The crab Polybius henslowii (Decapoda: Brachyura) as a main resource in the longgerhead turtle (caretta caretta) dier fron North Afric

              Rev. Acad. Canar. Cienc, XVII (Num. 4), 103-116 (2005) (publicado en agosto de 2006)
THE CRAB Polybius henslowii_(m.CA?OT)X: BRACHYURA)
AS A MAIN RESOURCE IN THE LOGGERHEAD TURTLE
{Caretta caretta) DIET FROM NORTH AFRICA
O. Ocana*, A. G. de los Rios y Loshuertos** & A. Brito***
=Instituto de Estudios Ceuties (CECEL-CSIC), Paseo del Revellin, 30. 51001 Ceuta (North-Africa), Spain;
lebruni@telefonica.net; iecuties@retemail.es
**Departamento de Biologia Marina, Fundacion Museo del Mar, Autoridad Portuaria de Ceuta,
Muelle Canonero Dato S/N.51001 Ceuta (NorthAfrica) Spain, caretta@eresmas.net
***Departamento de Biologia Animal, Facultad de Biologia, Universidad de La Laguna,
C/ Astrofisico Francisco Sanchez s. n., 38206 La Laguna , Tenerife, islas Canarias. abrito@ull.es
ABSTRACT
Marine turtles are known for feeding on a great variety of preys. . . from the soft jel-lyfishes
to the hard shells. However, this does not mean that every turtle in fact eat this wide
variety of preys throughout its life, but depending on the habitat and age they show certain
preferences, making this selection based on the abundance (quantity), the nutritive proper-ties
of the prey (quality) and how easy is to get (accessibility). In this paper we present the
almost exclusive diet of the Loggerhead turtle Caretta caretta (Linnaeus, 1758) thanks to 5
years of intensive research on either dead and alive specimens at the North African coasts
of Ceuta (Spain), Morocco and Western Sahara. We find out the real importance of the crab
Polybius henslowii (Leach, 1 820) in Caretta caretta diet, discussing some aspects of this
marine turtle as a specific rather than a generalist feeder.
Key words: Caretta caretta, feeding ecology, Polybius henslowii. North Africa.
RESUMEN
Es conocido que las tortugas marinas se alimentan de una gran variedad de presas. . .,
desde las blandas medusas hasta las duras conchas. Sin embargo, esto no significa que cada
tortuga tenga en su dieta esta gran variedad de alimento a lo largo de su vida, sino que,
dependiendo del habitat y de la edad, muestran ciertas preferencias, realizando esta eleccion
en funcion de la abundancia de la presa, de sus propiedades nutritivas y de la facilidad para
conseguirla. En este articulo presentamos la dieta de la tortuga boba Caretta caretta
(Linnaeus, 1758) con datos de 5 aiios de investigacion intensiva con ejemplares vivos y
muertos de la costa norte africana de Ceuta, Marruecos y Sahara Occidental. Descubrimos
la importancia del cangrejo Polybius henslowii (Leach, 1820) en la dieta de Caretta caret-ta,
aportando pruebas para creer que esta especie es, en cuanto a su alimentacion se refiere,
mas especifica que generalista.
Palabras clave.- Caretta caretta, ecologia alimentaria, Polybius henslowii, Norte de
Africa.
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1. INTRODUCTION
It is well known that the loggerhead turtle, —although primarily carnivorous—, may
feed on many different preys (see DODD, 1988 [9]; VAN NIEROP & DEN HARTOG, 1984
[30]). We offer new data on the feeding ecology of the Loggerhead turtle in neritic habitat
of shallow waters and sheltered bays in the African shore of the Strait of Gibraltar.
In 1817, the Reverend John Steven Henslow, Professor of Botany in Cambridge and
Charles Darwin's teacher (he persuaded his disciple to join the "Beagle" expedition) found
the crab Polybius henslowii (fig. 1) in a herring net in north Devon and sent the specimen
to Leach, who described it. Nowadays, there are still some aspects of this crab biology, as
the concentrations (blooms) and the reproduction pathways, that still remain unknown
(GONZALEZ-GURRIARAN et al, 1993 [16]), although those authors have remarked the
importance of this species as a seasonal resource in Galicia, on the Northwest corner of the
Iberian peninsula.
According to the literature, the species has been recorded from the North Sea to the
Canary Islands, including Western Mediterranean (ZARIQUIEY ALVAREZ, 1968 [31];
MANNING & HOLTHUIS, 1981 [20]). Furthermore, R henslowii is able to constitute large
pelagic concentrations in order to reproduce themselves (GONZALEZ-GURRIARAN,
1987 [14]; GONZALEZ-GURRIARAn etal, 1991 [15]; GONZAlEZ PEREZ, 1995 [17]).
GONZALEZ PEREZ (1995) [17] has recorded those crabs forming concentrations of thou-sands
of specimens in February, off Lanzarote coast (Canary Islands), and Dr. Peter Wirtz
(pers. com.) has recorded this crab sporadically from Azores and never forming concentra-tions.
We have observed many crabs remains in the food of some sea birds in the islets locat-ed
at the North of Lanzarote (winter 1997) (A. Brito, pers. obs.).
2. MATERIAL AND METHODS
Ceuta is located in North Africa, in the South shore of the Strait of Gibraltar (fig. 2),
with double influence, Mediterranean and Atlantic, and complex winds and sea current pat-terns.
There are noticeable records of sea turtle exploitation by ancient civilizations that
were established at this strategic land (CASASOLA & PEREZ, 1999 [6]; GARCIA DE LOS
RIOS et aL, 2003 [13]).
Although our research is being performed along the Ceuta region (Cape Negro to
Beliones Bay, about 100km. long)—fig. 2—we also have stored some data from other areas
along the Moroccan Atlantic littoral, where the crab is also present (De los Rios et aL, in
prep.). In addition, we offer news about other P. henslowii predators through almost 3000
km. of coast, remarking the importance of this crab as an important resource in the region-al
context of North Africa.
The present study is based on the investigation of more than 150 Loggerhead turtles
stranded at Ceuta region performed during the years 1998-2004 with the examination of the
gut content from the year 2000 on. Sporadically, we had the chance to perform necropsy on
turtles also coming from the Atlantic and the Mediterranean coast of Morocco.
Measurements and necropsy techniques were made following the Septem Nostra
(Association for the Study, Protection and Diffusion of the Natural and Historic Heritage)
protocols (see OCANA & DE LOS RIOS, 2002 [25]). The main biometry data were: SCL
(Straight carapace length) TL (Total length) SCW (Straight carapace with)
104
At sea, the turtles were hand captured and sporadically intubated to pump their stom-achs
out, in order to obtain food samples. For those ill animals under rehabilitation in the
tanks, we just have to wait for excrement to check out what they ate the previous days.
During the ruled necropsies, to find out the cause of death, the turtle are opened, cut-ting
through the carapace-plastron cartilaginous bridges, axilar and pelvic skin, and remov-ing
the plastron from the appendicular attachments and then the whole celomic cavity is
exposed. Later, the intestinal tract is opened and the content stored for further analysis. Once
the content is removed, we obtain the dry weight and examine the sample under the binoc-ular
dissecting microscope; the final result is stored afterwards in alcohol 70%.
Some commercial fish from the boats operating along Morocco (Mainly at El
Rincon, Larache, Tanger, Asilah and Agadir), was checked on a daily basis at the Spanish
border in the search for the crab presence (to help us to increase the knowledge about the
biology of this unknown specie) and the analysis of the stomach of other potential predators
of the crab (De los Rios et al., in prep.). Besides, sporadic direct observations of fishermen
working at the Harbour of El Rincon were made.
In order to detect the presence of the crabs in our sea shores as well as stranded
specimens of C. caretta, we were supported by a stranding network that search along our
littoral. Nowadays, such net involves a professional multidisciplinary team and more than
60 volunteers. Thanks to a project focussed on Ceuta marine tetrapods (DE STEPHANIS
et al., 2001 [8]) we had the opportunity of searching our littoral widely throughout during
the four seasons of the year, from boats looking for sea turtles and its main prey, by mak-ing
transects covering the whole studied area (see DE STEPHANIS et al, 2001 [8] for
methodology).
3. RESULTS
According to fig. 3, in our littoral (From Ceuta to Cape Negro), immature, juvenile,
sub adults and adults turtles are, from individuals recently recruited to neritic habitats meas-uring
34 cm. SCL to adults measuring 100 cm. SCL, but as we can see in the graphic, the
sub adult population is predominant present (Size range. n= 167; Mean: 67,2574; SD:
11,1550; Median: 68; Mode: 70; Minimum: 34; Maximum: 100. Measures: SCL).
At the same time, the crabs have been observed forming big concentrations (blooms)
from May to August stranded at the beaches (fig. 5), for reasons that we still ignore, but that
may have to do with the reproduction cycle (GONZALEZ-GURRIARAn, 1987 [14];
GONZALEZ-GURRIARAn et al, 1991 [15]). In addition to this, during the observations
on board, the turtles have been seen regularly eating these crabs.
Investigations about the biology of the crab reveal similar concentrations which take
place around March and April at the Atlantic Coast of Morocco, from the South Sahara
(Laayoune) to the north (Asilah —fig. 2—) and the Mediterranean as well. Sometimes in
the South coast of Morocco, there are so many crabs that they become a problem for the
fishermen nets (personal observations).
As a consequence of the veterinary inspection that take place in the Spanish bor-der
(see material and methods), specimens of P.henslowii were noticed all year round in
the fish boxes, mainly of Pagrus spp., where we found the highest biomass of crabs, giv-ing
an idea on the type of habitat and seasonal presence of this marine invertebrate at these
latitudes.
105
As we can see in fig. 4 (which represents monthly the mean of the years 2000-2004),
turtles are present all year long. After checking the gut contents of our turtle specimens, we
notice the presence of P.henslowii during all seasons, being in Spring and in Summer (with
a peak in July) when the biggest number of turtles stranded which, at the same time, showed
the crab inside their stomachs as a main gut contents (90% or 1 00% of the content is
P.henslowii).
We have reviewed the feeding ecology papers on similar behaviours of Loggerhead
turtle and other marine turtles in different world areas. According to our review and the one
made by Mortimer (see Table one), C. caretta is able to feed on single but abundant and easy
catching preys. Indeed, the preys are changing from one region to others, but in all the
regions analyzed the behaviours of feeding on certain preys confirm our hypothesis that C.
caretta populations exploit specific marine resources all over the world. This assertion is
consistent with our current data and also with the data presented in this paper (Table 1).
Also, for other species of sea turtles, we review similar feeding patterns (Table 2).
In our geographical area, we have also observed crabs in the drop pills of the sea Gull
(Larus argentatus} and inside the stomach of several fishes as Pagrus spp.. Tuna {Thunnus
thynnus), Dicentrarchus spp., Dentex dentex, Sparus aurata, Pagellus bogavareo (De los
Rios et al., in prep.) and Alepisaurus ferox (see GONZAlEZ PEREZ, 1995).
The main cause of death of these turtles (almost 100%)) is the interaction with fish-eries,
specially nets, been the most common, drifting nets and Almadrabas (an ancient art
whose main prey is the tuna fish, consisting of a labyrinth of nets through where the fish is
orientated until it gets to a final pool where it is kept alive until is lifted).
4. DISCUSSION
4.1. The regional resource importance
The most important crab-watching in our region, coincident with the abundance of
marine turtles, is during spring and summer, when we find the stomachs of C. caretta ftill
with crabs (99-100%) of the whole content). But the occurrence of crabs in the gut content
of some specimens of C. caretta stranded on January proves its presence as a food resource
all year long, further away than a seasonal happening.
The fact that these stranded turtles may have been drifted away from some other area,
enforce the idea of a true regional phenomenon. Nevertheless, many corpses are directly
rescued from the nets, so it can be certainly affirmed that those turtles belonged to the area.
It is obvious that the process of up-welling serves as a powerful enrichment of the
sea water surface, and a well known consequence of this phenomenon is the high marine
plankton production. According to GONZAlEZ-GURJUARAN (1987 [14]), the presence
of concentrations of this crab may be considered related to enrich areas affected by up-welling.
Along the Atlantic coast of Morocco there are a very strong up-welling influences
(ORBI et al., 1998 [26]); our region is strongly influenced from the general up-welling
process of Alboran Sea (see ESTRADA et aL, in MARGALEF, 1989 [10]) but also, in
Ceuta, there is a local up-welling having its epicentre at Punta Almina. (BALLESTER &
ZAVATTI, 1983 [1]). The occurrence ofjellyfishes blooms in this area (OCANA& DE LOS
RIOS, 2003 [24]) may be also linked with the high production that takes place in the area,
and this fact is consistent with the seasonal presence ofDermochelys coriacea in our littoral
(OCANA & DE LOS RIOS , 2003 [24] ; De los Rios & Ocana, in prep.). This kind of occur-
106
rence is not isolated, but have been described someplace else, like in West Florida Shelf,
Gulf of Mexico, where large Loggerhead turtles were found associated with two submarine
geothermal springs (BJORNDAL, 1997 [3]).
Furthermore, in the Strait of Gibraltar the fishermen use them as bait, keeping high
quantities of crabs on shallow waters in sheltered bays (personal observations). In the coast
of Portugal, during summer, this crab is even commercialized in some local markets
(COSTA et aL, 2003 [7]). Other industrial uses are found North-west Spain, in Galicia,
where many years ago they were used as fertilizer (see GONZALEZ-GURRIARAN, 1987
[14]). Nowadays, there is a project to obtain industrial application in aquaculture out of this
crab (IGLESIAS et aL, 2000 [19]).
Although very little is known about the occurrence and abundance of this crab along
the Atlantic Moroccan coast, we confirm it forms large pelagic concentrations from Larache
to Laayoune in spring and summer, been even a big problem for the shore fishermen.
In the region of Alhoceima (an important harbour fishery in the Mediterranean coast
of Morocco, 150 km. from the Spanish town of Melilla), the crab has been also recorded in
high quantities (Dr. Tudela, personal communication —De los Rios et aL, in prep.—).
What happens during the year along the coast of Morocco is something that remains
unknown. However, the remarkable occurrence of the crab in the stomachs of a number of
other marine vertebrate reveals the importance of P. henslowii in the context of the whole
marine ecosystem in this part of the world (De los Rios et aL, in prep.).
All these data support the idea of the importance of protecting such a key resource
from any kind of decreasing factor which may act against the equilibrium of the marine
ecosystem.
4.2. About the relation between the crab and the turtle
The discovery of this crab as a main gut content of C caretta in this part of the world
is a remarkable fact that has remained unknown until now. Although there are certain num-ber
of papers on the diet of C. caretta (see DODD, 1988 [9]), the presence of this crab in
the loggerhead turtle has never been reported. However, attending to the crab distribution
and concentrations, which is a well known phenomenon from North Sea to Canary Islands
(see GONZALEZ PEREZ, 1995 [17]) including Alboran sea, the lack of data of the relation
among this crab and this turtle could be due to the absence of post-mortem studies, further-more
the crabs could have been overlooked, remaining in the gut content or revealed on
papers as unidentified crabs!. The prevalence of P. henslowii in the gut content of our C.
caretta populations sets up its importance as a main resource for this species along several
months, so during these periods turtles can stock fat reserves. We realize the close relation
between both, the turtle and the crab, along the year. However, we also noticed other preys
(especially gelatinous plankton) (Table 1) during those months when the percentage of crabs
in the stomachs of the remaining turtles is low. Apparently, this seasonal adaptation occurs
anytime the main prey is not sufficiently present for whatever reason in the area. According
to this, in South Texas waters, and during the spring, the sea pen (Virgularia presbytes) is
the food of election for the Loggerhead turtles, while the crabs are eaten during summer and
fall when they increase in number (BJORNDAL, 1997 [3]).
C. caretta and P. henslowii perform a clear case of trophyc relationship between prey
and predator being the abundance, the nutritive value and easy accessibility of this resource
by C. caretta the keys to understand the phenomenon.
107
4.3. Generalist versus specialist
The Loggerhead turtle belong to a reduced group of marine turtles that inhabit the
seas from many millions of years ago (PRITCHARD, 1997 [28]; BOWEN, 2003 [5];
GULKO & ECKERT, 2003 [18]). So it is a plausibly option that loggerhead turtles knows
how to get food by searching for some resources able to support their vital requirements.
The data offered in the Table 1 shows there are abundant regional resources which
Caretta caretta is able to feed on along the different littorals of the world.
Ours is not the first finding of a prevalent food resource in Loggerhead turtle (Table
1), not even in the other marine turtles, especially Dermochelys coriacea (Table 2). This
aspect combined with some behaviour like the "in faunal mining" (see BJORNDAL, 1997
[3]; FRICK et al., 2001 [11]), indicates an active search with a previous idea of what is
wanted or what the turtle "feels like eating".
In our region, loggerhead turtles are eating one resource remarkably: After all, the
crab is a nutritive food (GONZALEZ-GURRIARAN, 1987 [14]) being easily caught by this
turtle at a low energetic cost due to its abundance, and the fact that P. henslowii spends most
of its time in the water column flouting with the currents.
In a general context, we have searched for bibliographic information and offer some
data of specialist feeding behaviour in other world coasts. There are not convincing evi-dences
that Caretta caretta is a feeding specialist all over the world but indeed there are
enough scientific evidences to think about avoiding the topic about the passive incidental
finding or the generalist loggerhead capability to feed on almost any marine creature that,
on the other hand, no author talks about clearly. Unfortunately, there are not papers about
feeding ecology or ecology of sea turtles in a wide sense (whatever pelagic or littoral habi-tats)
that allow us understand this phenomenon properly. Most of them are a simple list of
items found in the stomach, without a further analysis of the turtle and its environment in an
ecological context.
The specialization feeding pattern, presented in the current paper proves that a new
concept of integrated biological studies on sea turtles is necessary in order to increase our
knowledge about the ecological relation between sea turtles and the marine ecosystem.
So far, to conclude a loggerhead feeding ecology model, we need to search for new
information in order to make possible understanding the regional feeding ecology of log-gerhead
turtles around the world.
Loggerhead turtles can be also opportunistic (TOMAS et al, 2003 [29]), although
this is a very recent artificial phenomenon located in areas with fishery activities.
5. CONCLUSIONS
1) P. henslowii is the main resource for C caretta in the Ceuta region (Ceuta-Cabo Negro-see
map). According to the system of currents, some corps may come from Atlantic North
Africa, Alboran Sea or Southern Europe. Moreover, the fact that we recorded concentra-tions
of P. henslowii along the Atlantic and the Mediterranean coast of Morocco, from
Sahara coast to Al Hoceima (see map), remarks that is a regional phenomenon.
2) The Loggerhead turtle feeds on this crab along the year, although May and September are
when the turtles present the highest quantity of crabs in its gut content.
3) Our research sets up that C. caretta presents a very specific diet in North Africa, oppo-site
to the generalist perspective on this species.
108
4) The species P. henslowii is a resource not only for C. caretta but for a number of marine
species including birds and also pelagic and benthopelagic fishes.
5) Due to the close relation between predator and prey they should be protected at the same
extent at their habitats to prevent a disaster of lost of biodiversity.
6) Integral studies (with multidisciplinary teams) in order to understand the ecological rela-tions
between the marine turtles and the ecosystem as a whole are needed. Studies of
regional ecology are important for this purpose.
6. ACKNOWLEDGEMENTS
This paper is dedicated to the memory of the sadly disappeared J.C. Den Hartog, who
wrote some valuable papers about some aspects of the biology of marine turtles and also
provided us with valuable literature and data for the better comprehension of the feeding
ecology of the marine turtles. Part of this research program was financially supported by the
Ceuta Autonomic Government (Consejeria de Cultura y Patrimonio and PROCESA).
Part of the Moroccan data has been possible thanks to the friendly collaboration of
the Moroccan researches in the INRH (Amina Moumni) and Casablanca University (Hocein
Bazairi).
Thanks to Professor Wirtz, from Madeira University, for his comments about P.
henslowii
Thanks to our stranding network: Guardia Civil, Urbaser, Septem Nostra Volunteers
and fellows, Diving clubs, Ecoceuta S.L. etc.
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[28] PRITCHARD RC.H. 1997. Evolution, Phylogeny, and Current status. Pp 1-28. in: R
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[29] TOMAS J., F.J.AZNAR & J.A. RAGA. The influence of human activities upon feed-ing
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the First Mediterranean conference on marine turtles. Barcelona Covention-Bem
Convention-Bonn Convention (CMS). Nycosia, Cyprus. 270 pp.
[30] VAN NIEROP M. & J.C. DEN HARTOG 1984. A study on the gut contents of five
juvenile loggerhead turtles, Caretta caretta (Linnaeus) (Reptilia, Cheloniidae), from
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Zoologische Mededelingen, 59 (4): 35-54.
[31] ZARIQUIEY ALVAREZ, R.A. 1968. Crustdceos Decdpodos Ibericos. Inv. Pesq., 32:
xv+510 pp.
Ill
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Figure 1. The potunid crab Polybius henslowii.
ashahi
LAAACl
TANGER
B£EDrrERnAMEAN
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GIElLAITAm
STRAIT PTAAIMDJA
C£IITA<SPAIN^
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Figure 2. Map.
114
20-40 41-50 51-60 61-70
Size (cm.)
71-80 81-100
Figure 3. Turtle sizes.
45
40
35
30
25
20
15
10H
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fL
1 .Lj:k£k]Lll.[MEB
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
I N° STRANDINGS N** WITH CRABS
Figure 4. Monthly compared graph among turtles atranded and turtles with crabs (2000-2004).
115
Figure 5. Polybius henslowii bloom.
116