sympatric species

(Pianka 1982; Gonz�alez-Sol�ıs et al. 1997). Resource parti-

tioning between species may be indicative of the degree

of organization of animal communities, and can be

related to the concept of competition amongst species

(Gage & Tyler 1991). Both predation and prey availabil-

ity are factors that may influence inter-specific competi-

tion. However, studies on resource partitioning and prey

selection in demersal communities are limited (Colloca

et al. 2010). In the Mediterranean, these studies corre-

spond to fish from the continental slope (Macpherson

Marine Ecology (2015) 1–13 ª 2015 Blackwell Verlag GmbH 1

Marine Ecology. ISSN 0173-9565

1981) or to deep-water decapod crustaceans (Cartes

1998).

On the Mediterranean continental shelf, the longspine

snipefish, Macroramphosus scolopax, and the boarfish Ca-

pros aper are demersal species commonly co-existing on

detrital bottoms around the shelf-break (Colloca et al.

2004; Carpentieri et al. 2005). Capros scolopax is distrib-

uted in warm and temperate waters of the Mediterranean,

Atlantic and Pacific in a bathymetric range between 50

and 500 m, living mainly around 200-m depth (Fisher

et al. 1987). Capros aper is a small, planktivorous, pelagic

shoaling species with a pan-Atlantic distribution: it is

common throughout the Mediterranean and eastern

coasts of the USA (Froese & Pauly 2010). The depth

range falls between 100 and 600 m (Whitehead et al.

1986), with juveniles preferring shallow waters around

150–200 m whereas the adults go deeper (Fisher et al.

1987).

Given their usually high abundance and availability,

snipefish and boarfish are regularly caught by trawling

fleets and represent a significant fraction of the total dis-

card. Moreover, both species are likely to be food items

of many other species whose diets are not described in

the literature (Lopes et al. 2006). Most of the available

information on the two species comes from studies, con-

ducted in the Atlantic area, on their distribution and

abundance (Marques et al. 2005), biometric and genetic

characters (Zorica & Vrgoc 2005; Robalo et al. 2009), and

ecological significance and impact (Lopes et al. 2006).

The biology, growth, sexual cycle and reproduction of

snipefish and boarfish have been the subject of several

studies in different areas of the world (Brethes 1979; Bor-

ges 2000, 2001; White et al. 2011 for the Atlantic Ocean;

Assis 1993 for the Mediterranean Sea; Clarke 1984; Miya-

zaki et al. 2004 for the Western Pacific Ocean).

Although knowledge of resource partitioning and prey

selection between species may be indicative of the degree

of organization of animal communities, and can be

related to the concept of competition amongst species,

studies on these topics are limited (Macpherson 1981;

Carrass�on & Cartes 2002). The feeding behaviour of

M. scolopax and C. aper has been investigated along the

Southeast North Atlantic coast (Brethes 1979; Lopes et al.

2006; Emma et al. 2011) and along the Australian coast

(Clarke 1984; Fock et al. 2002). In the Mediterranean

area, notwithstanding the increasing interest in trophic

ecology and energy transfer through food webs, the feed-

ing periodicities of these two species have been poorly

investigated to date. Information on their food consump-

tion is scarce and fragmentary, and is limited in spatial

and temporal coverage (Macpherson 1979; Matallanas

1982). Moreover, there is no information on the trophic

overlap between these two abundant and co-existing

species. Such information may help to elucidate the roles

that they play within the Mediterranean ecosystem.

Therefore, in the present study, we investigated the tro-

phic ecology of boarfish and longspine snipefish in an

area of the Central Mediterranean Sea with the specific

objectives of (i) describing the activity rhythms and the

feeding habits of M. scolopax and C. aper according to

body size; (ii) providing information on their daily and

seasonal feeding behaviour; (iii) analysing their dietary

overlap and the inter-specific relationships between these

two species.

Methods

The study area is located off the central western coasts of

Italy, covering 13,404 km2 between 20 and 700 m depth

(outer boundaries: latitude 40°52, longitude 13°23; lati-tude 42°20, longitude 11°16; Fig. 1). Most of the samples

were collected between 100 and 200 m depth. This bathy-

metric range, representing a large part of the continental

shelf (generally around 120–160 m deep and 15–30 km

from the shoreline), is characterized by sand–muddy bot-

toms (VTC benthic assemblage – P�er�es & Picard 1964),

muddy bottoms (VTC, coastal terrigenous muds) and by

detrital sediments, with the occurrence of high concentra-

tions of suspensivors organisms, primarily the crinoid

Leptometra phalangium, which can reach densities up to

15 individuals�m�2 on the shelf-break (Colloca et al.

2004).

Size-stratified samples of Macroramphosus scolopax and

Capros aper were collected monthly, over a period of

18 months from January 2001 to June 2002, on board

commercial bottom trawlers and during two experimental

trawl surveys, namely the MEDITS and GRUND projects

(Relini & Piccinetti 1996; Bertrand et al. 2002), conducted

in early summer and autumn, respectively (Table 1).

All hauls were carried out with a commercial otter

trawl vessel, equipped with a cod-end bag liner of 40-mm

stretched mesh size. The towing speed of the vessel was

about 3 knots and each trawl haul covered a distance of

approximately 2.5 km. Moreover, to analyse the diel

movements and seasonal changes, during July and

November 2001 and March and May 2002, eight daily

hauls per season of 30 min each were performed every

3 h at a depth of 140–160 m throughout a 24-h period

to cover and to investigate the entire diel cycle.

Caught fish, kept on ice and subsequently frozen to

prevent digestion, were taken to the laboratory, measured

(total length, TL) to the nearest 1 mm, and weighed to

the nearest 0.01 g. Stomachs were removed and their

contents weighed to the nearest 0.001 g. In order to sepa-

rate immature from mature specimens, sex and maturity

stage were also recorded. Maturity state was determined

2 Marine Ecology (2015) 1–13 ª 2015 Blackwell Verlag GmbH

Feeding activity of M. scolopax and C. aper Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone

by macroscopic analysis of the gonads using the maturity

scale for partial spawners (Holden & Raitt 1974).

Prey items were identified and sorted out into taxo-

nomic groups down to the species level whenever possible.

When the state of digestion was more advanced, prey

items were checked and grouped into unidentified groups

(e.g. Isopoda n.i. and Decapoda n.i.). The degree of diges-

tion of the prey was not considered in the analysis. Empty

stomachs and those with partially everted or unidentified

contents were excluded from the total sample.

With the exception of the largest individuals (grouped

into two heterogeneous length classes), all samples for

both M. scolopax (Table 2) and C. aper (Table 2) were

grouped into four length classes. Size limits were chosen

in order to roughly separate immature (the first size group

corresponding to juveniles) from maturing and mature

specimens. For both species, the study of size-related diet

variations was based on the identified size groups.

The contribution of each food item to the diet of these

fish size groups was evaluated using the index of relative

importance (IRI, Pinkas et al. 1971) as modified by

Hacunda (1981):

IRI ¼ FðNþWÞ: (1)

where F = frequencyof observation index, N = numeric

index, W = gravimetric index

This index, expressed as:

IRI ¼ IRI�RIRI � 100; (2)

incorporates the percentage by number (N), wet weight

(CW) and frequency of occurrence (F) (Hyslop 1980).

Hierarchical cluster analysis and non-metric multidi-

mensional scaling (nMDS) based on Bray–Curtis simi-

larity and on the IRI% were used for classification and

ordination of fish size groups (Clarke & Warwich

1994).

Dietary overlap was estimated using the Morisitia–Horn index, which has been found to give a lower bias

Table 1. Number of stomach contents collected during the different trawl survey periods. For each period the values of stomach fullness (FI) are

reported.

full stomachs empty stomachs FI

Capros aper

Macroramphosus

scolopax Capros aper

Macroramphosus

scolopax Capros aper

Macroramphosus

scolopax

MEDITS survey 169 257 54 133 0.76 0.66

GRUND survey 79 337 161 262 0.33 0.56

summer 2001 37 263 40 125 0.48 0.68

autumn 2001 18 129 37 451 0.33 0.22

winter 2002 55 189 34 281 0.62 0.40

spring 2002 76 124 138 395 0.36 0.24

total 434 1299 464 1647 0.48 0.44

Fig. 1. Map of the research area.

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Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone Feeding activity of M. scolopax and C. aper

Table 2. Prey items, reported as frequency of occurrence (F%) and weight (Cw%), for the four identified size groups (A, B, C and D) in the diet

of (a) Macroramphosus scolopax and (b) Capros aper. For each size group the number of stomachs examined is reported.

size group A B C D

(a)

length (cm) 4.0–6.5 6.6–8.4 8.5–11 >11

no. stomachs 693 1030 889 334

indexes F% Cw% F% Cw% F% Cw% F% Cw%

Foraminifera

Foraminifera n.i. 0.2 0.55 13.4 0.05 13 0.02 8.24 0.02

Hydrozoa

Idrozoa n.i. 6.59 0.64 7.54 0.34 2.24 0.06

Nematoda

Nematoda n.i. 1.55 0.06 1.74 0.1 2.24 0.06 2.35 0.01

Polychaeta

Polichaeta n.i. 0.78 0.08 0.97 0.16 0.45 0.02 2.35 0.62

Gasteropoda

Alvania testae 1.19 0.003 1.12 0.09 1.18 0.03

Anatoma crispata 0.22 0.002 3.53 1.71

Cavolinia inflexa 0.22 0.01

Clelandella miliaris

Eulimidae n.i. 5.43 0.92 8.12 0.94 7.62 0.37 1.18 0.08

Limacina retroversa 1.94 0.55 7.35 9.41 20.2 1.01 3.53 2.12

Bivalvia

Neoleptonidae n.i. 4.65 0.15 3.48 0.17 3.81 0.08 1.18 0.002

Pycnoganida

Pycnoganida n.i. 0.19 0.003

Copepoda

Copepoda n.i. 3.49 0.11 3.68 1.22 3.59 0.07

Ostracoda

Ostracoda n.i. 8.91 0.28 5.61 0.27 5.16 0.08 2.35 0.04

Mysidacea

Anchialina agilis 57.7 79.18 24 34.62 33.7 36.62 37.7 25.48

Lophogaster typicus 4.26 1.66 6.38 3.72 15.5 4.14 24.7 8.17

Leptomysis gracilis 5.04 2.5 2.13 3.38

Leptomysis spp. 14.3 3.16 10.6 8.33 9.42 9.45 14.1 9

Erythrops spp. 17.1 2.32 12.4 11.69 13.5 3.36 5.88 0.41

Gastrosaccus spp. 0.39 0.05 0.39 0.03 0.67 0.02

Siriella sp. 1.16 0.23 0.69 0.07 0.67 0.08 1.18 0.03

Misidacea n.i. 1.94 0.53 1.74 0.93 3.36 0.38

Tanaidacea

Tanaidacea n.i. 1.55 0.02 1.57 0.01

Cumacea

Campylapsis glabra 1.55 0.01 2.32 0.15 2.02 0.02

Cumacea n.i. 0.19 0.003 0.67 0.08 1.18 0.02

Isopoda

Gnathia sp. 15.1 0.35 9.86 0.39 6.73 0.19 3.53 0.02

Desmosomatida 1.16 0.01 0.77 0.02 1.57 0.03

Isopoda n.i. 0.78 0.01 1.16 0.08 2.91 0.18 1.18 0.03

Amphipoda

Hyperidea n.i. 4.06 8.48 10.5 21.26 18.8 16.86

Ampelisca spp. 0.58 0.04

Harpinia spp. 0.39 0.01

Caprellidae n.i. 0.19 0.003

Phtysica marina 1.16 0.05 1.12 0.03

Pedoculina bacescui 0.19 0.01

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Feeding activity of M. scolopax and C. aper Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone

Table 2. Continued

indexes F% Cw% F% Cw% F% Cw% F% Cw%

Epimeria cornigera 0.45 0.04 1.18 0.07

Eusirus longipes 1.16 0.06 0.22 0.03

Stegocephaloides crystianiensis 1.16 0.01 0.97 0.04 0.22 0.02

Lembos spp. 1.35 0.15 1.35 0.04

Leucothoe incisa 3.48 0.51 1.18 0.01

Stenotoe bosphorana 2.33 0.18 0.19 0.003 1.57 0.08 1.18 0.08

Westwoodilla rectirostris 1.18 0.04

Rachotropis glabra 0.39 0.01 0.9 0.19

Monoculodes spp. 0.19 0.01 1.18 0.01

Oediceratidae 0.19 0.003 0.67 0.07 1.18 0.11

Orchomene spp. 0.19 0.01 0.22 0.001

Synchelidium haplocheles 0.19 0.02 0.22 0.01

Amphipoda n.i. 10.9 0.75 13.2 8.4 16.2 8.61 14.1 15.5

Decapoda

Anapagurus laevis 0.39 0.13 2.71 0.53 6.95 1.7 9.51 5.5

Decapoda n.i. 8.14 4.95 9.28 4.52 11.9 9.94 9.41 7.93

Bryozoa

Bryozoa n.i. 1.55 0.07 2.71 0.45 2.47 0.06

Crinoidea

Leptometra phalangium 5.04 0.43 1.37 0.07 3.36 0.62 4.71 0.96

Ophiuroidea

Amphiura n.i. 0.19 0.01 0.22 0.02 2.35 0.5

Ophiuroidea n.i. 4.71 4.64

Teleostea

Teleostea n.i. 0.39 0.12 0.97 0.523 0.9 0.85 1.18 0.0004

size group A B C D

(b)

length (cm) 2.4–4.5 4.6–6.4 6.5–8 >8

no. stomachs 245 477 109 67

indexes F% Cw% F% Cw% F% Cw% F% Cw%

Foraminifera

Foraminifera n.i. 0.60 0.29 2.33 0.76

Hydrozoa

Hydrozoa n.i. 10.19 11.61 10.84 5.57 5.00 3.56 6.98 10.65

Nematoda

Nematoda n.i. 1.85 0.01 1.25 9.30 0.37

Polychaeta

Polychaeta n.i. 2.78 0.10 4.22 1.21 11.25 3.09 2.33 0.76

Gasteropoda

Eulimidae n.i. 1.85 0.06 5.12 1.70 6.25 2.37

Limacina retroversa 0.93 0.01 4.22 2.33 1.25 0.01

Bivalvia

Neoleptonidae n.i. 0.93 0.01 1.25 0.01

Pycnoganida

Pycnoganida n.i. 0.90 0.06 1.25 0.14

Copepoda

Copepoda n.i. 27.78 2.78 28.92 2.27 40.00 3.02 11.63 0.94

Ostracoda

Ostracoda n.i. 0.93 0.50 3.31 0.85 2.50 0.01

Mysidacea

Anchialina agilis 4.63 5.33 3.31 4.04 1.25 0.01

Lophogaster typicus 1.51 0.91 1.25 0.61 13.95 33.14

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Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone Feeding activity of M. scolopax and C. aper

compared with other indices of overlap (Ricklefs & Lau

1980; Smith & Zaret 1982).

This index was calculated as follows:

Chj ¼ 2ðRphk:pjkÞðRp2hk:p2jkÞ�1; (3)

where Chj is the similarity between the predator species h

and j, and phk and pjk are measures of the use of resource

k by the predators h and j. Dietary overlap ranges from 0

to 1, and is generally considered to be biologically

significant when it exceeds 0.60 (Keast 1977; Wallace

1981). An overlap greater than 0.6 can be considered as

30 indicative of competition in situations of resource lim-

itation. By contrast, values lower than 0.5 may indicate

the absence of competition (McArthur & Levins 1967;

Zaret & Rand 1971). Input data for overlap calculations

were based on F%.

The diel feeding periodicity was investigated by means

of the stomach fullness index (FI), expressed as the ratio

of the weight of a fish’s stomach contents to its total

Table 2. Continued

indexes F% Cw% F% Cw% F% Cw% F% Cw%

Leptomysis gracilis 0.93 0.85 2.11 1.19

Leptomysis sp. 0.60 0.24 1.25 0.01

Erythrops sp. 1.51 0.99 2.50 0.25

Gastrosaccus sp. 0.93 0.82 0.30 0.39

Siriella sp. 0.30 0.13

Boreomysis megalops 1.25 2.51

Misidacea n.i. 2.11 2.11 1.25 2.23 2.33 2.64

Tanaidacea

Tanaidacea n.i. 14.81 0.07 19.88 0.16 7.50 0.06

Isopoda

Gnathia sp. 18.52 1.19 23.80 3.99 23.75 1.05 2.33 0.90

Desmosomatida n.i. 0.30

Isopoda n.i. 4.63 0.10 4.82 1.08 5.00 0.33

Amphipoda

Harpinia sp. 0.93 0.04 0.90

Hyperidea n.i. 2.71 16.62 6.25 16.02 4.65 10.78

Caprellidae n.i. 10.19 0.89 10.54 0.68 2.50 0.11

Phtysica marina 3.70 0.34 8.43 1.21 3.75 0.12

Palvipalpus linea 0.90 0.04

Pedoculina bacescui 0.60 0.01

Paraphoxus oculatus 1.85 0.04

Epimeria cornigera 3.70 4.40 4.82 3.61 5.00 11.45

Eusirius longipes 1.25 0.28

Stegocephaloides crystianiensis 0.30 0.13 3.75 0.10

Nicippe tumida 0.60 0.03

Rhachotropis grimaldii 2.50 0.11

Stenotoe bosphorana 2.68 0.09 7.23 0.70 3.75 0.26

Tryphosites longipes 0.30 0.10

Trischizostoma nicaeense 2.50 0.79 9.30 1.77

Oediceratidae n.i. 0.30

Amphipoda n.i. 6.49 4.16 9.34 8.48 10.00 3.03 2.33 0.04

Euphasiacea

Euphasiacea n.i. 4.82 3.35 13.75 7.72 18.60 13.91

Decapoda

Anapagurus laevis 8.50 5.64 0.30 0.24

Megalopa larvae 0.93 0.03 1.51 0.03 1.25 0.04

Decapoda n.i. 31.85 60.74 30.24 35.04 33.80 40.18 21.16 23.33

Crinoidea

Leptometra phalangium 1.51 0.20 2.50 0.48

Ophiuroidea

Amphiura sp. 1.25 0.03

Teleostea

Teleostea n.i. 0.93 0.16 4.82 0.01 1.25 0.01 2.33 0.01

n.i., not identified.

6 Marine Ecology (2015) 1–13 ª 2015 Blackwell Verlag GmbH

Feeding activity of M. scolopax and C. aper Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone

body weight (FI = Ws/Wt) (Tudela & Palomera 1995;

Benli et al. 2001).

One-way analysis of variance was used to assess the

differences between the stomach fullness index (FI) and

light intensity. The differences were considered significant

at P < 0.05. The average values of light intensity for each

time period were obtained from the data collected at

Anzio (latitude 41°26, longitude 12°37) by the Italian

Ministry of Agricultural and Forestry Policy (MIPAAF)

during the study period.

Results

Diet composition

A total of 2946 specimens of Macroramphosus scolopax,

mean standard length 8.13 cm (range: 4–18.5 cm TL)

and mean weight 5.26 g (range: 0.5–23.7 g) was collected

for diet analysis (Fig. 2a).

Amongst the 54 food items (Fig. 3a), belonging to 19

major groups, mysids were the most important prey (80.1

IRI%) for this species. Amphipods (8.12 IRI%), gastropods

(6.7 IRI%) and decapods (2.9 IRI%) represented secondary

prey items. The dietary patterns of M. scolopax showed

marked differences amongst seasons, mainly linked to the

high occurrence of mysids during the summer and spring

period, and of gastropods and amphipods in autumn and

winter, respectively (Fig. 3b).

The stomach contents of 898 individuals of Capros

aper, mean standard length 5.1 cm (range: 2.5–13.5 cm

TL) and mean weight 3.92 g (range: 0.5–16.4 g), were

analysed (Fig. 2b). For the boarfish, amongst the 47 dif-

ferent food items (Fig. 4a), belonging to 18 major groups,

copepods (34.5 IRI%) and decapods (24.3 IRI%) were

the most abundant prey. Isopods (8.5 IRI%), amphipods

(8.4 IRI%), mysids (7.7 IRI%) and euphausiids (6.7 IRI

%) represented secondary prey items. Tanaids (2.96 IRI

%), hydrozoans (2.4 IRI%), gastropods (2.1 IRI%) and

nematodes (2%) occurred in the diet of C. aper at lower

frequencies. Seasonal analysis showed that decapods were

present throughout the year in the stomachs of C. aper,

with an increase during spring and summer (Fig. 4b).

The importance of gastropods greatly increased in

autumn, whereas copepods and amphipods showed only

slight seasonal differences.

Ontogenetic development and dietary overlap

Cluster and nMDS analyses (stress = 0.02) based on the

IRI% allowed the identification of two cluster groups

a

b

Fig. 2. Relationships amongst abundance

(expressed as number of individuals per

hour), mean fish length, and depth (m).

a) M. scolopax b) C. aper.

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Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone Feeding activity of M. scolopax and C. aper

below 45% similarity, separated firstly along a species gra-

dient and thereafter along a specific size gradient (Fig. 5a).

The first branch is formed by longspine snipefish speci-

mens (Groups A and B), whereas the second branch, subdi-

vided into three other groups (Groups C, D and E), is

composed of different size classes of boarfish.

Group A contained longspine snipefish between 4 and

6.5 cm TL. The mysid Anchialina agilis (94.3 IRI%) almost

entirely dominated the diet of this group (Fig. 5b).

Group B, characterized by longspine snipefish longer

than 6.5 cm, showed a more heterogeneous diet, still

characterized by a high occurrence of the mysid A. agilis

(59.8 IRI%), but with Lophogaster typicus (3.7 IRI%),

Leptomysis spp. (5.8 IRI%) and Erythrops spp. (4.7 IRI%)

also recorded. The gastropod Limacina retroversa (8.3 IRI

%) and different amphipods (mostly hyperiids and the

species Leucothoe incisa) greatly increased in the diet of

this group, accounting for 20% of its diet.

Copepods (46 IRI%) and tanaids (around 5 IRI%) rep-

resented the main prey items for boarfish in Group C

(<4.5 cm TL). In Group D, boarfish specimens between

4.5 and 8 cm TL, the diet is still characterized by a high

occurrence of copepods (around 42 IRI%), but also with

a considerable amount of the isopod Gnathia sp. (12.2

IRI%).

In Group E (boarfish >8 cm TL), the mysid Lo. typicus

(27.3 IRI%), euphausiids (22.8 IRI%), nematodes (8.7

IRI%), hyperiids (5.2 IRI%) and the amphipod Trischi-

zostoma nicaeense (3.3 IRI%) were recorded. Decapods

were present at a high frequency in the diet of all of the

boarfish cluster groups (from Group C to Group E).

Considering all of the specimens examined, the results

showed a low overlap level (Chj > 0.55) between M. scol-

opax and C. aper. The seasonal variation pattern showed

the highest value of trophic overlap (Chj > 0.60) during

the autumn period, when gastropods dominated the diet

of both species. The lowest overlaps were recorded in

spring (Chj > 0.03) and summer (Chj > 0.16). In winter,

the slight increase in trophic overlap (Chj > 0.49) was

because of the presence of amphipods in the stomach

contents of both species.

Diel activity

The most intensive feeding period of both species was

observed to be at 15:00 h according to the calculated FI

a

b

Fig. 3. (a): Prey items of Macroramphosus

scolopax reported as index of relative

importance (IRI%); (b): seasonal variations of

the main food items in the diet.

8 Marine Ecology (2015) 1–13 ª 2015 Blackwell Verlag GmbH

Feeding activity of M. scolopax and C. aper Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone

values (Fig. 6). Diel activity displayed a clear trend for

Macroramphosus scolopax: feeding was concentrated in

daylight, generally from 08:00 to 18:00 h (r: 0.60;

P < 0.01). Following sunset, feeding intensity began to

decrease, showing a positive correlation with night-hauls

(r: 0.88; P < 0.01). During the night, almost all of the

stomachs were observed to be completely empty.

Similar findings were obtained for Capros aper: the

boarfish was an active diurnal feeder from dawn until

dusk. Feeding was concentrated mainly from sunrise

(from 05:00 and 08:00 h) to late afternoon (18:00 h),

with a slight decline just before sunset (Fig. 6). The sam-

ples caught during the night hours (from 21:00 to

05:00 h) showed a significant decline in feeding activity

(P < 0.01).

Discussion

Macroramphosus scolopax and Capros aper are eurypha-

gous fish. The low dietary overlap values generally

recorded imply high resource partitioning. During its

growth, the longspine snipefish showed a trophic behav-

iour shifting from a homogeneous diet, dominated by

mysids (Anchialina agilis), to a heterogeneous diet charac-

terized by mysids, amphipods and gastropods.

Crustacean decapods and copepods were the most

important prey in the stomachs of C. aper. The boarfish

showed a change in feeding activity that probably reflects

its ontogenetic bathymetry shift, with the adults living in

deeper waters (Fisher et al. 1987). Amphipods were con-

sistently present in all size classes, but a difference in the

composition of this taxon between juveniles and adults

was detected: the juveniles fed predominantly on amphi-

pods of the family Caprellidae (Phtysica marina and Palv-

ipalpus linea) whereas the adults fed mostly on larger

amphipods of the family Hyperidea and on the species

Epimeria cornigera.

The degree to which prey species contributed to the

diets of snipefish and boarfish also showed differences

across seasons. In the present study, it is clear that during

a

b

Fig. 4. (a): Prey items of Capros aper

reported as index of relative importance (IRI

%); (b): seasonal variations of the main food

items in the diet.

Marine Ecology (2015) 1–13 ª 2015 Blackwell Verlag GmbH 9

Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone Feeding activity of M. scolopax and C. aper

summer and spring, when there is higher prey species

availability, M. scolopax and C. aper fed on different spe-

cies, perhaps because of active selection of prey. In spring

and summer, crustacean decapods were the main prey

items for boarfish whereas in the longspine snipefish

stomachs, a high occurrence of mysids was observed.

Decapods were present in the M. scolopax diet through-

out the year without any significant variations. In winter,

when amphipods dominated the diet of longspine snipe-

fish, boarfish fed on a great variety of taxa such as cope-

pods, amphipods and decapods. High concentrations of

copepods were recorded in the diet of boarfish during

spring and winter. In autumn both species, M. scolopax

and C. aper, concentrated on different species of gastro-

pods. The presence of these prey in the diets of M. scol-

opax and C. aper reflects the ecology of the zooplankton

in the studied area (Franqueville 1971). The peak of co-

pepods in the stomachs of boarfish is in agreement with

the seasonal cycles of this group. Vives (1978) found the

a

b

Fig. 5. Dendrogram (a) and non-metric

multidimensional scaling (nMDS) plot (b)

based on the index of relative importance (IRI

%) values (a): The two groups defined at an

arbitrary similarity level of 45% are indicated

(dotted line). (b): nMDS showing the

ordination of Macroramphosus scolopax

(Mac) and Capros aper (Cap) into size classes

with similar diets (the details of each size

class are explained in the text).

Fig. 6. Relationship between time and stomach fullness index (FI;

ratio of the weight of a fish’s stomach contents to its total body

weight) for Macroramphosus scolopax and Capros aper. Hauls were

pooled into 2-h time steps according to the time of the day. Error

bars in the figure represent the standard error.

10 Marine Ecology (2015) 1–13 ª 2015 Blackwell Verlag GmbH

Feeding activity of M. scolopax and C. aper Carpentieri, Serpetti, Colloca, Criscoli & Ardizzone

maximum abundance of copepods on the Mediterranean

platform (100–200 m depth) to be during late winter and

early spring. In the Western Mediterranean, mysid abun-

dance reaches a maximum in late spring–summer

(Franqueville 1971; Sardou et al. 1996), which coincides

with the period of higher consumption by juveniles of

M. scolopax in the present study.

Light intensity also seemed to positively affect the feed-

ing behaviour of M. scolopax and C. aper. Both species

showed a marked daily temporal pattern, with a major

peak in feeding occurring during daylight and a decline just

before sunset. This diel cycle was found in all samples taken

and may be linked with the biology of both species:

remaining close to the bottom and resting during the night,

and feeding during daylight on the pelagic-benthic inverte-

brates that constitute the hyperbenthos (Mees & Jones

1997). In the study area, the hyperbenthos consists almost

entirely of crustaceans (mysids, euphausiids, amphipods

and decapods – Colloca et al. 2010), which make extensive

vertical migrations during the night, before returning to

the bottom by day (Franqueville 1971; Macquart-Moulin

1984; Macquart-Moulin & Ribera Maycas 1995).

Given the scant information available on the feeding

activity of M. scolopax and C. aper in the Mediterranean,

it is difficult to compare our results with those from

other areas. Along the Catalan coast, Matallanas (1982)

reported longspine snipefish to be almost exclusively

benthic feeders. The diet of adult M. scolopax was

mainly composed of the decapod Anapagurus laevis

(Paguridae), whereas polychaetes and amphipods were

the preferential prey for smaller individuals. These find-

ings are slightly different from our results in which mys-

ids accounted for more than 50% of the diet of

M. scolopax. Regarding the feeding habits of C. aper, in

a study conducted on the southern coast of Portugal

(Santos & Borges 2001), the euphausiid Meganyctiphanes

norvegica and hyperiid amphipods were the main prey

items. In the Western Mediterranean area, in addition to

copepods, Macpherson (1979) mentioned that the diet

of C. aper consisted largely of euphausiids and, with less

frequency, other crustaceans, fishes, polychaetes, molluscs

and hydrozoans.

This study contributes to the elucidation of the trophic

behaviour and inter-specific relationships of M. scolopax

and C. aper, two poorly studied, small-sized demersal

teleostean in the Central Mediterranean Sea. Our results

suggest that these two species, occupying the same habitat

and having the potential to prey upon the same species

at least during part of their life cycle, exhibit differences

in diet breadth and diet overlap. The distributions of

boarfish and longspine snipefish overlap on the Mediter-

ranean coast, reaching their highest densities around

the shelf-break (Colloca et al. 2010), although boarfish

seem to have a wider depth distribution than snipefish

(Busalacchi et al. 2010). Although the two species spa-

tially and temporally overlap, dietary overlap, as reflected

by Morisita-Horn index, was relatively low, suggesting

that food resources were well partitioned for these co-

existing species. It is well known that co-existence in the

same community for species with similar trophic habits

and narrow niches may be facilitated through differences

between species in the use of food resources (Shoener

1983; Ross 1986). Such differences may reduce direct

food competition, allowing the co-existence of M. scolop-

ax and C. aper. Other studies (Cartes 1998; Carrass�on &

Cartes 2002) on prey selection and resource partitioning

found that high overlap values between species were

uncommon in marine fish and decapod communities,

indicating that on the whole species do partition the

available resources. Prey abundance has been reported as

the main reason influencing diet composition of general-

ist and opportunistic feeders (Cabral et al. 2002). Our

findings also show that the main differences for both

species were mainly linked to an ontogenetic shift of their

diets. Obviously, the best indices are obtained from sam-

ple sizes that are as large as possible. Thus, the data

acquired here represent only the first step in ecological

studies of C. aper and M. scolopax. It will also be impor-

tant to analyse the influence that these two species, very

common on the Mediterranean continental shelf and

upper slope (between 150 and 500 m), exert on the

whole demersal fish assemblage (i.e. inter-/intra-specific

interactions).

Acknowledgements

I would like to thank the crew of the fishing trawler “Lib-

era” (particularly the captain Salvatore Azzolini) and the

PhD students of the Department of Environmental Biol-

ogy, “La Sapienza” University of Rome, for their help in

the stomach contents identification.

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