Identification of Potential Essential Fish Habitats for Skates Basedon Fishers’ Knowledge

Barbara Serra-Pereira • Karim Erzini •

Catarina Maia • Ivone Figueiredo

Received: 18 April 2013 / Accepted: 17 February 2014

� Springer Science+Business Media New York 2014

Abstract Understanding of spatio-temporal patterns of

sensitive fish species such as skates (Rajidae) is essential

for implementation of conservation measures. With insuf-

ficient survey data available for these species in Portuguese

Continental waters, this study shows that fishery-dependent

data associated with fishers’ knowledge can be used to

identify potential Essential Fish Habitats (EFH) for seven

skate species. Sites with similar geomorphology were

associated with the occurrence of juveniles and/or adults of

the same group of species. For example, sites deeper than

100 m with soft sediment include predominantly adults of

Raja clavata, and are the habitat for egg deposition of this

species. Raja undulata and R. microocellata are the more

coastal species, preferring sand or gravel habitats, while

coastal areas with rocks and sand seabed are potential

nursery areas for R. brachyura, R. montagui and R. clavata.

The main output of this study is the identification of

preferential fishing sites enclosing potential EFH for some

species, associated with egg-laying and nursery grounds.

The location of these areas will be considered for future

seasonal closures, and studies will be conducted to evaluate

the biological and socio-economic impacts of such mea-

sures. As in the past, fishermen will collaborate in the

process of evaluating those impacts, since they have

practical and applied knowledge that is extremely valuable

for evaluating the advantages and disadvantages of such

closures. In conclusion, this study is a first contribution to

the understanding and identification of EFH for skate

species, associated with nursery and egg deposition sites,

with direct application to management.

Keywords CCA � Sediment � Nursery � Rajidae �Portugal � Essential Fish Habitats (EFH)

Introduction

Elasmobranchs have suffered worldwide reductions in

abundance (Clarke 2009). Globally, conservation measures

have been adopted even for regions where information is

scarce and the status of some elasmobranch populations is

uncertain. These concerns are a direct consequence of their

low resilience to fishing, which derives from their life

history characteristics, such as late maturity, low fecundity

and requirement for specific areas for spawning and nurs-

eries (Rodrıguez-Cabello et al. 2004; Hunter et al. 2006).

To guarantee the sustainability of elasmobranch popula-

tions and the maintenance of biodiversity it is necessary to

significantly improve knowledge of their biology, the

temporal and spatial population structure and the intra- and

inter-specific relationships.

Demersal elasmobranchs belonging to Rajidae (rays and

skates) are known to have limited, well-defined distribu-

tions and low motility (Carrier et al. 2004). Most species

live close to shore, generally at depths\100 m (Stehmann

and Burkel 1984; Compagno et al. 2005). Mark-recapture

Electronic supplementary material The online version of thisarticle (doi:10.1007/s00267-014-0257-3) contains supplementarymaterial, which is available to authorized users.

B. Serra-Pereira (&) � C. Maia � I. Figueiredo

Divisao de Modelacao e Gestao de Recursos da Pesca,

Departamento do Mar e Recursos Marinhos, Instituto Portugues

do Mar e da Atmosfera (IPMA), Av. Brasılia, 1449-006 Lisbon,

Portugal

e-mail: bpereira@ipma.pt

K. Erzini

Centro de Ciencias do Mar (CCMAR), Faculdade de Ciencias e

Tecnologia (FCT), Ed. 7, Universidade do Algarve, Campus de

Gambelas, 8005-139 Faro, Portugal

123

Environmental Management

DOI 10.1007/s00267-014-0257-3

studies suggest that species live in local concentrations

with regular exchange of individuals (Walker 1999),

through movements of generally \60 km (e.g. Walker

et al. 1997; Rodrıguez-Cabello et al. 2004; King and

McFarlane 2010). Sexual segregation, implying differences

between sexes in behavioral strategy and habitat selection

is another general characteristic of skate populations

(Wearmouth and Sims 2008). Skates can also undergo

seasonal migrations towards spawning grounds that are

generally located closer to shore (Hunter et al. 2006) and

even into estuaries, where juveniles seem to remain after

birth (e.g. Prista et al. 2003; Moura et al. 2007). The for-

aging behavior of skates is strongly related with the nature

of the seabed of their habitat, since they prey mostly on

benthic species (e.g. Farias et al. 2006; Moura et al. 2008).

These specific areas for spawning, nursery and feeding that

are essential for the survival of the species are named

‘Essential Fish Habitats—EFH’ (e.g. Bergmann et al.

2004).

In the absence of reliable survey data on elasmobranch

species distribution and relative abundance, fishers’

knowledge can be essential to understand their dynamics.

For this reason, the importance of collaboration between

scientists and the fishermen has been increasingly recog-

nized (Bergmann et al. 2004; Mathew 2011). Although

sometimes undervalued, fishers’ knowledge has proven to

be very precise and helpful for fisheries management,

providing valuable information on fish species biodiversity,

catches, ecology and preferred habitats, stock structure,

interannual variability in stock abundance, migrations,

behavior of larval/post-larval fish, currents and the nature

of island wakes, spawning aggregations and locations, local

trends in abundance and local extinctions (Johannes and

Neis 2007; Rochet et al. 2008). Fishers’ knowledge has

even been officially acknowledged by the Code of Conduct

for Responsible Fisheries (FAO 2009), which recognizes

its use in decision-making in conservation, management

and development of fisheries, especially in the case of

small-scale fisheries. Fishers’ knowledge has been widely

applied across the globe, for example to evaluate changes

in species abundance in the English Channel (Rochet et al.

2008), to understand habitat use and trophic interactions of

coastal fishes in Brazil (Silvano and Begossi 2012), to

identify spawning migrations of Australian fishes (Johan-

nes and Neis 2007) and to identify cod and haddock

spawning areas in the Gulf of Maine (Johannes and Neis

2007). Following the successful use of fishers’ knowledge

in the above mentioned studies, the present work aims to

demonstrate the use of fishers’ knowledge to better

understand the distribution patterns of demersal elasmo-

branchs, like rays and skates, in central Portugal through

the identification, mapping and characterization of prefer-

ential fishing sites (PFS), and to contribute to the

identification of sensitive areas that could be linked to EFH

based on the aggregation of juveniles and adult breeders.

Material and Methods

Data were collected in 2010 and 2011 from vessels

belonging to the polyvalent or multi-gear fleet, with overall

vessel lengths between 5 and 19 m, landing skates in the

port of Peniche. Peniche was selected because it is the port

with the highest landings of skates in mainland Portugal

(Machado et al. 2004). As rays and skates are not the target

species of this fleet, catches are therefore suitable for

providing information on sites of different levels of abun-

dance of the different rays and skates species. The fishing

activity of the selected vessels took place in central Por-

tugal, from Nazare (up to 39.7�N latitude) to Cabo da Roca

(down to 38.7�N latitude), and from near shore (about

0.5 nmi) to 30–35 nmi W (around 10.0�W longitude)

(Fig. 1).

Data were collected through: (i) a combination of

questionnaire-based interviews coupled with sampling of

the landings; and (ii) self-interviews. For the first data

source, fishing trips with skate’s landings were selected;

and landed weights and size frequencies by sex were

recorded for all skates, as along with the landed weight of

each accompanying species, information about the fishing

gears used (type, mesh/hook size), fishing effort (fishing

time and number of nets or hooks), fishing ground location

(name of the fishing ground and geographical coordinates)

and depth. The self-interviews data were collected in col-

laboration with a Portuguese Artisanal Fishermen’s Asso-

ciation (CAPA). The fisherman filled out a questionnaire

similar and comparable to that used in interviews, i.e. for

each fishing trip in which they caught skates they needed to

register the following information: skates total landed

weight, identification and characterization of the fishing

gears used, fishing effort, fishing ground location (geo-

graphical coordinates) and depth. A close collaboration

with CAPA guaranteed the reliability of the data collected

and the fishermen were all informed about the objective of

the interviews. CAPA also promoted the self-interviews

used in this study. The landed weight for the remaining

landed commercial species from each of the trips was

provided afterwards by the Portuguese Directorate-General

for Natural Resources, Security and Maritime Services

(DGRM).

Due to data constraints (i.e. limited or incomplete data

by trip), a regular grid was applied, and spatial data were

converted to area data, i.e. 100 rectangular spatial units

with approximately 28 nmi2 (squares of 0.1� latitude and

0.1� longitude). Of these 100 spatial units, only 74 corre-

spond to sea area (Fig. 1).

Environmental Management

123

To characterize EFHs, it is essential to have knowledge

on the nature of the seabed of a given area, since its main

features determine the fauna and flora communities. Due to

its importance also for fisheries, fishermen typically have

knowledge on the types of seabed of the fishing sites that is

passed from generation to generation (Souto 1991). The

information on the sea geomorphology for the fishing area,

was gathered from fishermen (through interviews), historic

Fig. 1 Study area (bold rectangle) and geographical localization of

the samples collected by interviews and self-interviews. The shaded

rectangles represent preferential fishing sites grouped into four spatial

groups according to the constrained correspondence analysis (g1, g2,

g3 and g4)

Environmental Management

123

records (e.g. Silva 1889; Boavida 1948; Vanney and Mo-

ugenot 1981) and nautical charts of the area (Instituto

Hidrografico 1978, 1983).

Data Analysis

Data were georeferenced and visualized using ArcGIS 9.2

(ESRI 2006).

The collected information on the location of each fish-

ing trip was used to identify the main fishing units where

the artisanal fishing vessels from Peniche operate and catch

skates as by-catch. The next step was to evaluate, for each

vessel, the frequency of fishing operations performed in

each fishing unit. For each vessel, spatial units were

characterized as very frequent (C70 % of the trips sampled

by vessel), frequent (30–70 % of the trips sampled by

vessel) and less frequent (\30 % of the trips sampled by

vessel). The results from each vessel were then combined

for the whole fleet, and the spatial units were classified as

PFS, if they were very frequent for more than one vessel or

very frequent for one vessel and frequent for more than

three vessels. Since fishing operations are mainly targeting

other species, the intensity of fishing in different spatial

units can be associated with skate occurrence. In particular,

spatial units with a higher number of fishing trips corre-

spond to a higher occurrence of skates.

Furthermore, fishing trips were separated by the main

fishing gear used and additional fishing units were classi-

fied as PFS if they contained more than 5 % of fishing trips

from a given fishing gear (i.e. trammel nets or longline).

Trips using gillnets and artisanal trawl were too low to be

considered separately for this task.

Each preferential fishing site (i.e. selected spatial unit)

was then characterized in terms of: topography, geomor-

phology and skate composition by species, sex ratio and

size. Significant differences from the expected 1:1 sex ratio

were evaluated by the v2 test (Zar 1996).

Considering the selected PFS, sensitive sites were

identified according to the occurrence of juveniles and

adults of seven species of skates: Raja brachyura, Raja

clavata, Raja microocellata, Raja miraletus, Raja monta-

gui, Raja undulata and Leucoraja naevus. Juveniles were

defined as specimens with total length smaller than 50 cm,

generally \4 years old, except for R. miraletus, a smaller

sized species where 40 cm total length was used (Table 1).

Adults were defined as specimens with total length larger

than the size-at maturity (L50), for each species and sex

(Table 1). Proportions in number of juveniles and adults

for each species in each fishing trip were determined from

length data.

To model the presence of juveniles and adults of those

species in the selected PFS and to identify spatial groups

among those sites with similar species composition, a Ta

ble

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Environmental Management

123

constrained correspondence analysis (CCA) (ter Braak and

Verdonschot 1995) was fitted to the proportion of juveniles

and adults by fishing trip, using the spatial unit as an

explanatory variable. The significance of the model was

verified by ANOVA (a = 0.05). The CCA was performed

using the package ‘vegan’ in R software (R version 2.15)

(Oksanen 2011). Spatial groups were formed according to

proximity of spatial unit scores in the CCA 3D-plot. The

closest species (juveniles, adults or both) to each spatial

group were also identified based on proximity of species

scores. These results were further validated by cross-ref-

erencing with the qualitative data provided by fishermen.

Results

A total of 301 interviews and 937 self-interviews were

collected from a selection of 58 vessels. Of a total of 1,238

sampled trips, 86 % had spatial data detailed as geographic

coordinates. A total of 334 fishing trips were sampled from

vessels of \10 m overall length, and 904 from vessels

between 10 and 20 m overall length. Regarding the main

fishing gears used to capture skates and considering that

each vessel is licensed to operate with more than one type of

fishing gear: 3 vessels operated with trawl (total of 21 trips),

36 with trammel nets (total of 1,126 trips), 5 with gillnets

(total of 7 trips) and 22 with longline (total of 84 trips).

Geomorphology

In the area focused on in this study (Fig. 1, Supplementary

Fig. 1), which extends from Nazare to Cabo da Roca, the

coast is predominantly composed of limestone rocky cliffs

except for the coast between Foz do Arelho and Peniche

(Souto 1991). Pocket beaches can be found south of Pen-

iche, due to the rocky configuration of the Peniche Pen-

insula. The beaches of the region of Peniche are mainly of

coarse sand, with some gravel and almost without fine

sands (Ferreira et al. 1989). Close to Peniche, the seabed

topography is very irregular, forming three main eleva-

tions, which compose the Berlengas Archipelago (i.e.

Berlenga, Estelas and Farilhoes islands), which are

delimited by deep valleys (Silva 1889). The continental

platform between Cabo Carvoeiro and Cabo da Roca forms

a promontory more than 70 km wide (‘‘Promontorio da

Estremadura’’), with a smoother slope, compared to the

adjacent Nazare and Lisboa Canyons. In general, close to

shore the sediment is sand, while between 12 and 26 nmi at

depths [100 m the sediment is gravel, and beyond it is

sand again (Dias et al. 1980). Overall, this region is very

hydrodynamic because of its geomorphology (Souto 1991),

which could be one of the reasons for the high biodiversity

found in the study area.

Overall Delimitation of Fishing Grounds

Of 74 marine spatial units, 47 contained sampled fishing

trips. There were differences in the selected fishing ground

depending on the fishing gear used. Even though the

samples collected from each fishing gear are unbalanced,

trammel nets (mean depth of 46 m) operated at shallower

depths than longline vessels (mean depth of 119 m).

Trammel nets operated mainly from close to shore to the

100 m isobath, while longlines were generally set farther

from shore, between the 50 and 1,000 m isobaths, but with

most trips at depths [100 m. Trawl trips were sampled

between 50 and 220 m, while gillnet trips were between 30

and 200 m.

Identification and Characterization of PFS

Some spatial units were selected by fishermen more times

than others. A total of 11 fishing units were selected as PFS

(Fig. 1). As expected, due to the size and capacity of the

sampled vessels, the spatial units closest to shore and to the

landing port of Peniche (i.e. included in the main areas of

Santa Cruz, Areia Branca, Berlenga and Peniche) were, in

general, the ones enclosing the fishing grounds with more

intense fishing activity. Each preferential fishing site was

characterized by the following: (a) depth range (information

provided by fishermen), types of sediments and geomor-

phology (Table 2; Supplementary Fig. 1); (b) overall

importance of each skate species in relative weight, size range

and sex ratio by species and information given by fishermen

about the occurrence of nursery or spawning sites (Table 3

and more detailed information presented as Supplementary

Table 2). The criteria for selection of each fishing site,

identified by the name of the main fishing ground and by the

coordinates of its north western limit, were:

(A) Mar da Ericeira: 8.3 % of longline fishing trips

(n = 7);

(B) Santa Cruz: 7.2 % of trammel net fishing trips

(n = 81);

(C) Off Santa Cruz: very frequent for 6 vessels and

frequent for 3 sampled trips; 21.0 % (n = 246);

(D) Mar do NW da Roca: 6.0 % of longline fishing trips

(n = 5);

(E) Areia Branca: very frequent for 4 vessels and

frequent for 2; 6.4 % of trammel net fishing trips

(n = 74);

(F) Off Areia Branca: very frequent for 2 vessels and

frequent for 4; 10.1 % of trammel net fishing trips

(n = 127);

(G) Mar do Cachimbo: very frequent for 2 vessels and

frequent for 3; 16.0 % of trammel net fishing trips

(n = 182);

Environmental Management

123

Ta

ble

2G

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orp

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feat

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4

Environmental Management

123

Ta

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44

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(39

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[11

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do

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(39�0

9.40 N

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fin

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nd

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(39

.3�N

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9.4

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[13

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3m

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?4

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(39

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[24

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(39

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[18

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rd

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oIs

thm

us

(ro

cky

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tto

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that

mak

esth

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ecti

on

bet

wee

nth

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ds

off

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d,

atb

etw

een

30

and

40

md

epth

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44

4

HM

ar

do

SW

da

Ber

len

ga

(39

.4�N

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.8�W

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[12

8–

17

4m

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Ma

rd

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Wd

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erle

ng

a

(39�1

7.70 N

,9

�50

.50 W

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Sea

bed

com

po

sed

of

bla

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nd

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ud

dy

san

dan

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mu

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tto

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east

(i.e

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ose

rto

this

spat

ial

un

it)

the

seab

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com

po

sed

mo

stly

of

bla

cksa

nd

a

44

4

JF

oz

do

Are

lho

(39

.5�N

,

9.3

�W)

[15

–9

1m

]

Va

leJa

nel

as

Sit

uat

edb

etw

een

the

30

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Environmental Management

123

(H) Mar do SW da Berlenga: 11.9 % of longline fishing

trips (n = 10);

(J) Foz do Arelho: very frequent for 1 vessels and

frequent for 4; 10.2 % of trammel net fishing trips

(n = 117);

(K) Baleal: 8.5 % of trammel nets fishing trips (n = 96);

(L) Berlengas: very frequent for 3 vessels and frequent

for 7; 13.1 % of longline fishing trips (n = 17).

Identification of Potential EFH—by Similarity

between PFS for Juveniles and Adult Abundance

of Skate Species

To reduce the number of zeros, due to the low number of

juvenile observations for R. undulata, R. microocellata, R.

miraletus and L. naevus, the proportion of juveniles was

added to that of adults, and considered together as a

Table 3 Catch percentages by weight, TL range (cm) and sex ratio (* statistically different from 1:1) of the main skate, only species

representing more than 5 % in weight are represented

Name (coordinates) RJC RJH RJM RJU RJE RJN RJO Nursery Spawning

A Mar da Ericeira (39.1�N,

9.8�W)

81.2 % 6.2 % 7.9 % 4 4

43–88 cm 43–66 cm 50–63 cm RJH RJN

1:0.70* RJM

B Santa Cruz (39.2�N,

9.4�W)

46.3 % 20.3 % 18.1 % 13.6 % 4 4

43–91 cm 41–102 cm 40–95 cm 45–82 cm RJH RJH

1:1.33* RJC

C Off Santa Cruz (39.2�N,

9.5�W)

36.5 % 39.3 % 5.8 % 10.9 % 4 4

45–95 cm 44–108 cm 42–90 cm 45–86 cm RJH RJC

RJC

1:1.45* 1:1.86* RJE

RJU

D Mar do NW da Roca

(39.2�N, 9.8�W)

95.1 % N/A 4

46–85 cm RJC

1:0.34*

E Areia Branca (39.3�N,

9.4�W)

25.4 % 24.0 % 24.6 % 25.9 % 4 4

48–90 cm 53–111 cm 49–93 cm 33–87 cm RJH RJH

RJC

RJE

F Off Areia Branca (39.3�N,

9.5�W)

44.0 % 39.6 % 5.5 % 5.3 % 4 4

39–98 cm 18–107 cm 37–70 cm 44–95 cm RJH RJH

1:1:26* 1:1:86* RJM

G Mar do Cachimbo

(39.4�N, 9.5�W)

18.1 % 72.6 % 4.3 % 2.3 % 2.3 % 4 4

36–88 cm 38–107 cm 26–68 cm 41–82 cm 1:0.38* RJH RJH

RJM

H Mar do SW da Berlenga

(39.4�N, 9.8�W)

100 % 4

RJC

N/A

51–90 cm

1:2.21*

J Foz do Arelho (39.5�N,

9.3�W)

36.7 % 28.0 % 14.5 % 16.6 % 4 N/A

42–89 cm 47–102 cm 49–96 cm 38–80 cm RJH

RJC

K Baleal (39.5�N, 9.4�W) 25.8 % 53.7 % 5.6 % 9.6 % 5.4 % 4 N/A

57–43 cm 40–101 cm 42–63 cm 48–90 cm 52–76 cm RJH

1:1.71*

L Berlengas (39.5�N,

9.6�W)

42.1 % 17.4 % 9.4 % 24.2 % 4 4

45–98 cm 48–102 cm 45–91 cm 79–125 cm RJU RJE

See Fig. 2 for species abbreviations

Environmental Management

123

sensitive group. Consequently, a total of 10 species vari-

ables were used to build the CCA model. The CCA model

was significant (F = 2.17, d.f. = 10, a = 0.005), and the

spatial unit was able to explain 10.2 % of the variability of

the proportion of juveniles and adults of seven skate spe-

cies (Fig. 2). Species were scaled proportional to eigen-

values. The three first axes explained 86.5 % of the

accumulated constrained eigenvalues.

Juveniles of R. brachyura, R. clavata and R. montagui,

adults of R. montagui and juveniles/adults of L. naevus and

R. miraletus were positively related with the first con-

strained axis CCA1 (eigenvalue 0.2607, 62 %), whereas

juveniles/adults of R. microocellata and R. undulata were

negatively related. The second constrained axis CCA2

(eigenvalue 0.0636, 15 %) explained the proportion of

adults of R. clavata and juveniles/adults of L. naevus,

which were positively related to CCA2. The third con-

strained axis CCA3 (eigenvalue 0.0408, 10 %) was

negatively related with adults of R. montagui. Spatial units

were grouped into four groups (Fig. 1) according to the

skate’s assemblage (Fig. 3).

A first group (g1) composed of the spatial units of Mar

da Ericeira (A) and Mar do NW da Roca (D) was associ-

ated with the occurrence of adults of R. clavata, R.

montagui and juveniles/adults of L. naevus. Based on the

information from Table 2, g1 includes mostly sites[100 m

depth with seabed composed of soft sediment, between

mud and fine sand. Spatial group g1 was also identified as

an egg deposition site for both R. clavata and L. naevus.

Although not recognized by the model, due to the high

abundance of R. clavata, it was considered that the spatial

unit Mar do SW da Berlenga (H) was more similar to the

first group than the remaining units.

A second group (g2) composed of Santa Cruz (B), Areia

Branca (E) and Foz do Arelho (J) was more associated with

the occurrence of juveniles/adults of R. undulata and

Fig. 2 Ordination 3D-plot of constrained correspondence analysis

(CCA) relating the proportion of juveniles and adults of seven skate

species (RJN: Leucoraja naevus, RJH: Raja brachyura, RJC: Raja

clavata, RJM: Raja montagui, JAI: Raja miraletus, RJE: Raja

microocellata, RJU: Raja undulata) to the potential constraining

variable spatial unit (qA Mar da Ericeira, qB Santa Cruz, qC off Santa

Cruz, qD Mar do NW da Roca, qE Areia Branca, qF off Areia Branca,

qG Mar do Cachimbo, qH Mar do SW da Berlenga, qJ do Arelho, qK

Baleal, qL Berlengas). Four spatial groups were identified according

to proximity of spatial unit scores (1–4). The ? sign represent the

centroids for each spatial unit

Environmental Management

123

R. microocellata. Spatial group g2, includes mostly sites

close to shore and below 50 m depth, with a geomor-

phology dominated by underwater beaches (Table 2).

A third group (g3) composed of Berlengas (L) and off

Santa Cruz (C) was more associated with the occurrence of

adults of R. brachyura and R. clavata, but also with the

occurrence of other skate species. Berlengas and off Santa

Cruz are very different in terms of topography, but their

seabed is composed mainly of rocks surrounded by sand. A

fourth group (g4) composed of off Areia Branca (F), Mar

do Cachimbo (G) and Baleal (K) was more associated with

the occurrence of juveniles of several species, namely

R. brachyura, R. montagui and R. clavata. Adults of the

same species may also occur, with those of R. clavata

being less frequent. This spatial group is situated mostly at

depths of \100 m and includes different types of seabed,

from sand to rocky bottoms.

Figure 3 summarizes the seasonal variation, by quarter,

of the proportion in weight of the most relevant pairs of

skate species and spatial group. In summary, in the first

spatial group (g1) the abundance of adults of R. clavata

increased along the year, being higher in the third quarter,

and in the second quarter for R. montagui. No samples

were collected in the fourth quarter in g1. In the second

21

3

Spatial group 1

Proportion

21

33

0.0 0.4 0.8

RJCa

RJMa

RJN

1

Spatial group 2

Proportion0.0 0.4 0.8

RJU

RJE

1

Spatial group 3

Proportion0.0 0.4 0.8

RJHa

RJCa

43

21

Spatial group 4

Proportion

14

32

32

14

21

43

2

43

2

32

14

43

21

43

21

43

21

0.0 0.4 0.8

RJHj

RJHa

RJCj

RJMj

RJMa

Fig. 3 Skate species composition by spatial group and quarter (1–4),

in terms of proportion of landed weight of juveniles (j) and adults

(a) by species: RJC: Raja clavata, RJM: Raja montagui, RJN:

Leucoraja naevus, RJU: Raja undulata, RJE: Raja microocellata and

RJH: Raja brachyura

Environmental Management

123

spatial group (g2) R. undulata and R. microocellata were

more abundant in the second quarter. In the third spatial

group (g3) the abundance of R. brachyura adults was

higher in the second quarter, but with considerable vari-

ability. The abundance observed for adults of R. clavata in

g3 decreased along the year, with a maximum in the first

quarter. Juveniles of R. clavata and R. montagui were more

abundant in the first and third quarters, whereas those of R.

brachyura occur more in the last quarter. On the other

hand, in the same spatial group (g4), the abundance of

adults of R. brachyura increased along the year, being

higher in the fourth quarter, whereas R. montagui were

more abundant in the first quarter.

Discussion

The present study followed the recommendations made by

the Code of Conduct for Responsible Fisheries (FAO 2009)

to document traditional fishery knowledge on small-scale

fisheries and to assess its application to the conservation

and management of fisheries. The information presented

here is an example of how the fishing sector can provide

relevant information on species distribution and abun-

dance, particularly for cases where no other data sources

are available. By virtue of their profession, fishermen are in

possession of practical and applied knowledge that is

extremely valuable for these objectives. Interviews were

the method adopted to gather the information from fisher-

men since they allow quantification and simplify compar-

isons between responses (Huntington 2000; Johannes and

Neis 2007). In addition, fishermen helped to cross validate

some of the results and to gather information on geomor-

phology of the study area. Indeed, due to the interest of

fishermen in the present work and in the conservation of

the species, the possibility of future collaboration in

fieldwork that will help in the delimitation and conserva-

tion of EFH for skates in the study area was raised.

The information gathered from interviews and self-

interviews allowed us to identify and characterize different

fishing grounds, which correspond to areas with different

abundance and biodiversity of skate species. Since the

sampled vessels belong to a multi-gear fleet that targets

different species along the year, but generally not skates,

they do not always select the areas where they know they

have a higher probability of catching skates. Therefore, the

selected vessels allowed the acquisition of unbiased data on

the diversity of skate species from a large number of

fishing grounds around Peniche. The choice of the method

and spatial resolution also proved to be adequate for the

species studied here and for the spatial distribution of their

recorded occurrences (Engler et al. 2004), since even at this

scale significant differences were found between spatial

units.

Another aspect of this study that is very important to

highlight is that in the process of obtaining information

from fishermen, done in close collaboration with a Fishing

Association (CAPA), it was guaranteed that knowledge

sharing would benefit and not harm the fishers. This trust

agreement ensured the reliability of the information pro-

vided by the fishers. In general, the information used to

identify nursery and spawning grounds, obtained from

interviews was generally in agreement with that obtained

from sampling in landing ports. Bergmann et al. (2004)

also reported good agreement between fisher’s information

and scientific surveys when identifying areas with high fish

density and therefore of relevance for further research.

Mackinson (2001) also observed no conflict in information

regarding herring behavior and distribution obtained from

fishers, scientists and literature sources, and also reported

that information obtained from interviews of fishermen

provided unique and critical information not possible to

obtain from other sources. Yet, there are some disadvan-

tages of using fishers’ knowledge. Data were carefully

handled and validated during collection and before use,

since some information could be unreliable (Rochet et al.

2008). Also, the expertise gained by performing the ques-

tionnaires in the field allowed double-checking of the

fishermen being interviewed, whenever they gave infor-

mation that was not in agreement with that collected

beforehand. The skepticism that still exists in the scientific

community with regard the usefulness of fishers’ knowl-

edge (Huntington 2000; Rochet et al. 2008) is another

disadvantage of this type of study. However, the current

and other recent studies (e.g. Bergmann et al. 2004;

Johannes and Neis 2007; Mackinson 2001; Mathew 2011;

Rochet et al. 2008; Silvano and Begossi 2012) are proof

that this approach is valid.

Fishers’ knowledge was used here to understand habitat

selection by marine fishes over a range of spatio-temporal

scales, which is extremely important because habitat choice

is one of the processes influencing population distribution,

abundance, and hence potential availability to fishermen

(Freond and Misund 1999). In the specific case of mainland

Portugal, there is very little knowledge on the distribution of

skate species, especially those that occur preferentially very

close to shore, like R. undulata, R. microocellata and R.

brachyura, where scientific trawl surveys are not carried out

and therefore no data are available. The geographical area of

central Portugal, where the artisanal fleet of Peniche oper-

ates, is of particular interest due to the high biodiversity and

seabed complexity, a consequence of the proximity of the

Nazare canyon. Within the study area, including all the

platform and upper slope around Peniche, islands and

Environmental Management

123

Promontorio da Estremadura, the high biodiversity may, in

part, be due to the fact that most of seabed cannot be fished

by trawls, which are very bottom habitat destructive and

have a high impact on biodiversity because of their low

species and size selectivity (Souto 1991). Given the infor-

mation collected through interviews and self-interviews,

differences between skate species composition were

observed between spatial units. Along the coast between

Peniche and Cabo da Roca, possibly because of the heter-

ogeneous landscape in a relatively small area, preferential

aggregation sites (PAS) for different skate species assem-

blages were identified. Sites with similar geomorphology

were identified as being suitable for the occurrence of the

same skate species, which suggests that the characteristics of

the seabed are critical for the selection of habitats by these

species. Also, those closest to the coast showed a higher

biodiversity of skate species, compared to those farther from

shore. In particular, Berlengas (included in spatial group

g3), with its peculiar geomorphology, known for its high

biodiversity, and protected by the Marine Reserve since

1981 (Decreto-Lei no. 246/81, de 3 de Setembro), was the

place where more skate species were found, including

coastal and offshore species, like D. oxyrinchus. Due to the

variety of habitats, Berlengas could also be a favorable place

for reproduction of skates, a fact confirmed by fishermen

who mentioned that juveniles of R. undulata and egg cap-

sules of R. microocellata could be found in that area. Being

already partially enclosed by the Berlengas Natural Reserve,

it is believed that this area could be one of the main con-

tributors to the known biodiversity and abundance of skates

in the surroundings of Peniche.

The four spatial groups here identified represent PAS for

specific skate species assemblages that could be considered

EFH given the presence of juveniles and/or reproductively

active adults. In particular, the identification of nursery sites

for R. brachyura, R. montagui and R. clavata in spatial group

g4 as seen in the CCA analysis was corroborated by the

information given by fishermen, based on their professional

knowledge. This result suggests that nursery areas of these

three species are located at shallower depths than those of

adult habitats. In fact, the abundance of juveniles shows a

seasonal variation, suggesting that newborns move from the

nursery areas to other locations after hatching. This has also

been reported for these and other skate species in other geo-

graphical areas, like the British Isles (Ellis et al. 2005), the

eastern Bering Sea (Hoff 2007, 2008) and southern California

(Love et al. 2008). The time of greatest abundance for each

species in spatial group g4 (i.e. R. clavata and R. montagui in

the first and third quarters and for R. brachyura in the last

quarter) is in agreement with the peak of births for these

species, determined by the time between the egg-laying sea-

son and the duration of the incubation period (Serra-Pereira

et al. 2011; McCully et al. 2012; Pina-Rodrigues 2012).

The seabed of the three spatial units that composed

spatial group g4 are not homogeneous, but are all charac-

terized by the presence of rocks and sand that could con-

stitute a suitable habitat for juveniles. This is in accordance

with a quote repeated by several fishermen, saying that

habitats composed of sand surrounding rocks was one of

the most suitable to find certain skate species, including R.

brachyura. The presence of nursery areas shows that spa-

tial group g4 could be an EFH for R. brachyura, R.

montagui and R. clavata. Future studies will be conducted

in order to evaluate the consequences of a possible seasonal

fishing closure in this area. Fishermen will be invited to

play an active role in this process in order to help analyze

all the pros and cons of the proposal, due to their ability to

provide knowledge not possible to obtain from scientific

sources. This will not be the first time they will be

involved, since in recent years, fishing communities, sup-

ported by their Fishing Associations (like CAPA that

contributed significantly to this study), have been propos-

ing management measures themselves, like for example the

seasonal closure for skates implemented during the month

of May, since 2012 (Portaria no. 315/2011).

The four spatial groups also enclose EFHs associated

with egg laying grounds. Those for R. clavata were located

within spatial group g1 and g3, those for L. naevus in

spatial group g1, R. brachyura in spatial groups g2 and g4

and R. microocellata in spatial group g3. As shown, around

Peniche, the same area can be used as an egg deposition

site for more than one species. This type of behavior can be

more common in species inhabiting shallower habitats,

where the biodiversity is higher, since species from deeper

waters show a distinct pattern. For example, bathydemersal

skate species from the genus Bathyraja in the eastern

Bering Sea, where only three species of skates occur, have

nursery sites predominantly used by a single species for

egg deposition, although, as also observed in this study,

other species could live in the same area (Hoff 2010).

For most species and areas, sexual segregation was not

observed. In most of the spatial units sampled in this study,

R. clavata was the only species showing dominance of a

given sex. Sites closer to shore showed a dominance of

females, whereas those far from shore, at depths [100 m

showed a dominance of males. This distribution pattern

implies sex differences in behavioral strategy and habitat

selection, even over an extremely fine scale. This is com-

mon in elasmobranchs (Springer 1967), being described for

example for dogfish Scyliorhinus canicula (Sims et al.

2001) and the scalloped hammerhead Sphyrna lewini

(Klimley 1987). Although it is thought that segregation by

sex occurs predominantly for reasons associated with

reproduction, the behavioral strategies behind sexual seg-

regation could also be related to habitat suitability/

requirements related to foraging behavior (Sims et al.

Environmental Management

123

2001). Sims et al. (2001) suggest that females may form

female-only aggregations in refuges spatially separated

from males to reduce energetically demanding mating

activity. Since females store sperm, permitting egg-laying

throughout most of the year (e.g. Serra-Pereira et al. 2010),

it is suggested that females avoid multiple copulations to

conserve energy for the peak mating and egg-laying season

(Sims et al. 2001).

In summary, this study, stresses the usefulness of using

fishers’ knowledge, is the first step towards understanding

skate species distribution in Portugal and specifically the

identification of possible EFH associated with nursery and

egg deposition sites. Identification and description of sites

of occurrence of seven skate species was accomplished, in

particular those associated with the occurrence of juveniles

and reproductively active adults, which are directly related

with nursery and spawning grounds. The identification of

nursery and egg deposition habitats is often difficult due to

their small size and specific locations, generally located in

irregular slopes associated with rocky bottoms (Love et al.

2008; Hoff 2010). But a dedicated study, starting from a

gross scale to a finer scale, the last based on onboard

sampling and with close collaboration of fishermen, could

be the right approach for the delimitation of the most

important EFH for skates in the study area and in the

remaining coast of mainland Portugal. This information

will be essential for defining seasonal fishing closure areas.

Acknowledgments We would like to thank all fishermen from

Peniche who collaborated with this study, specially the CAPA asso-

ciates and its president Jeronimo Rato. A special thank to ‘‘Mae

Purissima’’ skipper, Jose Manuel Festas for providing detailed fishing

ground information from the study area and for his close collaboration

in the elaboration of this paper. This study was supported by project

EU Data Collection Framework (DCF, PNAB). B. Serra-Pereira was

funded by the Fundacao para a Ciencia e Tecnologia, SFRH/BPD/

72351/2010 and C. Maia by the Pilot Study on Skates included within

the DCF.

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