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Evidence of Sperm Storage in Nursehound ( Scyliorhinus stellaris , Linnaeus 1758): Juveniles Husbandry and Tagging Program

Authors:
  • Centro Studi Squali - Sharks Studies Centre - Scientific Institute
  • Institute for Biological Resources and Marine Biotechnology (IRBIM), National Research Council – CNR, Via Vaccara, 61 – 91026, Mazara del Vallo (Tp), Italy

Abstract and Figures

Nursehound, Scyliorhinus stellaris (Linnaeus 1758), is a shark of the Scyliorhinidae family, close to the Scyliorhinus canicula (Linnaeus 1758), frequently hosted in public aquaria. Information on biology and ecology is deficiently available regarding this species of sharks. In the Mediterranean basin, they are occasional rare and vulnerable species (Serena, 2005). In 2003 a female specimen of Scyliorhinus stellaris , 90 cm long, fished in the Tyrrhenian Sea was transferred to Tuscany Argentario Mediterranean Aquarium and placed in a 20.000 L tank. The female laid 42 eggs and juveniles were born on 2004 and 2005. They were transferred to the aquarium laboratory in order to get standard protocol for correct juveniles husbandry. After a total of 18-month observations, some of them were tagged and let free on 2006. To collect data about nursehound shark needs in terms of feeding and growing in captivity, especially during the first life years, is a necessary and fundamental step in order to develop a Mediterranean program of tagging and study in the field of conservation policy proposal. Husbandry protocol for this species’ juveniles was developed in this study. This is the first reported case of a nursehound storing sperm for 2 years, in captivity (Pratt, 1993; Hamlett et al., 2002; Awruch, 2007).
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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 deciently 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. Aer 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 dogsh (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,femalesandmale.Duringthe
twoyearsofcaptivity,thematurefemalelaideggs.Someof
Hindawi Publishing Corporation
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 aer 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,buttheywerenotshed
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)andeggswerelaidin
(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. Aer that,
the food increased to % of the body weight. Initially, at the
rst months, food consists in prawns and aer 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
Identication 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
Betweenand,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; aer 
months, specimens have a total length of . mm in average
and aer  months they measured . mm (Figure ). In
group B, the total length at birth varied between  and
 mm; aer  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 dierent.
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
.
aer months and  g aer  months in these captivity and
feeding conditions.
Also group B (Figure ) varied between  and  gr when
born to be attaint in average  g, aer  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-
mumwasppm,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.Inthefemalelaidandin.
istotalfecundityislowerthatwhatisreferredbyCapap
´
e
[], which indicated – per year in natural conditions
[].Atotalofofeggswereabletocompletethe
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.[].Botheggslaidinandin
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 aer 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 dierence 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. Aer  days, the mean length was, in rst group,
,mmand,insecondgroup,,mm;theselengthsin
Capap´
e et al. [] and Skaramuca and Prtenjaca [] were
reachedindays.Aermonthofcaptivity,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 aer  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 dicult 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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... The capacity for resilience of this species is affected by a low level of interconnectivity between isolated populations around islands far from the continental coast. Little information is available on its biology (Micarelli et al., 2006(Micarelli et al., , 2007(Micarelli et al., , 2016; however, we know that it is a large bodied species and it is likely more vulnerable to population depletion than the Smallspotted Catshark (Scyliorhinus canicula), which also occurs in this region. Given its large size, patchy distribution and evidence of decline in the Mediterranean Sea, an assessment of at least Near Threatened is warranted (IUCN Red List, 2009). ...
Research
Full-text available
The Nursehound, Scyliorhinus stellaris (Linnaeus, 1758), is a benthic catshark distributed in the Northeast and Eastern central Atlantic and throughout the Mediterranean. In the Mediterranean, the available data on exploitation is limited, while sharks’ decline has been indicated. In 2018 a new project was activated to locate, around the Monte Argentario Peninsula in Tuscany (Italy), the presence of Nursehound Nurseries using a new tool, Poseidon R.O.V. (Remote Operative Vehicle). The project, partially funded by the Tuscany Region (Go Green 2018), will allow it to identify egg-spawning areas. The f irst 3 years of observations, from 2018 to 2020, are presented here.
... Much of the knowledge we have on the elasmobranchs was built by research carried out within the aquaria in controlled conditions [1][2][3][4][5][6][7]. The small spotted catshark (Scyliorhinus canicula, Linnaeus 1758) is a common host of many aquaria through Europe. ...
Method
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While most people have no trouble in recognizing a specimen of S. canicula, the individual animals are much more difficult to distinguish. The specimens show variation in size and cryptic colors of the spots on the skin (black, white and brownish). Unless adopting invasive techniques such as the fin and subcutaneous tags, most of the animals remain unidentified. Tagging studies have many limitations and practical issues, linked to their short lifetime and detrimental effects to individual fitness and natural behavior. Lethal effects on fragile young individuals are possible. An effective and no invasive identification technique becomes of paramount importance in many behavioral and nutritional experiments in aquarium as in much individual treatments and therefore discrimination of each specimen is crucial. As far as the authors are aware, the ethological investigations are scarce, and the only one on social behavior was the Jacoby and colleagues’ work (2012) using invasive methods.
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Full-text available
Female sperm storage (FSS) has been reported in Chondrichthyans species, and involves the prolonged maintenance of viable sperm after mating events, prior to egg fertilization. Along with multiple paternity (MP–female producing offspring of multiple males within the same litter), FSS has been hypothesized to be related to the increased reproductive fitness of cartilaginous fish lineages. The present study aimed to investigate if: (1) are FSS and MP evolutionarily related and share the same evolutionary history in Chondrichthyes? (2) How is the presence of FSS implied by extinction and speciation rates and thus related to the current species diversity of the group? To answer these questions, we obtained FSS and MP records for Chondrichthyes species from the literature and performed ancestral reconstruction analyses for each character in the phylogenetic tree. We employed MEDUSA and MiSSE to determine if the shifts in diversification rates were related to the characters along the phylogeny. Finally, we utilized HiSSE to calculate the net diversity rates for observed and unobserved states. The ancestral reconstruction indicates that both characters are plesiomorphic for the group; FSS is suggested to be absent in Lamniformes and Rhinopristiformes, whereas MP may be absent in Galeocerdo cuvier. MEDUSA and MiSSE revealed that all clades lacking FSS showed no increase in rates, while there was a higher diversification rates in clades with FSS. HiSSE identified lower net diversity rates in clades lacking FSS associated with hidden states. Therefore, FSS absence seems to contribute to increased extinction rates by reducing diversity among the Chondrichthyes.
Preprint
Full-text available
Sperm storage in females (SS) has been reported in Chondrichthyans species, and involves the prolonged maintenance of viable sperm after mating events, prior to egg fertilization. Along with multiple paternity (MP – female producing Offspring of multiple males within the same litter), SS has been hypothesized to be related to the increased reproductive fitness of cartilaginous fish lineages. The present study aims to investigate if: (1) are SS and MP evolutionarily related and share the same evolutionary history in Chondrichthyes? (2) How the presence of SS is implied in the extinction and speciation rates and thus related to the current species diversity of the group? To answer these questions, we obtained SS and MP records for Chondrichthyes species from the literature and performed ancestral reconstruction analyses for each character in the phylogenetic. We employed MEDUSA and MiSSE to detect if shifts in diversification rates were related to characters along the phylogeny. Finally, we utilized HiSSE to calculate the net diversity rates for observed and unobserved states. The ancestral reconstruction indicates that both characters are plesiomorphic for the group, SS is suggested to be absent in Lamniformes and Rhinopristiformes, whereas MP may be absent in Galeocerdo cuvier. MEDUSA and MiSSE detected that all clades lacking SS showed no increase in rates, whileareas higher diversification rates in clades with SS. HiSSE identified lower net diversity rates in clades with lacking SS associated with hidden states. Therefore, SS seem to contribute to increase extinction rates by reducing diversity among the Chondricthyes.
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Book
Full-text available
This volume presents a fully illustrated field guide for the identification of the sharks and rays most relevant to the fisheries of the Mediterranean. An extensive literature review was carried out for the preparation of this document. A total of 49 sharks, 34 batoids and 1 chimaera are fully treated. The presence of 5 sharks and 2 batoid included in this field guide, need, however, to be confirmed. The guide includes sections on technical terms and measurements for sharks and batoids, and fully illustrated keys to those orders and families that occur in the region. Each species account includes: at least one annotated illustration of the species highlighting its relevant identification characters; basic information on nomenclature, synonyms and possible misidentifications; FAO, common names; basic information on size, habitat and biology, importance to fisheries, distribution and conservation status. Colour plates for a large number of the species are included as well as two plates showing the egg cases.
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Over 50 species of chondrichthyan fishes are known from waters around the British Isles, of which 26 have been recorded in The Centre for Environment, Fisheries and Aquaculture Science (CEFAS) trawl surveys. The distribution and relative abundance of dogfishes, skates and rays are described from groundfish surveys in the North Sea, English Channel, Irish Sea and Celtic Sea. The contemporary distribution of species in relation to their biogeography and major changes in the distribution are discussed. Nursery areas of elasmobranchs were typically in shallower water than adult habitats, a pattern evident for blonde (Raja brachyura), thornback (R. clavata), small-eyed (R. microocellata) and spotted ray (R. montagui). In contrast, juvenile cuckoo ray Leucoraja naevus occurred further offshore and were most abundant in the western Irish Sea and northern St George's Channel. Oviparous species require a suitable substratum for the deposition of eggs, and the distribution of egg-cases is illustrated and important egg-laying substrates identified.
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In view of the fact that dogfishes are now of undoubted importance as marketable food fishes, it is necessary that the life-history of each of the species concerned should receive closer attention than hitherto. The present publication is the result of an endeavour to gain a personal working knowledge of the general life-history of the species which are landed at Plymouth. In carrying out a scheme of work of this kind it is certain that many of the observations made will have already been carried out previously by other workers, but, nevertheless, the results obtained are of value, not only in regard to the degree of confirmation which they afford, but also in the building up of an account of the life-history under the local conditions. In some instances, too, it will be seen that the actual numeric results in themselves are of little statistical value, but they yield very interesting suggestions which may be confirmed or disproved by a repetition of the experiments on a larger scale. I express my thanks to the fish-buyers at Plymouth fish-market, particularly Mr. J. Vanstone, for their kindness in allowing me to handle their fish before dispatch, and for their assistance in obtaining a regular supply of material for many months.
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Article
Spermatozoa stored in oviducal glands of sharks sampled off the North American east coast were revealed by viewing stained tissue sections using light microscopy. Of eleven species surveyed, sperm were found in nine:Alopias vulpinus, Lamna nasus, Carcharhinus obscurus, Carcharhinus plumbeus, Galeocerdo cuvieri, Prionace glauca, Rhizoprionodon terraenovae, Sphyrna lewini andSphyrna tiburo. Three insemination patterns are proposed to account for differences noted in these findings: (1) non-storage/immediate insemination for sharks such asLamna nasus; (2) short-term storage/delayed insemination as found in sharks in which ovulation is prolonged over weeks or months such asRhizoprionodon terraenovae, and (3) long-term storage/repeated insemination, a characteristic of nomadic sharks such asPrionace glauca andCarcharhinus obscurus which can store sperm in specialized tubules for months to years.
Article
1.1. Changes in respiration and circulation induced by hypoxia were studied in the dogfish Scyliorhinus stellaris (L.) by reducing the O2 pressure in ambient water from 142 mm Hg to 54 mm Hg. The following changes were observed in hypoxia: (a) O2 uptake decreased markedly. (b) Respiratory rate did not change significantly, but the ventilation increased, showing a maximum at moderate hypoxia. (c) Heart rate decreased, and cardiac output measured according to the Fick principle also showed a slight tendency to decrease. (d) Mean blood pressure in the ventral aorta and in peripheral arteries decreased.2.2. These effects of hypoxia are mostly in agreement with those found in other elasmobranchs but differ in many respects from changes observed in teleosts.