LI

TRKRa

b

c

d

e

f

g

h

i

j

k

l

m

n

a

ARRAH

KCDLPS

h0

Fisheries Research 157 (2014) 47–61

Contents lists available at ScienceDirect

Fisheries Research

j ourna l ho me page: www.elsev ier .com/ locate / f i shres

arge-scale distribution of three deep-water squaloid sharks:ntegrating data on sex, maturity and environment

eresa Mouraa,∗, Emma Jonesb, Maurice W. Clarkec, Charles F. Cottond, Paul Croziere,oss K. Daleyf, Guzman Diezg, Helen Dobbyh, Jan E. Dybi, Inge Fosseni, Sarah B. Irvine j,lara Jakobsdottirk, Luis J. López-Abellán l, Pascal Lorancem, Pedro Pascual-Alayónl,icardo B. Severinon, Ivone Figueiredoa

Divisão de Modelac ão e Gestão de Recursos da Pesca, Instituto Português do Mar e da Atmosfera, Av. Brasília, 1449-006 Lisbon, PortugalNational Institute of Water and Atmospheric Research, 41 Market Place, Auckland Central 1010, New ZealandMarine Institute, Rinville, Oranmore, Galway, IrelandFlorida State University Coastal and Marine Lab, 3618 Coastal Hwy 98, St. Teresa, FL, USAWorld Wildlife Fund New Zealand, PO Box 6237, Marion Square, Wellington 6141, New ZealandCSIRO Wealth From Oceans Flagship, GPO Box 1538, Hobart 7001, TAS, AustraliaAZTI-Tecnalia, Marine Research Division, Txatxarramendi Ugartea z/g, 48395 Sukarrieta, Bizkaia, SpainMarine Scotland Science, Marine Laboratory, 375 Victoria Road, Aberdeen AB11 9DB, United KingdomMøre Research, Section of Fisheries, PO Box 5075, Larsgård, N-6021 Ålesund, NorwayIrvine Consulting, 617 Dorans Rd, Sandford 7020, TAS, AustraliaMRI, Marine Research Institute Iceland, Skúlagata 4, 121 Reykjavík, IcelandCentro Oceanográfico de Canarias, Instituto Espanol de Oceanografía, Vía Espaldón Dársena Pesquera Pcl. 8, 38180 Santa Cruz de Tenerife, SpainIFREMER, rue de L’Ile d’Yeu, BP 21105, 44311 Nantes Cedex 3, FranceCIMAR Laboratório Associado/CIIMAR, Centro de Investigac ão Marinha e Ambiental, Universidade do Porto, Rua dos Bragas, 289, 4050-123 Porto, Portugal

r t i c l e i n f o

rticle history:eceived 2 October 2013eceived in revised form 25 March 2014ccepted 30 March 2014andling Editor K.A. Rose

eywords:ommercial fishery dataeep-seaife stageopulation structureurvey data

a b s t r a c t

Deep-water sharks exhibit species-specific reproductive strategies, which include segregation by sex,size and reproductive stage. However, due to the wide spatial distribution of most species, availableinformation, usually collected at a regional scale, is usually not adequate to infer species reproductivespatial dynamics. This study draws together information on the distribution of reproductive stages ofthree species of squaliform sharks: Portuguese dogfish Centroscymnus coelolepis (Somniosidae), leafscalegulper shark Centrophorus squamosus (Centrophoridae) and birdbeak dogfish Deania calcea (Centrophori-dae), gathering data from several geographical areas from the Atlantic, Indian and Pacific Oceans. For eachspecies we analysed the sex ratio and the spatial patterns of reproductive stages within regions, consid-ering the influence of geographical area, depth, season, temperature and salinity. The combination ofstatistical methods used in this study successfully identified a number of life history patterns whichreflect different use of habitats by sex and life cycle stage. Pregnant females of the three species are spa-tially segregated, inhabiting shallower and/or warmer waters. In the case of the leafscale gulper shark thissegregation might be associated with large scale migrations. In contrast, in Portuguese dogfish all adultmaturity stages occur in the same geographical area. Pregnant female birdbeak dogfish were rare in allsamples. Larger immature specimens of all the three species distribute deeper than the remaining matu-rity stages in most of the regions analysed. Mature males of leafscale gulper shark and birdbeak dogfish

were more broadly distributed than mature females, supporting the possibility of sex-biased dispersal.Neonates and small sized specimens were scarce in the Northeast Atlantic potentially explained by theirconcentration in nurseries, and/or by gear selectivity. Management measures will benefit from consider-ing the geographic scale of demographic variation between species. However, standardized collaborative

d for

approaches will be neede

∗ Corresponding author. Tel.: +351 21 302 71 31.E-mail address: tmoura@ipma.pt (T. Moura).

ttp://dx.doi.org/10.1016/j.fishres.2014.03.019165-7836/© 2014 Elsevier B.V. All rights reserved.

comprehensive assessment.

© 2014 Elsevier B.V. All rights reserved.

4 s Rese

1

s(ifGda

alaisssbaC2mtrrppdte

feIsdeaihcewdiMisb

dCtmIrwaaw1scsn

8 T. Moura et al. / Fisherie

. Introduction

There is worldwide concern for the conservation of deep-waterharks due to low biological productivity and population declinesKyne and Simpfendorfer, 2010). Life history characteristics typ-cally include a slow growth rate, late age-at-maturity and lowecundity, indicating long generation times (Garcia et al., 2008;raham and Daley, 2011). Consequently, populations that haveeclined will require decades or even centuries to recover (Prattnd Casey, 1990; Simpfendorfer and Kyne, 2009).

Effective management of these species requires precaution-ry approaches founded on an understanding of species-specificife histories (Simpfendorfer and Kyne, 2009). Life-history traitsre quite diverse among deep-water sharks, but some strategies,ncluding segregation patterns, are similar to other elasmobranchpecies (Wearmouth and Sims, 2008). Although less studied thanhallow-water species, segregation within a population by sex,ize and/or reproductive stage has been reported for a num-er of deep-water shark species (Munoz-Chapuli, 1984; Yanond Tanaka, 1988; Wetherbee, 1996; Girard and Du Buit, 1999;larke et al., 2001; Jakobsdóttir, 2001; McLaughlin and Morrissey,005). Segregation may be advantageous in a population toaximize reproductive success, minimize predation risk or poten-

ial aggressive interactions, and for size or sex-specific foragingequirements (Sims, 2005; Wearmouth and Sims, 2008). Seg-egation can occur at different scales, and is often linked toarticular environmental or ecological features. The set of factorsotentially influencing segregation may be complex. Therefore,emographic data from the full range of a population is fundamen-al to assessing status and particularly for predicting responses toxploitation.

Attempts to develop adequate quantitative stock assessmentsor deep-sea sharks have fallen short of expectations due to inad-quate data, particularly in the Atlantic and southwestern Pacific.nformation available on deep-water sharks is derived either fromampling of commercial catches or from scientific surveys. Fisheryata are often restricted to those deep-sea sharks that are of great-st commercial importance, and have been limited historically by

lack of taxonomic and geographic precision. In contrast, fishery-ndependent surveys are often temporally irregular, and none havead sufficient geographic coverage to ensure that all demographicomponents of the populations are sampled. These deficiencies arexacerbated by the global distribution of some species that includeaters under many jurisdictions, and also by their specific repro-uctive strategies where mating and pupping might be decoupled

n space and time, due to sperm storage (Moura et al., 2011a).ajor scientific investment is required to gain a full understand-

ng of the spatial and temporal population dynamics of deep-waterharks, and enable estimates of sustainable exploitation levels toe derived.

The Portuguese dogfish (Centroscymnus coelolepis, Somniosi-ae), the leaf scale gulper shark (Centrophorus squamosus,entrophoridae) and the birdbeak dogfish (Deania calcea, Cen-rophoridae) are viviparous sharks widely distributed on the

id-continental slope at depths of 800–1600 m in the Atlantic,ndian and Pacific Oceans (Compagno et al., 2005). These specieseach 120–160 cm total length and are frequently caught by deep-ater trawl and bottom longline fleets (Stevens, 2003; Stevens

nd Correia, 2003; White, 2003). In the EU waters, a zero totalllowable catch (TAC) was adopted in 2010 for a variety of deep-ater sharks, including these species (Council Regulation (EU) no

359/2008). In Australia, in addition to a TAC regime, there are

patial/depth closures over some areas with important historicalatches (Woodhams et al., 2012). In the northwest Atlantic Ocean,outhwest Indian Ocean and in New Zealand, there are currentlyo management regulations for these species.

arch 157 (2014) 47–61

This study draws together regional knowledge of size distribu-tion and reproductive stages of three species of squaliform sharks.For each species, we analysed and compared the spatial patternswithin and among different regions of the Atlantic, Indian andPacific Oceans, using commercial and survey data. Spatial varia-tion of the defined maturity groups was studied considering theinfluence of depth, temperature, salinity, area and season. Thekey findings are presented in the context of regional managementarrangements required to ensure sustainability of populations.

2. Material and methods

2.1. Data sources

Biological data were collected onboard commercial trawl andlongline fishing vessels, and during research surveys conductedin six different ocean regions: northeastern (NE) Atlantic Ocean(including the mid-Atlantic ridge), centre-eastern (CE) AtlanticOcean, southeastern (SE) Atlantic Ocean, northwestern (NW)Atlantic Ocean, southwestern (SW) Indian Ocean and southwest-ern (SW) Pacific Ocean (Fig. 1; Table A1). All specimens were caughtwithin the bathymetric range of 200–3200 m.

2.2. Data collation and standardization

The spatial and temporal resolution of the data varied amonggeographic areas due to the logistical constraints associated withthe different sampling methods (e.g. depth, gear, duration, year,season). In order to allow the comparison of datasets from dif-ferent sampling years the distribution patterns of each species ineach geographical area and region were assumed to be temporallyconsistent.

A number of data standardization steps were applied to pro-duce a single database. As much of the data had been collectedopportunistically, the geographic precision of the capture loca-tions varied among sources. Therefore, the first key step was tostandardize locations by ocean ‘region’. Data from NE Atlantic,SW Indian and SW Pacific regions were further classified by ‘geo-graphic area’. The second step was to ensure that the biologicalattributes recorded were consistent among regions. Biological dataprovided for each specimen included the species total length (TL),sex and maturity stage. Maturity stage data were standardized byclassifying each individual according to a maturity stage group.These groups are based on Stehmann (2002) modified after byFigueiredo et al., (2008) and Irvine et al., (2012) (equivalent stagesindicated in parentheses). For males, two groups were consid-ered: immature (immature and maturing) and mature (matureand active). For females four groups were considered: immature(immature and maturing), mature (mature-non-pregnant, pre-ovulatory), pregnant (developing, differentiating and expecting)and post-natal (post-natal). Where regenerating females (matur-ing, not for the first time) had been observed, they were combinedwith post-natal stages. In the dataset from the SW Indian Ocean theinformation was not sufficient to discriminate between post-nataland mature females.

Published studies show that neonates of these three species arescarce or entirely absent from the NE Atlantic. This study examineda size-based subset of the data for immature specimens for the samepattern. The term “juvenile” was used for small immature individ-uals between length-at-birth and a pre-determined upper limit.These sizes were based on published values from the NE Atlantic

(Girard and Du Buit, 1999; Clarke et al., 2002; Figueiredo et al.,2008) and were assumed to be applicable to other regions. Size-at-birth was taken as 25–31 cm for the Portuguese dogfish (Mouraet al., 2011b), 38–44 cm for the leafscale gulper shark (Banon et al.,

T. Moura et al. / Fisheries Research 157 (2014) 47–61 49

Fig. 1. Worldwide sampling sites for the Portuguese dogfish, leafscale gulper shark and birdbeak dogfish. NW Atlantic, including (a) Gulf of Mexico; (b) U.S. east coast; and(c) Greenland. NE Atlantic including (d) Iceland; (e) Rockall and Hatton Banks; (f) Scotland; (g) north of the Charlie-Gibbs Fracture Zone; (h) Ireland; (i) north Azores; (j) Bayof Biscay; (k) Portugal; (l) south Azores; (m) Madeira Archipelago; and (n) Canarias Archipelago. CE Atlantic in particular (o) Mauritania. SE Atlantic in particular (p) Namibia.SW Indian including (q) Mozambique Plateau; and (r) Madagascar Plateau. SW Pacific including (s) New South Wales; (t) Tasmania (Australia); (u) Chatham Rise and NorthIsland; and (v) South Island and Campbell Plateau (New Zealand).

5 s Rese

2fifftlcg

i

2

mtc

mdm

2

stTh8sTp

2

mawc

tvgbt

2

bA(t2alsrrted

hbsR

0 T. Moura et al. / Fisherie

006; Figueiredo et al., 2008) and 28–33 cm for the birdbeak dog-sh (Irvine et al., 2012). The upper limit sizes applied were <60 cm

or the Portuguese dogfish and leafscale gulper shark and <55 cmor the birdbeak dogfish. Hereafter term “immature” will refer onlyo the fraction of immature stage specimens above the upper sizeimit for juveniles. Juvenile and immature specimens were onlyombined when estimating the proportion of maturity stages byeographical area.

Datasets lacking maturity stage, sex or size were only consideredn some analysis or in assessing geographic distribution.

.3. Statistical analysis

All data analyses were conducted in the R software environ-ent (R Core Team, 2012). For each species-region combination,

he relationship of maturity to depth was evaluated with boxplotsonstructed using the package Lattice (Sarkar, 2008).

The influence of gear type (trawl or longline) on length andaturity stage was also evaluated for the NE Atlantic region, where

ifferent types of gears were used for the collection of the speci-ens.

.3.1. Sex ratioThe influence of depth on sex ratio was examined for each

pecies-area combination by calculating the median and interquar-ile ranges of the proportion of females by depth strata (100 m).his analysis was restricted to geographical areas with 25 or moreauls of >1 individual. The depth intervals varied between species:00–1700 m for the Portuguese dogfish, 500–1700 m for the leaf-cale gulper shark and 500–1400 m deep for the birdbeak dogfish.hese intervals include the depths where each species were sam-led more frequently.

.3.2. Mapping and occurrence of maturity stagesFor males and females, the proportion of individuals at each

aturity stage was described and plotted for each geographicalrea and region where sufficient data were available (only datasetsith maturity information for a total of 30 or more individuals were

onsidered).To characterize the spatial pattern of the different life stages,

he occurrence of each maturity stage was mapped using ArcGIS.9.0. The analysis was restricted to observations with precise geo-raphic location. These data were overlaid on mapped coastline andathymetry data extracted from the General Bathymetric Chart ofhe Oceans (GEBCO) (IOC, IHO and BODC, 2003).

.3.3. Environmental variables and maturityTemperature and salinity values were estimated for each haul,

ased on geographical position and depth, using the World Oceantlas 2009 database from U.S. National Oceanographic Data Center

Antonov et al., 2010; Locarnini et al., 2010) and the 3D estima-ion method implemented in Ocean Data View Software (Schlitzer,011). 3D point estimation is a fast weighted averaging procedurend combines the environmental information with user specifiedongitude, latitude and depth, assuming specific averaging lengthcales (Schlitzer, 2011). Scales were considered as 2.5% of the axisanges for longitude and latitude and 100 m for depth. Yearly envi-onmental values were used in calculations because a preview ofhe monthly data found only minor variation. Further, the monthlynvironmental data did not cover the full depth range of the catchata.

Constrained correspondence analysis (CCA) was used to explore

ow the maturity stages of each species were influenced as aiological response to four environmental variables: temperature,alinity, depth and season. This analysis used the Vegan package for

software (Oksanen, 2011). This method combines a multivariate

arch 157 (2014) 47–61

ordination presence/absence of maturity stage with a constrainedregression maximizing the correlation between the maturity stagesordination axes and the selected environmental variables. It wasassumed that the ecological range of each maturity stage ana-lysed has been sampled and further assumed that each maturitystage presents a unimodal response to each independent variable(ter Braak, 1986; Borcard et al., 2011). It is pertinent to note thatwhilst the inertia (percentage of variation explained) is typicallylow (<10%) when CCA is applied to binary variables, the resultscan still be ecologically meaningful (ter Braak and Verdonschot,1995; Oksanen, 2011). Two matrices were constructed for thisanalysis: one corresponding to the occurrence of maturity stages(presence/absence, dependent variable), and the other correspond-ing to the environmental variables mentioned above (independentvariables). CCA were fitted conditioned to the geographical area,i.e. area was partially out from the analysis before constraints,and only to regions with representative data (>100 georeferencedhauls with maturity information). The final selection of indepen-dent variables for inclusion in the CCA model followed a stepwiseprocess, based on the Aikaike information criterion (AIC). The vari-ance inflation factor (VIF) was used to avoid multicollinearity, i.e.inclusion of environmental variables strongly correlated with eachother (ter Braak, 1986; Oksanen, 2011). VIFs > 10 should be exam-ined and avoided (Borcard et al., 2011). In cases where VIF > 10, allthe possible combination of variables were considered in the CCAs.Variable selection considered the Spearman correlation coefficientestimated between variables and the most rational results for VIF,AIC and proportion of inertia explained. Results of the analysis wereplotted and scaled to maturity stages. Monte Carlo permutationtests were used to assess the significance of the terms and axis ofthe model. In both cases a significance level of 5% was adopted.

The function “ordisurf”, from the vegan R package was used forweighted fitting and plotting of a smooth surface of the selectedvariables. This function fits the environmental surface using thinplate splines in a generalized additive model (GAM), and thenuses the results to predict and plot the surface on an ordinationdiagram (Oksanen et al., 2012). This analysis allows curvilinear rela-tionships, and tests the linearity hypothesis of the biplot method(Oksanen, 2011). It is important to note that this method enablesthe evaluation of trends for each variable independently and isbased on the proportion of variance explained by the variablesincluded in the model.

3. Results

3.1. Portuguese dogfish

3.1.1. Sampling detailsPortuguese dogfish data were obtained for all six regions and

represented eighteen geographical areas. A total of 9388 speci-mens were recorded, of which up to 5940 individuals were selectedfor more detailed analysis, based on precision of recorded locationand maturity information. This number excluded individuals fromSW Pacific, without geo-referenced data, which were used solely todetermine the proportion of individuals by maturity stage. Depthand TL ranges by sex and maturity stage are reported in Fig. 2and Table A2. Maximum length was sexually dimorphic in mostregions and geographic areas, with females attaining larger sizesthan males. Exceptions were the SW Indian regions, New Zealand(SW Pacific) and Tasmania (SW Pacific).

3.1.2. Sex ratioFemales outnumbered males in the NE Atlantic (with excep-

tion of the Bay of Biscay), in the CE Atlantic and in the SE Atlantic,whereas the opposite was observed for the SW Indian and SW

T. Moura et al. / Fisheries Research 157 (2014) 47–61 51

Portuguese dogfish Leafscale gulper shark Birdbeak dogfish

3000200010000

NE

Atlantic

JVIM

MMMFPGPN

PN CE

Atlantic

JVIMMMMFPG

PGPN

Mat

urity

sta

ges

JVIM

MMMF

MMMFPGPN

SE

Atlantic

JVIM

IMMMMFPGPN

NW

Atlantic

SW

Indian

JV

JVIMMMMFPGPN S

W P

acific

Depth (m)

30002000100003000200010000

Fig. 2. Relationship between the sampling depth and maturity stage by region for the Portuguese dogfish, leafscale gulper shark and birdbeak dogfish (n = 16,042). In theb s repreo aturec y that

PsMd

3

cmbfitapptepsti

ox-and-whisker plots, the box represents the 25th and 75th quantiles. The whiskerutliers. The black dots represent the medians. JV: juveniles; IM: immatures; MM: mells represent a lack of sampling data for the respective species and not necessaril

acific Oceans (Table 1). Sex ratios varied within and between depthtrata for all geographical areas analysed (Fig. A1). In Scotland,auritania and Namibia the proportion of females increased with

epth.

.1.3. Mapping and occurrence of maturity stagesPopulation structure varied between regions and geographi-

al areas. In the NE Atlantic and in the SW Pacific (Australia) allaturity stages were sampled (Table 1, Fig. 3), with length ranges

eing similar among fishing gears in the first region (Fig. A2). Foremales, the proportions by different maturity stages were similarn some NE Atlantic geographical areas (excluding Rockall and Hat-on Banks, North Azores and Canarias) and in Tasmania. In thesereas, mature females accounted for around 17–25% of the sam-les, with pregnant females making up 8–17%. In contrast, theroportion of mature and immature males varied widely withinhe NE Atlantic and SW Pacific regions. The pattern was differ-nt for other regions. In the CE and SE Atlantic regions, mature,

regnant and post-natal females and mature males were absent oreldom observed. In the NW Atlantic region, juveniles prevailed inhe samples and only one mature female was recorded. Some areasn the SW Indian region provided contrast: off the Mozambique

sent 1.5 times the interquartile range. The points beyond the whiskers are potential males; MF: mature females; PG: pregnant females; PN: post-natal females. Emptythe species doesn’t occur.

plateau, immature and mature females were most common, withsome pregnant females also recorded; off the Madagascar plateau,mature males were more common and pregnant females made upnearly 30% of the female sample.

The number of juveniles caught varied among regions: zero orlow numbers were recorded in the NE Atlantic (n = 7), SW Indian(n = 0) and SW Pacific, Australia (n = 8), whilst much higher numberswere reported for the NW Atlantic (n = 53), CE Atlantic (n = 796),with the highest numbers recorded in the SE Atlantic (n = 695).Some of these were potentially neonates since their sizes were closeto the estimated length-at-birth. Most of the juvenile specimenswere caught by trawlers, with the exceptions being one individualcaught by longline in the NE Atlantic and a small portion of the NWAtlantic sample that was caught with traps.

3.1.4. Environmental variables and maturityFor the NE Atlantic data (excluding juveniles, that were

recorded in low number), depth was the only factor selected

in the CCA model. This model explained 10% of the total iner-tia (pcanonical relationship = 0.005; paxis = 0.002). Depth was negativelycorrelated with axis 1. The ordination and surface model of theenvironmental variable selected showed that pregnant females

52 T. Moura et al. / Fisheries Research 157 (2014) 47–61

Table 1Portuguese dogfish. Proportion of maturity stages, total numbers by sex (n) and sex-ratio by geographical area and by region (in bold). The immature groups include juveniles.F: females; M: males.

Geographical(area/region)

Portuguese dogfish Sex ratioF:M

Males Females

n Immature Mature n Immature Mature Pregnant Post-natal

Iceland 45 0.87 0.13 262 0.40 0.23 0.17 0.20 5.82Rockall and Hatton Banks 104 0.44 0.56 669 0.42 0.23 0.00 0.34 6.43Scotland 136 0.51 0.49 272 0.52 0.19 0.08 0.21 2.00Ireland 255 0.33 0.67 538 0.43 0.25 0.08 0.24 2.09Bay of Biscay 39 0.10 0.90 26 0.58 0.19 0.12 0.12 0.67Portugal 114 0.32 0.62 253 0.37 0.23 0.17 0.23 2.22North Azores (MAR) 19 0.21 0.79 30 0.20 0.80 – – 1.58Canarias Archipelago 88 0.27 0.73 181 0.35 0.63 0.02 – 2.06Total NE Atlantic 800 0.39 0.61 2231 0.42 0.27 0.07 0.24 2.80

CE Atlantic (Mauritania) 616 1.00 0.00 765 0.98 0.01 0.01 – 1.24

SE Atlantic (Namibia) 391 0.98 0.02 553 0.99 0.01 – – 1.41

NW Atlantic (U.S. east coast) 21 1.00 – 21 0.95 0.05 – – 1.00

Mozambique Plateau 229 0.60 0.40 207 0.34 0.57 0.09 – 0.90Madagascar Plateau 72 0.39 0.61 34 0.32 0.38 0.29 – 0.47Total SW Indian 301 0.55 0.45 241 0.34 0.54 0.12 – 0.80

hae

dAsSost

New South Wales 62 0.68 0.32 23Tasmania 171 0.09 0.71 70Total SW Pacific 233 0.25 0.75 93

ad the shallowest distribution, mature males were deeper andll other stages deeper still, and at closely located sites (deviancexplained = 58%) (Fig. 4).

All the other datasets were inadequate to run the CCA, eitherue to the low representation of maturity groups (CE Atlantic and SEtlantic datasets were composed mainly of juveniles and immaturepecimens) or to insufficient data (as the case of NW Atlantic and

W Indian Ocean). In the CE Atlantic, 68% of the juveniles caughtccurred between 1300 and 1500 m deep. Juveniles and immaturepecimens were caught in the same hauls, although each haul wasypically dominated by one group or the other. Those hauls clearly

Fig. 3. Portuguese dogfish. Occurrences of (a) juveniles, (b) mature males an

0.65 0.09 0.09 0.17 0.370.51 0.17 0.16 0.16 0.410.55 0.15 0.14 0.16 0.40

dominated by juveniles were mostly located at centre-south slopeof Mauritania. In the NW Atlantic, juveniles were recorded from 670to 2624 m but 88% of these catches were shallower than 1000 m.In the SW Indian Ocean, maturity stages were not correlated withdepth.

3.2. Leafscale gulper shark

3.2.1. Sampling detailsData for the leafscale gulper shark were obtained for all regions

of the Eastern Atlantic and for the SW Pacific. A total of 5480

d females, and (c) pregnant and post-natal females in the NE Atlantic.

T. Moura et al. / Fisheries Rese

-1-2 10 32

0-1

2

13

Portuguese dogfish, NE Atlantic

CCA1

CA

1

ImmatureF

MatureF

Pregnant

PostnatalImmatureM

MatureM

600

1000

1200

1400

Fig. 4. Constrained correspondence analysis of the Portuguese dogfish distributionbc(

siaa

3

dIiradseaca

3

raamwmdaiPAwCnol

y maturity stage. Ordination of the maturity stages (black circles) and hauls (greyircles) overlaid with the surface model fitted for depth (in metres) in the NE Atlanticn = 2991; 509 hauls). Axes 1 accounted for 100% of the variance of the fitted values.

pecimens were sampled, with up to 3483 meeting the criteria fornclusion in the statistical analyses. Depths and TL ranges by sexnd maturity stage are reported on Fig. 2 and Table A3. Femalesttained larger sizes than males for most geographical areas.

.2.2. Sex ratioIn the NE Atlantic, sex ratios varied between areas. Males pre-

ominated over females on the Rockall and Hatton Banks, offreland, Portugal, on the Mid Atlantic Ridge (Northern Azores) andn Madeira (Table 2). Females were more frequently caught in theemaining areas. In the northern areas of the NE Atlantic (Scotlandnd Ireland) the proportion of females increased with increasingepth although there was also high variability within each depthtrata (Fig. A3). In the CE Atlantic, males and females were caught inqual numbers, but samples sizes were too low for more detailednalysis. In the SW Pacific (New Zealand), females were signifi-antly more abundant than males in the two geographical areasnd sex ratios were not influenced by depth.

.2.3. Mapping and occurrence of maturity stagesThe proportions of maturity stages varied considerably among

egions and geographical areas (Table 2, Fig. 5). In the NE Atlantic,ll the maturity stages were caught and size ranges did not differmong fishing gears (Fig. A4). In this region, apart from Iceland,ature males were more common than immature males, andere broadly distributed along the continental slopes. In contrast,ature females were far less common, with immature specimens

ominating the catch, except around Iceland and further southround Madeira and Canarias. Pregnant females were only recordedn three regions: off Iceland (n = 5 out of 36 females sampled),ortugal (n = 3 out of 122 females sampled) and from the Madeirarchipelago (n = 30 out of 60 females sampled). Post-natal femalesere recorded from most of the geographical areas except the

anarias and Madeira Archipelagoes and the mid-Atlantic ridgeorth to the Azores. Despite the large sample sizes in many areas,nly 3 juveniles were caught from SW of the Portuguese main-and. These specimens, as well as all the other juvenile specimens

arch 157 (2014) 47–61 53

recorded from other regions, were caught using trawl nets. In theCE Atlantic, immature specimens dominated the sample. Maturemales were recorded all along the surveyed slope. No maturefemales were caught in this area. The few records of this species inthe SE Atlantic included immature (including juveniles) and maturespecimens from both sexes. Around New Zealand in the SW Pacificregion, immature individuals were dominant for both males andfemales. Pregnant and post-natal females were rare (n = 12 and4 out of 508 females sampled, respectively). Juveniles occurredmainly on the northern slopes of the Chatham Rise and also to thesouthwest of the South Island of New Zealand (Puysegur Bank).

3.2.4. Environmental variables and maturityIn the NE Atlantic, juveniles were excluded from the CCAs

due to small sample sizes. In this region, depth and tempera-ture were the environmental factors selected in the CCA model,explaining 16% of the total inertia (pcanonical relationship depth = 0.005;pcanonical relationship temperature = 0.005; paxis1 = 0.002; paxis2 = 0.002).These two environmental variables were highly correlated withaxis 1, with depth being positively related and temperature beingnegatively related with this axis. Axis 2 was also negativelycorrelated with temperature. The surface model of the selectedenvironmental variables indicated that the distribution of maleswas not related to depth or temperature, but post-natal and maturefemales tended to occur in relatively shallower sites (devianceexplained = 76% and 53% for depth and temperature, respectively)(Fig. 6a and b). Pregnant females were distributed preferentially atwarmer stations compared to the remaining maturity stages, par-ticularly immature females, which were usually found at greaterdepths and lower temperatures.

In the SW Pacific data (excluding pregnant and post-natal females due to their low numbers in the samples),the best CCA model included only depth and salinity (6% ofthe total inertia explained; pcanonical relationship depth = 0.002;pcanonical relationship salinity = 0.075; paxis1 = 0.002; paxis2 = 0.950).Depth was positively correlated with axis 1 and salinity waspositively correlated to axis 2, the latter explaining a small fractionof variation. The ordination and the surface models of the selectedenvironmental variables showed that immature males, femalesand juveniles all co-occurred at relatively deeper and less salinewaters (deviance explained = 96.5% and 100% for depth and salin-ity, respectively) (Fig. 6c and d). Mature males were associatedwith shallower, more saline waters. Nine of the twelve femaleswere found in waters shallower than 900 m. The two post-natalfemales sampled in the South Island were collected from depthsshallower than 650 m, whereas those sampled in the Chatham Riseand North Island were both collected in the 900 m stratum.

Sample sizes from the CE Atlantic and SE Atlantic were insuf-ficient for CCA (n = 26 and 13 hauls, respectively), but differencesin maturity stages occurrence were also found to be related withdepth. In the CE Atlantic, 75% of the juveniles occurred <900 m deep,at similar depths to mature males, whereas immature specimenswere found relatively deeper. In the SE Atlantic, juveniles (n = 4)were caught between 550 and 800 m deep, shallower than all othermaturity stages.

3.3. Birdbeak dogfish

3.3.1. Sampling detailsData were obtained from the Atlantic and the SW Pacific. A total

of 14 468 specimens was collected, of which 12 189 met the criteriafor inclusion in the statistical analysis. Depth and TL ranges by sexare reported in Fig. 2 and Table A4. In all the areas sampled, femalesattained larger sizes than males.

54 T. Moura et al. / Fisheries Research 157 (2014) 47–61

Table 2Leafscale gulper shark. Proportion of maturity stages, total numbers by sex (n) and sex-ratio (number of females for one male) by geographical area and by region (in bold).The immature groups include juveniles. F: females; M: males.

Geographicalarea/region

Leafscale gulper shark Sex ratioF:M

Males Females

n Immature Mature n Immature Mature Pregnant Post-natal

Iceland 10 0.80 0.20 36 0.22 0.28 0.14 0.36 3.60Rockall and Hatton Banks 352 0.28 0.72 275 0.90 0.04 – 0.06 0.78Scotland 308 0.25 0.75 405 0.82 0.10 – 0.08 1.31Ireland 322 0.39 0.61 248 0.95 0.04 – 0.01 0.77Portugal 133 0.25 0.75 122 0.81 0.09 0.02 0.07 0.92North Azores (MAR) 82 – 1.00 1 1.00 – – – 0.01Madeira Archipelago 145 0.06 0.94 60 0.42 0.08 0.50 – 0.41Canarias Archipelago 31 0.48 0.52 43 0.42 0.58 – – 1.39Total NE Atlantic 1383 0.27 0.73 1190 0.81 0.09 0.03 0.06 0.86

CE Atlantic (Mauritania) 42 0.76 0.19 44 1.00 – – – 1.04

73

35

08

3

me

Fm

Chatham Rise and North Island 134 0.87 0.13 2South Island, Campbell Plateau 182 0.58 0.42 2Total SW Pacific 316 0.70 0.30 5

.3.2. Sex ratioSex ratios varied between regions. For the NE Atlantic region,

ales predominated over females at most sampling locations,xcept in the Bay of Biscay, Portugal and Canarias Archipelago

ig. 5. Leafscale gulper shark. Occurrences of (a) juveniles, (b) mature males and femalesales and females; (f) pregnant and post-natal females in the SW Pacific (New Zealand).

0.81 0.16 0.03 0.01 2.040.74 0.23 0.02 0.01 1.290.78 0.19 0.02 0.01 1.61

(Table 3). In this region, sex ratios were variable among depth strata,but with no discernable trend (Fig. A5). In the CE Atlantic, femalespredominated over males but in the SE Atlantic the contrary wasobserved. In these two regions, the proportion of females decreased

; (c) pregnant and post-natal females in the NE Atlantic; of (d) juveniles, (e) mature

T. Moura et al. / Fisheries Research 157 (2014) 47–61 55

-3 -2 -1 0 1 2 3

-3-2

-10

12

3Leafscale gulper shark, N E Atlantic

CCA1

CC

A2

ImmatureF

MatureF

Pregnant

Postnatal

ImmatureM

MatureM 1

000

150

0

200

0 -3 -2 -1 0 1 2 3

-3-2

-10

12

3

Leafscale gulper shark, NE Atlantic

CCA1C

CA

2

ImmatureF

MatureF

Pregnant

Postnatal

Immatu reM

MatureM

4

5

5

6 7

8

9

10

-3 -2 -1 0 1 2

-10

12

3

Leafscale gulper shark, SW P acific

CCA1

CC

A2

ImmatureF

MatureFImmatureM

MatureM

Juveniles

500

600

700

800

900

1000

1100

-3 -2 -1 0 1 2

-10

12

3Leafscale gulper shark, SW P acific

CCA1

CC

A2

ImmatureF

MatureFImmatureM

MatureM

Juveniles

34.4

34.45

34.5

34.55

a b

c d

Fig. 6. Constrained correspondence analysis of leafscale gulper shark distribution by maturity stage. Ordination of the maturity stages (black circles) and hauls (grey circles)o e (in ◦

S countS s, resp

woCcti

3

aA

verlaid with the surface model fitted for (a) depth (in metres) and (b) temperaturW Pacific (New Zealand; n = 808; 241 hauls). In the NE Atlantic data axes 1 and 2 acW Pacific axes 1 and 2 accounted for 97% and 3% of the variance of the fitted value

ith depth. In the SW Pacific region (New Zealand), the numbersf males and females were similar off the South Island but on thehatham Rise and around the North Island, females were moreommon than males. In this area, the proportion of females seemedo decrease with depth, despite the high variability observed (widenterquartile ranges).

.3.3. Mapping and occurrence of maturity stagesThe proportion of maturity stages observed varied considerably

mong geographical areas and regions (Table 3, Fig. 7). In the NEtlantic, specimens of all maturity stages were caught and size

C) in the NE Atlantic (n = 2435; 374 hauls) and for (c), depth and (d), salinity in theed for 63% and 37% of the variance of the fitted values, respectively, whereas in theectively.

ranges were similar among fishing gears (Fig. A6). In this region,mature males were widely distributed, but their proportion wasvariable among geographical areas. Immature females outnum-bered mature females in almost all regions, except the CanariasArchipelago. The number of pregnant females was low or totallyabsent in most geographical areas. Post-natal females were mainlyrecorded in northern areas, often spatially separated from other

stages. In this region, juveniles were caught both with trawls andlonglines, and were recorded on Hatton Bank (n = 10), off Ireland(n = 2) and on the SW Portugal mainland (n = 5), but representingless than 1% of the total sample from these areas. In contrast, the

56 T. Moura et al. / Fisheries Research 157 (2014) 47–61

Table 3Birdbeak dogfish. Proportion of maturity stages, total numbers by sex (n) and sex-ratio by geographical area and by region (in bold). The immature groups include juveniles.F: females; M: males.

Geographicalarea/region

Birdbeak dogfish Sex ratioF:M

Males Females

n Immature Mature n Immature Mature Pregnant Post-natal

Iceland 151 0.19 0.81 100 0.55 0.24 0.04 0.17 0.66Scotland 218 0.51 0.49 112 0.79 0.06 0.01 0.13 0.51Ireland 901 0.48 0.52 602 0.83 0.10 0.02 0.05 0.67Rockall and Hatton Banks 248 0.21 0.79 129 0.76 0.10 – 0.14 0.52Bay of Biscay 66 0.12 0.88 100 0.85 0.14 0.01 – 1.52Portugal 0 – – 33 0.76 0.18 0.06 – –Canarias Archipelago 5 0.4 0.6 46 0.28 0.72 – – 9.20Total NE Atlantic 1589 0.40 0.60 1122 0.77 0.14 0.02 0.07 0.71

CE Atlantic (Mauritania) 542 0.93 0.07 722 0.90 0.06 0.02 0.00 1.33

SE Atlantic (Namibia) 211 0.55 0.45 113 0.53 0.47 – – 0.53

960

87

147

cMnsfst(auftowbwCt

3

stetaadc(

mtoppsoefetsv

Chatham Rise and North Island 3548 0.37 0.63 3South Island, Campbell Plateau 195 0.12 0.88 1Total SW Pacific 3743 0.36 0.64 4

entral and southern areas of the eastern Atlantic, off the coasts ofauritania (CE Atlantic) and Namibia (SE Atlantic), much higher

umbers of juveniles were caught, representing 38–41% of theamples (all caught with trawl nets). In the CE Atlantic, immatureemales and males (including juveniles) made up over 90% of thepecimens caught. Further south, in the SE Atlantic region, imma-ure specimens also accounted for a large percentage of the catches∼50%). Here, pregnant and post-natal females were entirelybsent. In the SW Pacific around New Zealand, mature males madep nearly 90% of males caught from the Campbell Plateau, and 63%urther north on the Chatham Rise and off the North Island., imma-ure females (including juveniles) were more common, making upver 78% of females examined. Pregnant and post-natal femalesere common around North Island but were absent from the Camp-

ell Plateau. Juveniles were caught by trawl nets in both areas forhich data were available, and were far more common on thehatham Rise and North Island shelf (23% of specimens caught)han around the Campbell Plateau further south (2.8%).

.3.4. Environmental variables and maturityIn the NE Atlantic, depth was the leading environmental factor

elected by the CCA model, explaining 12% of the total iner-ia (pcanonical relationship depth = 0.005; paxis1 = 0.002). Juveniles werexcluded from this analysis due to low numbers. Depth was posi-ively correlated with axis 1. The ordination of the maturity stagesnd the overlaid surface model for depth showed that mature malesnd both immature males and females tended to occur at greaterepths, while pregnant, post-natal and mature females were asso-iated with relatively shallower depths (deviance explained = 80%)Fig. 8a).

In the SW Pacific New Zealand data, the CCA adjustment showedulticollinearity for temperature, depth and season. As a result

he selected model just included salinity and temperature (10%f the total inertia explained; pcanonical relationship temperature = 0.005;canonical relationship salinity = 0.005; paxis1 = 0.002; paxis2 = 0.002). Tem-erature was highly negatively correlated with axis 1 whereasalinity was primarily correlated (negatively) with axis 2. Therdination of the maturity stages overlaid on the surface mod-ls of each selected variable showed that post-natal and pregnantemales occurred in warmer and higher salinity waters (deviance

xplained = 99.5% and 96.1% for temperature and salinity, respec-ively) (Fig. 8b and c). Mature males were associated with deeperites and juveniles with intermediate temperatures and salinityalues.

0.78 0.05 0.02 0.16 1.120.83 0.17 – – 0.960.78 0.05 0.02 0.15 1.11

The CE Atlantic and SE Atlantic datasets were not adequate forCCA because they were dominated by immature specimens. In theCE Atlantic 92% of the juveniles occurred shallower than 1000 m.Juveniles and immature specimens co-occurred in the same haulsbut each instance either juveniles or immature specimens clearlydominated.

4. Discussion

Progress in understanding the population structure of the Por-tuguese dogfish, leafscale gulper shark and birdbeak dogfish hasbeen impaired by the difficulty of compiling and comparing datafrom the many different geographical areas and jurisdictionalwaters where these species occur. This study combined availablebiological information from research surveys and sampling of com-mercial catch to understand the population dynamics of thesespecies within each region. However, the likely effects of differ-ent fishing gears limited some analyses among areas and withinregions to qualitative or semi-quantitative descriptions. Previouslypublished finer-scale spatial resolution analysis identified that sizefrequencies and selectivity ogives for Portuguese dogfish and bird-beak dogfish off Ireland differed between trawls and longlines(Clarke et al., 2005). In this study, trawls and longlines adequatelysampled all maturity stages and sizes, except for juveniles, whichwere primarily caught with trawls. It was hoped that the use ofpresence/absence of maturity stages in each haul minimized thisgear effect.

4.1. Species distribution

The combined data for the Portuguese dogfish, leafscale gulpershark and birdbeak dogfish indicate that all three species are widelydistributed at a global scale. Regional differences in bathymetricdistributions were observed; the leafscale gulper shark specimenswere mainly caught between 600 and 1500 m in the NE Atlantic,with occasional records in down to 3300 m. The depth range fromthe New Zealand region (SW Pacific) extended into shallower water(361 m) to at least 1250 m (with 1300 m the maximum depth sam-pled in this region). Its average range clearly overlaps that of the

birdbeak dogfish, but is shallower than that of the Portuguesedogfish, which was regularly sampled as deep as 2000 m, with occa-sional records down to 2800 m. Spatial distribution patterns alsodiffered among species, as discussed below.

T. Moura et al. / Fisheries Research 157 (2014) 47–61 57

Fig. 7. Birdbeak dogfish. Occurrences of (a) juveniles, (b) mature males and females; (c) pregnant and post-natal females in the NE Atlantic; of (d) juveniles, (e) mature malesa f (g) juS

4

s

nd females; (f) pregnant and post-natal females in the CE Atlantic (Mauritania); oW Pacific (New Zealand).

.2. Sex ratio and population segregation

Variations in sex ratio must be considered when assessingpecies population dynamics, particularly in those areas where

veniles, (h) mature males and females; (i) pregnant and post-natal females in the

fishing pressure is high. In all three species, sex ratio varied with,geographical area and is likely to vary with depth. This variabil-ity might be associated with sex or maturity stage segregation andrequires a more detailed data.

58 T. Moura et al. / Fisheries Research 157 (2014) 47–61

-3 -2 -1 0 1 2

-3-2

-10

1Birdbeak do gfish, SW Paci fic

CCA1

CC

A2

Juveniles

Immatu reF

MatureF

Pregnant

Postnatal

Immatu reM

MatureM

34.4

34.45

34.5 34.55

34.6

34.65 34.7

-3 -2 -1 0 1

01

23

Birdbeak dogfish, NE A tlantic

CCA1

CA

1

Immatu reF

MatureF

Pregnant

Postnatal

Immatu reM

MatureM 4

00

500

600 700

800

900 1000

1100

120

0

-3 -2 -1 0 1 2

-3-2

-10

1

Birdbeak dogfish, SW Pacific

CCA1

CC

A2

Juveniles

ImmatureF

MatureF

Pregnant

Postnatal

ImmatureM

MatureM

4

4.5 5

5.5 6

6.5 7

7.5

8 8.5 9

a

b c

Fig. 8. Constrained correspondence analysis of birdbeak dogfish distribution by maturity stage. Ordination of the maturity stages (black circles) and hauls (grey circles)overlaid with the surface model fitted for (a) depth in the NE Atlantic (n = 2672; 310 hauls) for (b) depth (in metres) and (c) salinity (in PSU) in the SW Pacific (New Zealand,n arianc3

btaat1sst

= = 7508; 445 hauls). In the NE Atlantic analysis axis 1 accounted for 100% of the v9% of the variance of the fitted values, respectively.

The three species share some similarity in patterns of distri-ution by sex and maturity stage. For example, pregnant femalesended to be spatially segregated from the rest of the population,s well as mature and post-natal females of leafscale gulper sharknd birdbeak dogfish. The distribution of the different reproduc-ive stages has often been related to depth (e.g. Yano and Tanaka,

988; Girard and Du Buit, 1999; Clarke et al., 2002), and depth washown to be an important factor in the distribution of all threepecies in this analysis. Temperature and salinity were also impor-ant. Results suggest that habitat requirements change through the

e of the fitted values whereas in the SW Pacific axis 1 and 2 accounted for 61% and

different life phases of these sharks. Season was not found to sig-nificantly affect the occurrence of maturity stages, which likelyreflects the longer-than-annual reproductive cycle known to occurin squaliform sharks (Kyne and Simpfendorfer, 2010).

Despite relatively extensive sampling of research and com-mercial catches in the NE Atlantic, neonates and small immature

specimens (juveniles) were scarce for all three species, as previ-ously reported in a number of individual studies (Girard and DuBuit, 1999; Clarke et al., 2002; Banon et al., 2006; Figueiredo et al.,2008; Severino et al., 2009). In contrast, high numbers of juveniles

s Rese

wScitct((

HrihlhrwsSuacTtid

pTiifHoalCebljaBclttvcetrpa

oAedlw

(ui

T. Moura et al. / Fisherie

ere caught in other areas such as CE Atlantic, SE Atlantic, andW Pacific. The data collected in these regions are not adequate toonfidently infer the habitat preferences of neonates and smallermmature specimens in the NE Atlantic. However, the absence ofhese small fish in the NE Atlantic may be a consequence of theironcentration in nurseries outside the sampling areas, movemento/occurrence in pelagic (Compagno et al., 1991) or deeper watersJakobsdóttir, 2001; Banon et al., 2006) and/or by gear selectivityIrvine et al., 2012).

The concentration of juvenile sharks in nurseries, defined byeupel et al. (2007) as aggregations in spatially separated locations

epeatedly used across years, is a relatively common phenomenonn elasmobranchs. Such areas are suggested to provide suitableabitats for somatic growth due to high prey abundance and

ow mortality rates, although this assumption might not alwaysold true (Heupel et al., 2007). In Japan, juveniles of the closelyelated Owston’s dogfish (Centroscymnus owstonii, Somniosidae)ere found outside Suruga Bay, in around 300–800 m water depth,

hallower than the adult population (Yano and Tanaka, 1988).piny dogfish (Squalus acanthias, Squalidae) neonates, poorly doc-mented off the US east coast, were recently found in a particularrea, in shallower and colder waters than the adults, and also asso-iated with a different type of substrate (Sulikowski et al., 2013).he existence of nursery areas seems a plausible explanation forhe high numbers of neonates and smaller immature fish observedn particular locations comparative to other areas of the overallistribution range for the species in this study.

Another possible explanation for these early life stages beingoorly documented in the NE Atlantic region is gear selectivity.rawl nets using comparatively smaller mesh codends were usedn CE Atlantic, SE Atlantic, and SW Pacific, and could have resultedn a higher retention of juveniles, as has been previously reportedor the birdbeak dogfish in the SW Pacific (Irvine et al., 2012).owever, it is unlikely that differences in size composition couldnly be ascribed to gear selectivity since small-sized species, suchs the lantern sharks (Etmopterus spinax and Etmopterus pusil-us, Etmopteridae; maximum TL = 60 cm and 50 cm, respectively,ompagno et al., 2005) are frequently caught by the longline fish-ries (e.g. Armstrong, 2010), and in research trawl surveys. It shoulde noted that data from the SW Pacific (New Zealand) for the

eafscale gulper shark and for the birdbeak dogfish indicated thatuvenile specimens co-occurred with other maturity stages in somereas, e.g., the northern slopes of the Chatham Rise and on Puysegurank south of New Zealand. In the CE Atlantic, where a signifi-ant concentration of juveniles was also observed, an experimentalongline haul fished approximately 15 m off the sea floor and cap-ured only large specimens which were seldom recorded in therawl samples (P. Pascual, personal communication). These obser-ations suggest that juveniles and adults of the three species mighto-occur in the same area or potential nurseries, but have differ-nt habitat and/or prey choices, with juveniles being more benthichan adults. In fact, ontogenetic differences in the diet are usuallyeported for elasmobranchs with modifications from a benthic to aelagic feeding strategy in some species (Farias et al., 2006; Hallettnd Daley, 2011).

Given the results presented here, it is likely that a combinationf factors could be hampering the detection of juveniles in the NEtlantic. Further investigations in the NE Atlantic should includexperiments to test habitat hypotheses, such as sampling greaterepths, “untrawlable” hard substrates and the use of vertical long-

ines to assess the relative position of the different life stages in theater column.

The probability of occurrence of larger immature specimens>55 or 60 cm) of all three species increased with depth (partic-larly for females), with the exception of the birdbeak dogfish

n SW Pacific. In addition, immature specimens of both sexes of

arch 157 (2014) 47–61 59

Portuguese dogfish and birdbeak dogfish may aggregate accordingto age or size, as suggested by the CCA models.

Mature males of leafscale gulper shark and birdbeak dogfishwere more broadly distributed than mature females, supportingthe possibility of sex-biased dispersal in these species. A geneticpopulation study has shown that male leafscale gulper sharks havehigher levels of male-mediated gene flow in comparison to females,which were found to have more limited dispersal (Verissimo et al.,2012). Sex-biased dispersal has been documented for other sharkspecies (Pardini et al., 2001; Portnoy et al., 2010; Daly-Engel et al.,2012) and has been related to the reproductive philopatry offemales that, in some elasmobranchs species, return to specificareas to give birth (Hueter et al., 2005).

The aggregation of pregnant females of all the three speciespreferentially occurred at relatively warmer and/or shallowerdepths. These conditions are favourable to embryonic develop-ment as physiological processes are accelerated (Economakis andLobel, 1998; Robbins, 2007). Another possible trigger for segre-gation might be related to specific nutritional requirements ofpregnant females that could necessitate their migration to par-ticular grounds. In the case of the birdbeak dogfish, matrotrophyappears to occur (Paiva et al., 2012), whilst the Portuguese dogfishand leafscale gulper shark are assumed to be lecithotrophic (Mouraet al., 2011b; Figueiredo et al., 2008), although the existence of sup-plemental maternal nourishment (e.g. histotrophy) has never beenstudied in the latter.

4.3. Portuguese dogfish

The Portuguese dogfish was the only species where matureand pregnant females were regularly caught in multiple regions,with mature fish often comprising over 50% of all females sampled(e.g. NE Atlantic and Australia, SW Pacific). The occurrence of alladult reproductive stages within the same geographical area and,in many cases in similar proportions, suggests that this species isable to complete its life cycle within these areas. However, this isnot incompatible with a widespread mixing across the continu-ous distribution of the species. Indeed, an apparent lack of geneticstructure was found for the NE and CE Atlantic, and a large scalemigration of the NE specimens to the CE Atlantic waters to give birthhas been proposed (Verissimo et al., 2011). However, the captureof even low numbers of small specimens, post-natal and pregnantfemales with near-term embryos in a number of areas of the NEAtlantic (Girard and Du Buit, 1999; Clarke et al., 2001; Banon et al.,2006; Figueiredo et al., 2008), suggests that the existence of undis-covered concentration areas of juveniles in the NE Atlantic may alsobe hypothesized.

The only other published studies for this species outside theNE Atlantic are from Suruga Bay (Japan), and are in agreementwith those presented here: all maturity stages except juvenileswere commonly found, and sexual segregation was evident, withpregnant and mature females commonly found shallower than theremaining specimens (Yano and Tanaka, 1984, 1988).

4.4. Leafscale gulper shark

In most regions, immature females of leafscale gulper shark pre-dominated over mature females, and pregnant individuals wererare. The distribution pattern formerly assumed for this speciesin the NE Atlantic is based on the proposed existence of a largescale migration, where females would give birth off the MadeiraArchipelago, from which there are reports of pregnant females

(Severino et al., 2009). In the combined dataset presented here,pregnant females were also found off Iceland, indicating anotherpotentially important reproductive area in the northern part of theNE Atlantic. Occasional captures of pregnant females off Portugal

6 s Rese

aet(wOadd

4

tpacscteotpasidtewacilIarA(dcf

4

ug2aswciitesdpwsgs

0 T. Moura et al. / Fisherie

nd off Galicia have also been reported (Banon et al., 2006). Thexistence of migratory patterns for this species is proposed forhe SW Pacific too, where all the maturity stages were presentalthough with pregnant females being rare), but were associatedith specific geographical areas at a certain time in their life cycle.ur data also suggest the existence of at least two nursery groundslong western Africa, in Mauritania and Namibia, but no geneticifferentiation between Eastern Atlantic and South Africa has beenetected yet (Verissimo et al., 2012).

.5. Birdbeak dogfish

All life stages of the birdbeak dogfish were recorded in most ofhe regions analysed, although with some differences in the pro-ortions of maturity stages (or lack of some) among geographicalreas. Based upon the minimal size overlap between specimensaught off Ireland and those caught off Portugal, Clarke et al. (2002)uggested that the birdbeak dogfish undergoes a migration alongontinental slopes between Irish and Portuguese waters, similaro that has been postulated for New Zealand populations, wherextensive migrations associated with reproduction are thought toccur (Clark and King, 1989). Our data support breeding migra-ions. However, in the NE Atlantic, all maturity stages, includingregnant and post-natal females, were present in almost all areas,nd at least 50% of males were mature. Juveniles were caught inmall numbers on Hatton Bank and off the SW of Portugal, suggest-ng the existence of more than one nursery area, likely at shallowerepths. In the CE and SE Atlantic, despite the dominance of imma-ure specimens, mature fish were also relatively common (morevident in the SE Atlantic), but pregnant and post-natal femalesere scarce or lacking. In New Zealand waters, juvenile fish were

bundant, particularly on the Chatham Rise and off the easternoast of the North Island, but the proportions of mature fish var-ed by geographical area. Pregnant females were encountered inow numbers, and only on Chatham Rise and around the Northsland. The results suggest the existence of population partitioningccording to life stage, particularly for pregnant stages, despite theirarity. Similarly, the occurrence of pregnant females was rare on theustralian continental slope (Irvine et al., 2012). Here, juveniles

30–60 cm) were the major component of the catch in shallowerepth strata (700–900 m) reflecting possible regional differencesompared to the New Zealand population, where juveniles wereound at intermediate depths, in relation to other maturity stages.

.6. Management implications

The successful management of deepwater sharks relies on annderstanding of the spatial and temporal distribution of the demo-raphic components of their populations (Wearmouth and Sims,008). This knowledge is required for the development of man-gement measures that ensure the stability of their demographictructure (Simpfendorfer and Heupel, 2004), especially in caseshere exploitation impacts differ at regional scales. The identifi-

ation of the life stages most critical and vulnerable to exploitations also essential, and if adequate information is made available,t will be possible to establish specific regulations, probably spa-ially/depth structured, to preserve those stages as well as theirssential habitats (Simpfendorfer and Heupel, 2004). The presenttudy contributes to these management goals by compiling manyifferent data sources to make progress in elucidating the likelyopulation structure, habitats and migration patterns of deep-

ater sharks. The resulting hypotheses need to be tested in future

tudies, particularly to elucidate migrations, and further investi-ate spatial distribution and preferential habitats for these threepecies.

arch 157 (2014) 47–61

Despite some similarities in the distribution patterns of thethree species studied, there are differences in habitat usage by sexand by life history stage. Given their scarcity in our data, it is likelythat neonates and small immature sharks, and pregnant femaleleafscale gulper shark and birdbeak dogfish (in some regions),are not directly impacted by current fishing pressure. However,it is important to note that the protection of nursery areas alonemay not be sufficient to conserve a shark population (Kinney andSimpfendorfer, 2009). The available data also suggests that thesefisheries have impacted only portions of the whole population anddistribution area of these three species: the spatial extent of com-mercial fishing is limited and is therefore unlikely to overlap withtheir full distribution.

This study was innovative in collating worldwide informationfor these wide-ranging species. The continuation of such collabo-rative data pooling is essential to update life-history data, spatialand temporal information. It is also necessary to implement stan-dardized, long-term and broader-scale monitoring programs thatwill enable the determination of the stock status (Ward-Paige et al.,2012). There is currently no standardized sampling at a global scale,but coordinated efforts are required for adequate stock assess-ments as well as monitoring the impacts of fishing on these species.Future studies should also focus on other ecological factors influ-encing the demographic-specific distributions of each population,such as oceanographic conditions, substrate characterization andprey interactions. Such factors are important for understanding theresponse of populations to either anthropogenic-induced changesor environmental variations.

Acknowledgements

The authors would like to thank Miguel Santos and Jim O.Roberts for their support with mapping software and climatologicalgrid data extraction, respectively. We also thank Andy Williston andJack Musick (NW Atlantic), Malcolm Clark (New Zealand), Deep-Cproject (www.deep-c.org; Gulf of Mexico) and TUBAPROF (MARE22-05-01-FEDER-00028; Portugal) for their assistance in collat-ing, interpreting data and/or providing data for this study. Weare also grateful to the two anonymous reviewers for their help-ful comments. T. Moura and I. Figueiredo were partially supportedby PNAB (EU DCR) and CERTIFICA (PROMAR 31-03-01-FEP-0032).The contribution of T. Moura, G. Diez, K. Jakobsdottir, P. Loranceand I. Figueiredo received financial support from the and FP7-DEEPFISHMAN project (Management and Monitoring of Deep-SeaFisheries and Stocks, Grant agreement no.: 227390). The contribu-tion of E. Jones was funded by an International Mobility Fund grantfrom the Royal Society of New Zealand (contract no: ISATA10-29).

Appendix A. Supplementary data

Supplementary data associated with this article can befound, in the online version, at http://dx.doi.org/10.1016/j.fishres.2014.03.019.

References

Antonov, J.I., Seidov, D., Boyer, T.P., Locarnini, R.A., Mishonov, A.V., Garcia, H.E., Bara-nova, O.K., Zweng, M.M., Johnson, D.R., 2010. Volume 2: salinity. In: Levitus, S.(Ed.), World Ocean Atlas 2009. NOAA Atlas NESDIS 69. U.S. Government PrintingOffice, Washington, DC.

Armstrong, M., 2010. Joint data collection between the fishing sector and thescientific community in Western Waters. In: Final Report to the European Com-mission, Directorate-General for the Fisheries and Maritime Affairs. ContractSI2.491885, Ref. FISH/2007/03 Lot 1. European Commission.

Banon, R., Pineiro, C., Casas, M., 2006. Biological aspects of deep-water sharksCentroscymnus coelolepis and Centrophorus squamosus in Galician waters (north-western Spain). J. Mar. Biol. Assoc. U.K. 86, 843–846.

Borcard, D., Gillet, F., Legendre, P., 2011. Numercal Ecology with R. Springer, NewYork, NY.

s Rese

C

C

C

C

C

C

D

E

F

F

G

G

G

H

H

H

I

I

J

K

K

L

M

M

M

M

O

T. Moura et al. / Fisherie

lark, M.R., King, K.J., 1989. Deepwater fish resources off the North Island, NewZealand: results of a trawl survey, May 1985 to June 1986. In: New ZealandFisheries Technical Report 11. New Zealand Fisheries.

larke, M.W., Connolly, P.L., Bracken, J.J., 2001. Aspects of reproduction of the deep-water sharks Centroscymnus coelolepis and Centrophorus squamosus from westof Ireland and Scotland. J. Mar. Biol. Ass. UK 81, 1019–1029.

larke, M.W., Connolly, P.L., Bracken, J.J., 2002. Catch, discarding, age estimation,growth and maturity of the squalid shark Deania calceus west and north ofIreland. Fish. Res. 56, 139–153.

larke, M.W., Borges, L., Officer, R.A., 2005. Comparisons of trawl and longline catchesof deepwater elasmobranchs west and north of Ireland. J. Northwest Atl. Fish.Sci. 35, 429–442.

ompagno, L., Dando, M., Fowler, S., 2005. Sharks of the World. Collins Field Guide.London, Harper Collins Publishers.

ompagno, L.J.V., Ebert, D.A., Cowley, P.D., 1991. Distribution of offshore demersalcartilaginous fish (class Chondrichthyes) off the west coast of southern Africa,with notes on their systematics. S. Afr. J. Mar. Sci. 11, 43–139.

aly-Engel, T.S., Seraphin, K.D., Holland, K.N., Coffey, J.P., Nance, H.A., Toonen,R.J., Bowen, B.W., 2012. Global phylogeography with mixed-marker analysisreveals male-mediated dispersal in the endangered scalloped hammerheadshark (Sphyrna lewini). PLoS One 7, e29986.

conomakis, A.E., Lobel, P.S., 1998. Aggregation behavior of the grey reef shark, Car-charhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environ. Biol.Fishes 51, 129–139.

arias, I., Figueiredo, I., Moura, T., Gordo, L., Neves, A., Serra-Pereira, B., 2006. Dietcomparison of four ray species (Raja clavata, Raja brachyura, Raja montagui andLeucoraja naevus) caught along the Portuguese continental shelf. Aquat. LivingResour. 19, 105–114.

igueiredo, I., Moura, T., Neves, A., Gordo, L.S., 2008. Reproductive strategy ofleafscale gulper shark, Centrophorus squamosus, and Portuguese Dogfish, Cen-troscymnus coelolepis, on the Portuguese continental slope. J. Fish Biol. 73,206–225.

arcia, V.B., Lucifora, L.O., Myers, R.A., 2008. The importance of habitat and life his-tory to extinction risk in sharks, skates, rays and chimaeras. P roc. R. Soc. London,Ser. B: Biol. Sci. 275, 83–89.

irard, M., Du Buit, M.H., 1999. Reproductive biology of two deep-water sharks fromthe British Isles, Centroscymnus coelolepis and Centrophorus squamosus (Chon-drichthyes: Squalidae). J. Mar. Biol. Assoc. U.K. 79, 923–931.

raham, K.J., Daley, R.K., 2011. Distribution, reproduction and population structureof three gulper sharks (Centrophorus, Centrophoridae) in southeast Australianwaters. Mar. Freshwater Res. 62, 583–595.

allett, C.S., Daley, R.K., 2011. Feeding ecology of the southern lanternshark(Etmopterus baxteri) and the brown lanternshark (E. unicolor) off southeasternAustralia. ICES J. Mar. Sci. 68, 157–165.

eupel, M.R., Carlson, J.K., Simpfendorfer, C.A., 2007. Shark nursery areas: concepts,definition, characterization and assumptions. Mar. Ecol. Prog. Ser. 337, 287–297.

ueter, R.E., Heupel, M.R., Heist, E.J., Keeyney, D.B., 2005. Evidence of philopatry insharks and implications for the management of shark fisheries. J. Northwest Atl.Fish. Sci. 35, 239–247.

OC, IHO, BODC, 2003. Centenary Edition of the GEBCO Digital Atlas. IOC, IHO andBODC, Liverpool (Published on CD-ROM on behalf of the IntergovernmentalOceanographic Commission and the International Hydrographic Organizationas part of the General Bathymetric Chart of the Oceans).

rvine, S.B., Daley, R.K., Graham, K.J., Stevens, J.D., 2012. Biological vulnerabilityof two commercial gulper sharks (Deania, Centrophoridae) from southeasternAustralia. J. Fish Biol. 80, 1181–1206.

akobsdóttir, K.B., 2001. Biological aspects of two deep-water squalid sharks: Cen-troscyllium fabricii (Reinhardt, 1825) and Etmopterus princeps (Collett, 1904) inIcelandic waters. J. Fish Biol. 51, 247–265.

inney, M.J., Simpfendorfer, C.A., 2009. Reassessing the value of nursery areas toshark conservation and management. Conserv. Lett. 2, 53–60.

yne, P.M., Simpfendorfer, C.A., 2010. Deepwater chondrichthyans. In: Carrier, J.C.,Musick, J.A., Heithaus, M.R. (Eds.), Sharks and Their Relatives II—Biodiversity,Adaptive Physiology, and Conservation. CRC Press, Boca Raton, FL,pp. 37–113.

ocarnini, R.A., Mishonov, A.V., Antonov, J.I., Boyer, T.P., Garcia, H.E., Baranova, O.K.,Zweng, M.M., Johnson, D.R., 2010. Volume 1: temperature. In: Levitus, S. (Ed.),World Ocean Atlas 2009. NOAA Atlas NESDIS 68. U.S. Government PrintingOffice, Washington, DC.

cLaughlin, D.M., Morrissey, J.F., 2005. Reproductive biology of Centrophorus cf.uyato from the Cayman Trench, Jamaica. J. Mar. Biol. Assoc. U.K. 85, 1–8.

oura, T., Serra-Pereira, B., Gordo, L.S., Figueiredo, I., 2011a. Sperm storage in malesand females of the deepwater shark Portuguese dogfish with notes on oviducalgland microscopic organization. J. Zool. 283, 210–219.

oura, T., Nunes, C., Bandarra, N., Gordo, L.S., Figueiredo, I., 2011b. Embryonicdevelopment and maternal-embryo relationships of the Portuguese dogfish Cen-troscymnus coelolepis. Mar. Biol. 158, 401–412.

unoz-Chapuli, R., 1984. Éthologie de la reproduction chez quelques requins del’Atlantique nord-est. Cybium 8, 1–14.

ksanen, J., 2011. Multivariate Analysis of Ecological Communities in R: Vegan Tuto-rial, Available at 〈http://cc.oulu.fi/∼jarioksa/opetus/metodi/vegantutor.pdf〉(accessed 22 February 2013).

arch 157 (2014) 47–61 61

Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B.,Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2012. Vegan:community ecology package. In: R Package Version 2.0-4, 〈http://CRAN.R-project.org/package=vegan〉 (accessed 22 February 2013).

Paiva, R.B., Neves, A., Sequeira, V., Nunes, M.L., Gordo, L.S., Bandarra, N., 2012. Repro-ductive strategy of the female deep-water shark birdbeak dogfish, Deania calcea:lecithotrophy or matrotrophy. J. Mar. Biol. Assoc. U.K. 92, 387–394.

Pardini, A.T., Jones, C.S., Noble, L.R., Kreiser, B., Malcolm, H., Bruce, B.D., Stevens, J.D.,Cliff, G., Scholl, M.C., Francis, M.P., Duffy, C.A.J., Martin, A.P., 2001. Sex-biaseddispersal of great white sharks. Nature 412, 139–140.

Portnoy, D.S., McDowell, J.M., Heist, E.J., Musick, J.A., Graves, J.E., 2010. World phy-logeography and male-mediated gene flow in the sandbar shark, Carcharhinusplumbeus. Mol. Biol. 10, 1994–2010.

Pratt, H.L., Casey, J.G., 1990. Shark reproductive strategies as a limiting factor indirected fisheries, with a review of Holden’ method of estimating growth param-eters. In: Pratt Jr., H.L.S., Gruber, H., Taniuchi, T. (Eds.), Elasmobranchs as LivingResources: Advances in the Biology, Ecology, Systematics and the Status of theFisheries. NOAA Technical Report NMFS 90. NOAA, pp. 97–109.

R Core Team, 2012. R: A Language and Environment for Statistical Computing.R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0〈http://www.R-project.org〉 (accessed 22 February 2013).

Robbins, R.L., 2007. Environmental variables affecting the sexual segregation of greatwhite sharks Carcharodon carcharias at the Neptune Islands South Australia. J.Fish Biol. 70, 1350–1364.

Sarkar, D., 2008. Lattice: Multivariate Data Visualization with R. Springer, New York,NY.

Schlitzer, R., 2011. Ocean Data View, 〈http://odv.awi.de〉 (accessed 22 February2013).

Severino, R., Afonso-Dias, I., Delgado, J., Afonso-Dias, M., 2009. Aspects of the biologyof the leaf-scale gulper shark Centrophorus squamosus (Bonnaterre, 1788) offMadeira archipelago. Arquipélago—Life Mar. Sci. 26, 57–61.

Simpfendorfer, C.A., Heupel, M.R., 2004. Assessing habitat use and movement. In:Carrier, J.C., Musick, J.A., Heithaus, M.R. (Eds.), Biology of Sharks and their Rela-tives. CRC Press, Boca Raton, FL, pp. 553–572.

Simpfendorfer, C.A., Kyne, P.M., 2009. Limited potential to recover from overfishingraises concerns for deep-sea sharks, rays and chimaeras. Environ. Conserv. 36,97–103.

Sims, D.W., 2005. Differences in habitat selection and reproductive strategies of maleand female sharks. In: Ruckstuhl, K.E., Neuhaus, P. (Eds.), Sexual Segregation inVertebrates: Ecology of the Two Sexes. Cambridge University Press, New York,NY, pp. 127–147.

Stehmann, M., 2002. Proposal of a maturity stages scale for oviparous and viviparouscartilaginous fishes (Pisces, Chondrichthyes). Arch. Fish. Mar. Res. 50, 23–48.

Stevens, J., 2003. Deania calcea. In: IUCN 2011. IUCN Red List of Threatened Species.Version 2011.1. IUCN, 〈http://www.iucnredlist.org〉 (accessed 29th September2011).

Stevens, J., Correia, J.P.S., 2003. Centroscymnus coelolepis. In: IUCN 2011. IUCN RedList of Threatened Species. Version 2011.1. IUCN, 〈http://www.iucnredlist.org〉(accessed 29th September 2011).

Sulikowski, J.A., Prohaska, B.K., Carlson, A.E., Cicia, A.M., Brown, C.T., Morgan, A.C.,2013. Observations of neonate spiny dogfish, Squalus acanthias, in Southern NewEngland: a first account of a potential pupping ground in the NorthwesternAtlantic. Fish. Res. 137, 59–62.

ter Braak, C.J.F., 1986. Canonical correspondence analysis: a new eigenvector methodfor multivariate direct gradient analysis. Ecology 67, 1167–1179.

ter Braak, C.J.F., Verdonschot, P.F.M., 1995. Canonical correspondence analysis andrelated multivariate methods in aquatic ecology. Aquat. Sci. 57, 255–289.

Verissimo, A., McDowell, J.R., Graves, J.E., 2011. Population structure of a deep-watersqualoid shark, the Portuguese dogfish (Centroscymnus coelolepis). ICES J. Mar.Sci. 68, 555–563.

Verissimo, A., McDowell, J.R., Graves, J.E., 2012. Genetic population structureand connectivity in a commercially exploited and wide-ranging deepwatershark, the leafscale gulper (Centrophorus squamosus). Mar. Freshwater Res. 63,505–512.

Ward-Paige, C.A., Keith, D.M., Worm, B., Lotze, H.K., 2012. Recovery potential andconservation options for elasmobranchs. J. Fish Biol. 80, 1844–1869.

Wearmouth, V.J., Sims, D.W., 2008. Sexual segregation in marine fish, reptiles, birdsand mammals: behaviour patterns, mechanisms and conservation implications.Adv. Mar. Biol. 54, 107–170.

Wetherbee, B.M., 1996. Distribution and reproduction of the southern lanternsharkEtmopterus granulosus from New Zealand. J. Fish Biol. 49, 1186–1196.

White, W.T., 2003. Centrophorus squamosus. In: IUCN 2011. IUCN Red List of Threat-ened Species. Version 2011.1. IUCN, 〈http://www.iucnredlist.org〉 (accessed 29thSeptember 2011).

Woodhams, J., Vieira, S., Stobutzki, I., 2012. Fishery Status Reports 2011. AustralianBureau of Agricultural and Resource Economics and Sciences, Canberra.

Yano, K., Tanaka, S., 1984. Some biological aspects of the deep-sea squaloid

shark Centroscymnus from Suruga Bay, Japan. Bull. Jpn. Soc. Sci. Fish. 50,249–256.

Yano, K., Tanaka, S., 1988. Size at maturity, reproductive cycle, fecundity and depthsegregation of the deep-sea squaloid sharks Centroscymnus owstoni and C.coelolepis in Suruga Bay. Nippon Suisan Gakk. 54, 167–174.