ČELEBIČIĆ ET AL. I S P I N N A N O B I L I S L . C R I T I C A L LY E N D A N G E R E D ?

221

SHORT COMMUNICATION

IS PINNA NOBILIS L. CRITICALLY ENDANGERED

IN NEUM BAY, BOSNIA AND HERZEGOVINA?

Mirza Čelebičić1, Nedžad Gradaščević2*, Vedad Viteškić3

1
University of Sarajevo, Faculty of
Science, MA Biology, Bosnia and ABSTRACT
Herzegovina
2
University of Sarajevo, Veterinary After the mass mortality events of Pinna nobilis L. occurred in
Faculty, Department of Radiobiology
the neighboring Croatia, and conservation status of this species
with Radiation Hygiene, Biophysics &
Environmental Protection, Bosnia and was changed in the IUCN Red List to critically endangered
Herzegovina (CE), a survey was conducted to determine whether this
3
March. MSc. Urban planning, Bosnia
and Herzegovina emerging disease had spread to Bosnia and Herzegovina (B&H).
A site of 1.4 HA, located at the north side of the Neum bay,
*Corresponding author:
was investigated. All populations found had 100% mortality
Dr. sc. Nedžad Gradaščević,
Associate professor rate. Furthermore, there was absence of juveniles and younger
University of Sarajevo, individuas. Irregularities in the age structure and density of
Veterinary Faculty,
Department of Radiobiology with
dead populations found are the signs of certain environmental
Radiation Hygiene, pressures on this species for a long time. The results indicate
Biophysics & Environmental that the situation is serious and requires a systematic approach
Protection,
Zmaja od Bosne 90 of all competent institutions for the conservation of this species.
710 000 Sarajevo
Bosnia and Herzegovina Keywords: Neum bay, conservation, marine ecology, mass
Phone: +387 33 729 159 mortality event, Pinna nobilis
ORCID: 0000-0003-4759-3192
E-mail:
nedzad.gradascevic@vfs.unsa.ba
INTRODUCTION
Original submission:
24 September 2020 Pinna nobilis L. is an endemic bivalve of the Mediterranean, whose
Revised submission: populations biofilter water in the amount of 6 lit/min (Zavodnik
25 October 2020
et al., 1991; Schultz and Huber, 2013) lives at depths of 0.5-60 m
Accepted:
28 October 2020 (Butler et al., 1993), and at depths of 2-30 m in the Adriatic (Hrs-
Brenko, 1991; Hrs-Brenko, 1997; Zavodnik, 1967). Its habitat is
in the meadows of Posidonia oceanica and Cimodotia nodosa, on
gravelly substrate and in mud (Zavodnik et al., 1991; Katsanevakis,
2005). It is the largest shellfish in the Mediterranean and its height
exceeds 1 m (García-March and Vincente, 2006), and it reaches up
to 27 years of age (García-March et al., 2008). This species has a
significant role in maintaining cleanliness and improving visibility in
the sea, serves as a host to a large number of epibiotic organisms,
222 VETERINARIA VO L . 6 9 • I S S U E 3 • 2 0 2 0
its dense populations forming small oases of life
such as reefs. The presence of this species in the
Mediterranean dates back to the Miocene (Gómez-
Alba, 1988) and its beauty, from ancient times to
the present day, attracts people who once used it in
clothing, food, and now tourism.
Pinna nobilis has always been exposed to
anthropogenic pressures: hunting, trampling,
destruction by anchors, habitat degradation, and
pollution. Especially at the end of the last century
this led to decreases in populations which was
the reason it was included in a protection regime
under the Annex II of the Barcelona Convention
(SPA/BD Protocol 1995) and Annex IV of the EU
Habitats Directive (European Council Directive
92/43/EEC). Italy protected it by the Legislative
Decree 190/2010, Art. 11 for the Marine Strategy
Monitoring Program, including Pinna nobilis
among the Mediterranean species worthy of
particular attention. These efforts led to the recovery
of populations throughout the Mediterranean basin.
Efforts to conserve this species in the future must
be based on an understanding of adaptive potential
and genetic variability ot the species. Systematic,
extensive research and analysis of populations in
this genetic context will result in the right decisions
and actions towards recovery and conservation
(Sanna et al., 2013; Sanna et al., 2014).
In 2016, the first mass deaths of the Pinna nobilis
population began occuring, starting in Spain and
then spreading through surface currents through
the Mediterranean basin in Italy, France, Tunisia,
Greece, Cyprus, Albania and Turkey (IUCN 2019;
Öndes et al., 2020). During these four years, the
disease spread and emerged in to the Adriatic Sea
and devastated populations. Populations in some
localities in the Mediterranean, such as the Alfacs
Bay, Mar Menor, and rare specimens that have
shown immunity to this disease give hope, albeit
small, for the survival of this species (Catanese et
al., 2018; Cabanellas-Reboredo et al., 2019; Saric
et al., 2020; Scarpa et al., 2020).
The disease is manifested by a slower closure of
the shell valves and later by a total inability to
close. If the unprotected individuum is not eaten by
the predators such as Gilthead sea bream,  Sparus
aurata and the common octopus, Octopus vulgaris,
then in the last stage of the disease after her mantle
separates from the valves and falls to the bottom of
the shell it will die very quickly (Addis et al., 2009;
Catanese et al., 2018).
The first researches indicated that the protozoan
Haplosporidium pinnae was the main cause of the
disease but the sum of all epidemiological studies
to date indicates that this is a multifactorial disease.
It is now known that the protozoa Haplosporidium
pinnae and Mycobacterium sp. are major pathogens,
followed by Vibrio sp., Rhodococcus erythropolis,
and another protozoan parasite Perkinsus sp. (see
Scarpa et al., 2020 and reference therein).
All this led to the fact that now Pinna nobilis L. is a
critically endangered CE species on the IUCN Red
List (IUCN 2019).
In the Neum Bay, although ubiquitous, this shell
has never been surveyed, except for the fact that
it had been mentioned in the inventory of marine
fauna 39 years ago (Soljan, 1980). Just 2 years ago,
one population was identified and georeferenced
(Celebicic et al., 2018).
During a diving course in October we witnessed a
large number of dead individuals of Pinna nobilis L.
A survey was organized to collect accurate data and
to determine whether it is necessary to alert first the
scientific public and then the relevant institutions
regarding the situation we witnessed. It was a
necessary ecological research aimed at determining
whether the Pinna nobilis mass mortality event
had occurred in the Neum Bay, as it had happened
nearby, in the Ston Bay, Croatia (Saric, 2020).
 ČELEBIČIĆ ET AL. I S P I N N A N O B I L I S L . C R I T I C A L LY E N D A N G E R E D ? 223

MATERIAL AND METHODS
Locality and Research Methods
The surveyed area was 1.3 HA and was located on
the north side of the Neum Bay. At the site, a group
of 17 divers performed SCUBA dives for 4 days.
Given the size of the Pinna nobilis L. individuals,
the absence of seagrass in which they could be
more difficult to spot, and the visibility of about 6
meters, one diver could cover a terrain width of 4
meters (2 meters on each side) (García-March and
Vicente, 2006). The distance covered in the dives
was between 100 and 150 meters. The individuals
found were photographed using GoPro Hero 7
Black, photo mode, Hugyfot housing, warm white
lighting, ISO 400 sensitivity.

Table 1. Projected Coordinate System:  MGI_Balkans_6; Geographic Coordinate System:  GCS_MGI;

Date:   D_MGI; Prime Meridian: Greenwich; Angular Unit: Degree.

1 2 3 4 5 6 7 8 9

X 1959033,964 1958998,681 1958980,566 1958914,202 1958855,202 1958865,049 1958956,600 1958986,620 1959015,849

Y 5301224,846 5301166,292 5301177,287 5301247,364 5301256,006 5301323,718 5301310,307 5301258,509 5301235,840

The health status was determined by examining the
possibility of closure and the rate of closure of the
shell. Healthy individuals close the shell at a rate of
<5 s and sick ones >5 s after the stimulus (pressing
the opening of the shell), or with no closure of shell
if they were dead (Saric et al., 2020).
Population density is calculated by dividing the
number of individuals found by the investigated
area (Siletić and Peharda, 2003). We recorded the
depth and the type of the seabottom substrate in
which they were found.
P. nobilis shell heights were measured by the
methods used by Siletic and Peharda (2003), the
shell height above the sediment (Hs) and width of
the shell at sediment level (a) were determined.
Total shell height (HT) was calculated using the
following equation: HT = (1.79 a + 0.5 ± 0.2) +
Hs. Maximum width of the shell was measured
following the procedure of Garcia March et. al
(2006).

Figure 1 Exploration site

224 VETERINARIA VO L . 6 9 • I S S U E 3 • 2 0 2 0
RESULTS
Nine upright individuals were found and one laid
on the bottom. Out of those ten, all of them were
dead, empty with opened valves. They were found
at depths of 9-15m with average depth of 9.6 meters,
and all were buried in a muddy bottom without the
presence of flowering plants. Dimensions of the
Figure 2 Dead individua of Pinna nobilis L. at the bottom of the Neum Bay
DISCUSSION AND CONCLUSION
Based on the previous results, we assumed that
the mass mortality event involving Pinna nobilis
L has occurred in the Neum Bay as well as in the
nearby Ston Bay (Saric, 2020). As we did not
find any juvenile individuas and the shells were
completely empty, we concluded that the death had
occurred within a period of three years, when the
first population of Pinna nobilis was recorded in
October 2017 at the south side of the Neum bay
(Celebicic et al., 2018). It is most likely, though it
shortest individuum in height was 61.3 ± 0.2 cm
and had 19.8 cm in width. Maximum height of 71.7
± 0.2 cm was recorded in individua that was 16.7
cm in width. The average height of the shell was
64.92 ± 0.2 cm and width 17.37 cm. Population
density was 0.00077 ind/m2 . Morbidity at this
location was 100% (Figure 2 A,B,C,D,E,F).
happened within the last year, after the first recorded
occurence of Pinna nobilis mass mortality in the
Adriatic sea (Cizmek, 2020).
Average height of our specimens had been 64.92
± 0.2 cm, so the assumption of the population age
was around 15 years (Siletic, 2003). The smallest
individual found was unexpectedly 61.3 ± 0.2 cm
high showing irregular age structure of surveyed
populations. Absence of juveniles and younger
individuas is an indicator of ecosystem degradation
and a sign of certain changes that do not benefit
 ČELEBIČIĆ ET AL. I S P I N N A N O B I L I S L . C R I T I C A L LY E N D A N G E R E D ?
the normal structure, development and growth of
Pinna nobilis L. population (Siletic, 2003). For
a long period of time there have been serious
environmental pressures on this species. This
was noticed by Celebicic et. al (2018), pointing at
anthropological pressures through the disposal of
large quantities of construction material (gravel and
sand) on the shores of the Neum Bay. In that study,
juvenile individuals were found buried in sediment
unable to develop, which can be one of the reasons
for absence of juvenile individuas in our survey.
Figure 3 Significantly low population density found in comparision to previous studies
Low population density and irregular age structure
are effects of prolonged environmental pressures on
Pinna nobilis populations in the Neum bay. There
are many unknowns given the lack of research
work and available data related to the Neum Bay
and the species that live in it. But from the data
obtained in two studies that took place in the Neum
Bay, we see that Pinna nobilis L. populations have
not lived in optimal conditions for some time, and
we cannot say the cause with precision. We can
say that adverse conditions certainly had an effect
on the immune system of this species and could
have made them more susceptible to the emerging
225
The values have changed drastically compared
to the previous measurements of the population
density of Pinna nobilis of 0.0125 ind/m2
(Celebicic, 2018), which is now at extremely low
value of 0.00077 ind/m2. It is not appropriate in
the light of the average values measured in the
Mediterranean Sea 0.01 ind/m2 (Combelles et al.,
1986), and it is extremely low in comparison to the
average population density of 0.1 ind/m2 in the
Adriatic Sea (Zavodnik et al., 1991) (Fig. 3).
parasitic disease that brought them to the brink
of extinction. This view and thinking returns the
ball back to us. Maybe our role in this possible
extinction is much bigger than we are aware of.
The situation is alarming and requires systematic
research of the wider area of the Neum Bay and
the part of the Mali Ston Bay that belongs to B&H,
as soon as possible. We hope to find a number of
healthy individuals or at least one which is immune
to actual disease, which would mean a lot for
the maintenance and survival of this endangered
species and the conservation of the biodiversity of
this part of the Adriatic Sea.
226 VETERINARIA VO L . 6 9 • I S S U E 3 • 2 0 2 0
We need to properly understand the ecology of
this shell that hosts a huge number of epibiont
organisms (Plećaš 2017). Pinna nobilis is a
symbiote with decapod crustaceans (IUCN, 2019).
It also has a role in reducing water turbidity and
therefore in the illumination and photosynthesis of
autotrophs. All this shows us how important it is in
the process of oxygenation of ecosystems, so we
can only guess what consequences its extinction
will have for the ecosystem of Adriatic sea and the
entire Mediterranean.
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CONFLICTS OF INTEREST
The authors declare no conflict of interest.
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DA LI JE PERISKA (PINNA NOBILIS L.) KRITIČNO UGROŽENA U

NEUMSKOM ZALJEVU U BOSNI I HERCEGOVINI ?
SAŽETAK
Nakon što su se masovni pomori Pinna nobilis L. dogodili u susjednoj Hrvatskoj, a status zaštite
ove vrste na Crvenoj listi IUCN-a promijenjen u kritično ugroženu (CE), provedeno je istraživanje
kako bi se utvrdilo da li se ova nova bolest proširila u Bosnu i Hercegovini (BiH). Istraženo je
područje od 1,4 HA smješteno na sjevernoj strani Neumskog zaljeva. Sve pronađene populacije
imale su stopu smrtnosti od 100%. Nije bilo juvenilnih jedinki niti mlađih adulta. Odstupanja
od standardnih vrijednosti za starosnu strukturu i gustinu kod mrtvih populacija su jasan znak
djelovanja određenih nepovoljnih ekoloških faktora na ovu vrstu već duži period. Rezultati
ukazuju na to da je situacija ozbiljna i zahtijeva sistematski pristup svih nadležnih institucija u
cilju očuvanje ove vrste.

Ključne riječi: Neumski zaljev, konzervacija, marinska ekologija, masovni pomor, Pinna nobilis