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Research Article
Evidence of Sperm Storage in
Nursehound (Scyliorhinus stellaris, Linnaeus 1758):
Juveniles Husbandry and Tagging Program
Primo Micarelli,1Emilio Sperone,2Fabrizio Serena,3and Leonard J. V. Compagno4
1Aquarium Mondo Marino, Centro Studi Squali, Massa Marittima, Italy
2DipartimentodiBiologia,EcologiaeScienzedellaTerra,Universit
`
a della Calabria, Rende, Italy
3Responsabile Unit`
aOperativaRisorsaItticaeBiodiversit
`
a Marina, ARPAT Settore Mare, Via Marradi 114, 57100 Livorno, Italy
4Shark Research Center, 8 Lower Glen Road, Glencairn, South Africa
Correspondence should be addressed to Primo Micarelli; primo.micarelli@gmail.com
Received March ; Revised June ; Accepted June
Academic Editor: Heinrich H¨
uhnerfuss
Copyright © Primo Micarelli et al. is is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Nursehound, Scyliorhinus stellaris (Linnaeus ), is a shark of the Scyliorhinidae family, close to the Scyliorhinus canicula (Lin-
naeus ), frequently hosted in public aquaria. Information on biology and ecology is deciently available regarding this species
of sharks. In the Mediterranean basin, they are occasional rare and vulnerable species (Serena, ). In a female specimen
of Scyliorhinus stellaris, cm long, shed in the Tyrrhenian Sea was transferred to Tuscany Argentario Mediterranean Aquarium
and placed in a . L tank. e female laid eggs and juveniles were born on and . ey were transferred to the
aquarium laboratory in order to get standard protocol for correct juveniles husbandry. Aer a total of -month observations,
some of them were tagged and let free on . To collect data about nursehound shark needs in terms of feeding and growing in
captivity, especially during the rst life years, is a necessary and fundamental step in order to develop a Mediterranean program
of tagging and study in the eld of conservation policy proposal. Husbandry protocol for this species’ juveniles was developed in
this study. is is the rst reported case of a nursehound storing sperm for years, in captivity (Pratt, ; Hamlett et al., ;
Awr uch , ).
1. Introduction
e Scyliorhinus stellaris (Linnaeus ) is a benthonic shark.
It is distributed in the Mediterranean Sea, being absent from
theBlackSea,anditalsooccursintheAtlanticOcean,from
Shetlands and southern Scandinavia to Senegal being rare in
the North Sea. Greater-spotted dogsh (S. stellaris)isarare
species. At the southern and western coasts of the British
Isles, the species occurs over shallow rough inshore grounds
(e.g., Gower Peninsula, Pembrokeshire, and Lleyn Peninsula)
at depths from to m deep, where maximum catch
rate is ind.hr.−1 [,Fig.b].IntheMediterraneanSea,data
from MEDITS surveys indicated that the species could be
caught down to m deep, extending its previous bathy-
metric range []. e species feeds on crustaceans, molluscs,
and small shes, which may include small specimens of the
species [, ]. Although the maximum size of the species is set
as cm, length of larger shed specimens varies from to
cm.isspeciesleavesonrockybottomanditisbigger
than small-spotted catshark Scyliorhinus stellaris (Linnaeus
); female is mature at about cm and male at cm
[]. e conservation and exploitation status is: FAO, B;
Mediterranean, rare and vulnerable species []. Egg-cases of
S. stellaris were never caught in large numbers, and it is likely
that they are laid in shallow water, attached to macroalgae
[, ]. e Scyliorhinus stellaris can be easily maintained in
captivity [], which facilitates the development of physiologi-
cal studies on the species observations [–]. In December
, a mature female shed in the Tyrrhenian Sea, was
transferred to the Argentario Aquarium, in a large tank with
otheryoungspecimens,femalesandmale.Duringthe
twoyearsofcaptivity,thematurefemalelaideggs.Someof
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International Journal of Oceanography
Volume 2016, Article ID 8729835, 5 pages
http://dx.doi.org/10.1155/2016/8729835
International Journal of Oceanography
the fertilised eggs completed embryonic development and
hatched in the aquarium. Juveniles were kept in the labora-
tory to observe growing rate and to obtain information on a
correct captivity husbandry protocol. is was the rst case
in which a female laid fertilised eggs during a -year period
in the absent of males [–]. is implies that sperm from
previousinseminationcouldbestoredinashellglandand
be viable aer years. Metten [] and Richards et al. []
have reviewed earlier evidence on sperm survival []. Some
of the juveniles, and months old, were tagged in the
aquarium for the National Elasmobranch tagging program
from Italian ARPAT (Tuscany Agency for Environmental
Protection)andletfreeonJuly,buttheywerenotshed
again until . e aim of this study was to verify a correct
husbandry protocol for juveniles. eir behaviour can be
observed during their growth and when they are years old,
they can be used for tagging programs to study sea nursery
and movements.
2. Material and Methods
2.1. Sexually Mature Female. Afemale,cmlong,shed
along the Argentario coasts, was transferred on December
in the exposition pelagic tank (. L) of Argentario
Mediterranean Aquarium, Tuscany. e pelagic aquarium is
equipped with external lter, controlled temperature, iodure
lamp w, % per week seawater changing, and a pipeline
directly keeping seawater in front of the aquarium at m
depth. Later the female laid eggs (Figure ); a total of eggs
werelaidin(groupA)andeggswerelaidin
(group B). All the eggs were laid between January and March
and hatched between August and September.
e laid eggs were transferred to the aquarium laboratory.
On late August of , eggs from group A completed the
embryonic development and hatched. Between August and
September , eggs from group B completed the embry-
onic development but only survived.
2.2. First Group A, 2004–2006/Second Group B, 2005-2006.
Every hatched egg was transferred to an aquarium in the
laboratory. Each aquarium was equipped with internal lter
for nanoreef aquarium, illuminated from the laboratory u-
orescent tubes watts from : to : in October–May
and from : to : in June–September. Twice a month the
% of aquarium water was changed by natural and ltered
seawater. During the rst months, juveniles were weekly
feed with food representing % of its body weight. Aer that,
the food increased to % of the body weight. Initially, at the
rst months, food consists in prawns and aer that it was
composed of anchovy. e total lengths (TL) were measured
on neonates and specimens to the nearest millimeter, and
the weight was measured with Hanna pce-pm t precision
balance. e same husbandry protocol was followed and the
data were collected for months for group A (–)
and along months for group B (-). e analysis
instruments include mercury thermometer, electronic pH-
meter, refractometer for salinity, eld Spectrophotometer
Hanna C-, for nitrates and nitrites, and Hanna pce-pm
tprecisionbalance.
F : Scyliorhinus stellaris egg.
T : Tagging information.
Tagging
Identication code Sex TL
Female , cm
Female , cm
Male , cm
Male cm
Female , cm
Male , cm
Male cm
2.3. Tagging and Free. In June , juveniles belonging to
group A and to group B were tagged (Figure ) following
the protocol for the National Elasmobranch Tagging Program
from ARPAT Tuscany Agency for Environmental Protection,
managed by Dr. Fabrizio SERENA, and seven were released
and let free on July (Figure ). e remaining juveniles were
maintained in the aquarium as control cases. Yellow short
strings tags with progressive number were placed in the
dorsal n (Table ).
3. Results
Betweenand,eggswerelaidandthengrouped
as A: rst –, B: second (-): juveniles
hatched in the laboratory where one specimen was hosted per
aquarium which were daily controlled and monitored. Of
those survived. Data on weight, total length, and weight of
food in gr weekly distributed were collected along months.
Water parameters such as T∘, pH, salinity, nitrates, and
nitrites were also collected. In group A, the total length of
specimens at birth varied between and mm; aer
months, specimens have a total length of . mm in average
and aer months they measured . mm (Figure ). In
group B, the total length at birth varied between and
mm; aer months, specimens have, in average, a total
length of mm, group B (Figure ). Length at birth was
similar in the two groups but the aquarium conditions were
slightly dierent.
Regarding weight, group A (Figure ) specimen varied at
birth between and gr, they attained a mean of , g
International Journal of Oceanography
F : Juvenile tagged with yellow short string.
F : Juveniles let free in Monte Argentario island on July
.
aer months and g aer months in these captivity and
feeding conditions.
Also group B (Figure ) varied between and gr when
born to be attaint in average g, aer months in the same
captivity and feeding protocol.
In group A, water temperature varied between ∘Cand
∘C, pH between and ,, salinity between and ‰,
and nitrites between , and , ppm and nitrates maxi-
mumwasppm,andingroupB,watervariedbetween
∘C
and ∘C, pH between , and ,, salinity between and
‰, and nitrites between , and , ppm and nitrates
maximum was , ppm.
4. Discussion
e female caught in laid eggs in the absence of mature
males. is derives from the capacity of Scyliorhinidae and
elasmobranchs in general to store sperm for at least - years
and fertilise the egg later. e tank where the female was
hosted contained one male specimen with cm length but
notsexuallymature.Inthefemalelaidandin.
istotalfecundityislowerthatwhatisreferredbyCapap
´
e
[], which indicated – per year in natural conditions
[].Atotalofofeggswereabletocompletethe
embryonic development in individual aquarium. is means
that % of fertilised eggs survived which is also lower than
what is estimated by Capap´
e et al. in natural conditions (%)
[]. e surviving percentage of neonates was % ( of
neonates survived), which is higher than % determined
by Capap´
eetal.[].Botheggslaidinandin
Juveniles Length (Scyliorhinus stellaris)
First group
12345
Length (cm)
Series 1
Series 2
Series 4
Series 5
Series 6
Series 7
12
15
18
21
24
27
30
33
August 2004–February 2006 (19 months)
F : Total length group A.
Juveniles Length (Scyliorhinus stellaris)
Second group
12345
August 2005–June 2006 (11 months)
Series 1
Series 2
Series 3
Series 4
Series 5
Series 6
Series 7
Series 8
Series 9
12
14
16
18
20
22
Length (cm)
F : Total length group B.
hatched aer and months; this time interval is slightly
lower than the estimate by Serena [] for the Mediterranean
Sea ( months) and more than the months estimated by
Moreau [] and Ehrehbaum [] for S. stellaris specimens
in the Atlantic Ocean and North Sea. ese faster rates are
likely to be related to captivity conditions. Length of birth
was also larger than the estimate of Skaramuca and Prtenjaca
[] for Adriatic nursehounds in natural conditions (in
average mm). Such dierence contradicts Capap´
eetal.’s
hypothesis [] according to which in captivity the neonates
grow less than in natural conditions.
We decided to feed sharks with a quantity of weight food
per day, corresponding weekly to the total of food weight
included between and % of their body weight and change
it in function of juveniles length, daily needs, and ability to
search for food, in order to get a standard husbandr y protocol
to be used. Aer days, the mean length was, in rst group,
,mmand,insecondgroup,,mm;theselengthsin
Capap´
e et al. [] and Skaramuca and Prtenjaca [] were
reachedindays.Aermonthofcaptivity,young
specimens from group A have a growth rate in weight of
, gr per day while specimens from group B had a growth
of , gr per day aer months. Both values are about half
International Journal of Oceanography
Juveniles weight (Scyliorhinus stellaris)
First group
1234567
Weight (gr)
Series 1
Series 2
Series 4
Series 5
Series 6
Series 7
0
10
20
30
40
50
60
70
80
90
August 2004–February 2006 (19 months)
F : Weight group A.
Juveniles weight (Scyliorhinus stellaris)
Second group
12345
August 2005–June 2006 (11 months)
5
9
13
17
21
25
29
33
Weight (gr)
Series 1
Series 2
Series 3
Series 4
Series 5
Series 6
Series 7
Series 8
Series 9
F : Weight group B.
of the one observed by Capap´
e et al. []. All the juveniles
were in good health state and none died during - and -
month observations. In captivity embryos can hatch at the
same length as in natural conditions but during development
theweeklyfoodratioincaptivitycanbeincreasedtomore
than % and %. Seven specimens were tagged on June
with a yellow string with a code number useful to
identify them if shed. Other specimens were hosted in the
aquarium to be able to compare data with those let free on July
in the Argentario Tyrrhenian coast close to Porto Santo
Stefano village (Tuscany). In the program, the coast guard and
professional shermen were involved; no information about
the free juveniles was collected since until .
5. Conclusions
e captivity hatching and juveniles husbandry of nurse-
hound seem to be not particularly dicult in public aquaria
equipped with large tanks and laboratory; this husbandry
protocol permitted us to obtain a regular growing rate along
the observed period, and more information is needed to
establish at which age Tyrrhenian nursehound is sexually
matureincaptivity.Tolayandhatcheachyearfertilisedeggs,
it could be useful to research about reproductive physiology
ofbenthicsharksandtodevelopprogramsoftagginginthe
Mediterranean Sea, where conservation problems seem to
attend the nursehound population.
Competing Interests
e authors declare that they have no competing interests.
Acknowledgments
e authors thank Marco Tarantino, Luca de Lucia, Davide
Canetti, ARPAT, and Argentario Mediterranean Aquarium
for their contribution in tagging and letting the sharks free to
sea. e authors thank Miss Spinetti Sara for her contribution
in collecting some water chemical-physical parameters data
during the experience.
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