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ICES CM 2008/F:20 TROPHO-PARASITIC RELATIONS OF ARROW SQUID TODARODES SAGITTATUS IN THE WATERS OF THE NORTHWEASTERN AFRICAN ECOSYSTEM AND THEIR CONDITIONALITY BY SQUID SIZE Ch.M. Nigmatullin 1 , O.A. Shukhgalter 1 , V.V. Laptikhovsky 2 , S.M. Kasatkina 1 1 Atlantic Research Institute of Marine Fisheries and Oceanography (AtlantNIRO), Donskoy Str. 5, Kaliningrad 236000 Russia [tel. +4012-225385, fax +4012-219997, e- mail: [email protected]] 2 Falkland Islands Fisheries Department, P.O. Box 598, Stanley, FIQQ 1ZZ Falkland Islands [tel.: 500-27-260, fax: 500-27-265, e-mail: [email protected] ABSTRACT An isolated population of arrow squid inhabits the shelf and slope waters of North African coast from 11° to 26°N. There were studied stomach contents of 491 squid of ML 5-30 cm and parasitic helminth of 180 squid of ML 8-25 cm. Food spectrum includes more than 50 food groups of amphipods, mysids, euphausiids, shrimps, munids, squids and small teleosts. Myctophids, shrimps, squids and euphausiids were the main food. The predators of this squid in the North African coast are common abundant demersal and pelagic squids, skates, sharks, teleosts and mammals. 8 species and larval form of helminths were found. Trematoda: Didymozoidae mtc II (prevalence 40.9%, intensity 1-10), Hirudinella ventricosa (0.5%, 1); Cestoda: Scolex pleuronectis unilocularis (22.3%, 1-2), S. pleuronectis bilocularis (3.2%, 1), Phyllobothrium sp. (1.1%, 1); Nematoda: Porrocaecum sp. (0.5%, 1), Spinitectus sp.l. (4.2%, 1-2). All revealed helminths are in the larval stage, have broad specificity, theirs life cycles are realized by trophic chains and squids infected from their preys. By food and parasite data there are well-marked multistage squid life cycle that is conditional on predator-prey size relations. Arrow squid plays the important role in pelagic and demersal ecosystems as consumers of II-IV orders, and it’s the important transport host for helminths between invertebrates and small teleosts (intermediate and transport hosts) on the one hand, and sharks, large teleosts and mammals (definitive hosts) on the other hand. Keywords: Arrow squid, Todarodes sagittatus, Northwestern African coast, feeding and parasite relations INTRODUCTION

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Page 1: TROPHO-PARASITIC RELATIONS OF ARROW SQUID Doccuments/CM-2008/F/F2008.pdf · Donskoy Str. 5, Kaliningrad 236000 Russia [tel. +4012-225385, fax +4012-219997, e- mail: squid@atlant.baltnet.ru]

ICES CM 2008/F:20

TROPHO-PARASITIC RELATIONS OF ARROW SQUID

TODARODES SAGITTATUS IN THE WATERS OF THE

NORTHWEASTERN AFRICAN ECOSYSTEM AND THEIR

CONDITIONALITY BY SQUID SIZE

Ch.M. Nigmatullin1, O.A. Shukhgalter1, V.V. Laptikhovsky2 , S.M. Kasatkina1

1Atlantic Research Institute of Marine Fisheries and Oceanography (AtlantNIRO), Donskoy Str. 5, Kaliningrad 236000 Russia [tel. +4012-225385, fax +4012-219997, e-mail: [email protected]] 2 Falkland Islands Fisheries Department, P.O. Box 598, Stanley, FIQQ 1ZZ Falkland Islands [tel.: 500-27-260, fax: 500-27-265, e-mail: [email protected]

ABSTRACT

An isolated population of arrow squid inhabits the shelf and slope waters of North African coast from 11° to 26°N. There were studied stomach contents of 491 squid of ML 5-30 cm and parasitic helminth of 180 squid of ML 8-25 cm. Food spectrum includes more than 50 food groups of amphipods, mysids, euphausiids, shrimps, munids, squids and small teleosts. Myctophids, shrimps, squids and euphausiids were the main food. The predators of this squid in the North African coast are common abundant demersal and pelagic squids, skates, sharks, teleosts and mammals. 8 species and larval form of helminths were found. Trematoda: Didymozoidae mtc II (prevalence 40.9%, intensity 1-10), Hirudinella ventricosa (0.5%, 1); Cestoda: Scolex pleuronectis unilocularis (22.3%, 1-2), S. pleuronectis bilocularis (3.2%, 1), Phyllobothrium sp. (1.1%, 1); Nematoda: Porrocaecum sp. (0.5%, 1), Spinitectus sp.l. (4.2%, 1-2). All revealed helminths are in the larval stage, have broad specificity, theirs life cycles are realized by trophic chains and squids infected from their preys. By food and parasite data there are well-marked multistage squid life cycle that is conditional on predator-prey size relations. Arrow squid plays the important role in pelagic and demersal ecosystems as consumers of II-IV orders, and it’s the important transport host for helminths between invertebrates and small teleosts (intermediate and transport hosts) on the one hand, and sharks, large teleosts and mammals (definitive hosts) on the other hand. Keywords: Arrow squid, Todarodes sagittatus, Northwestern African coast, feeding and parasite relations

INTRODUCTION

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The arrow squid Todarodes sagittatus (Lamarck, 1798) (family Ommastrephidae)

is abundant and wide distributed in the Northeastern Atlantic and the Mediterranean Sea

(Nesis, 1987). This species is polymorphic and probably it is the complex of 2-3

subspecies or separate species (Nigmatullin et al., 1998, 2002). Amongst theirs there is the

northwestern African form that differs with complex of important morphological and

especially ecological traits. This isolated population of arrow squid inhabits the shelf and

slope waters of North African coast from 11° to 26°N with shelf-slope lifestyle. There

were described this population life cycle, growth, distribution and abundance variability

(Nigmatullin et al., 1998, 2002; Arkhipkin et al., 1999), but data on its food composition

are very deficient and based on small studied samples (Nigmatullin, 1972; Hernandes-

Garsia, 1992, 1995; Piatkovski et al., 1998) and data on its predators is absent. Moreover,

in literature is not detail description of helminth fauna and data on infestation rates for

Todarodes sagittatus of NW African coast. There is only very scarce information on

finding (0.4%) of cestodes larvae Phyllobotrium sp. in adult squids in that area

(Gaevskaya, Nigmatullin, 1978).

The aim of this communication is to describe in first approximation of Todarodes

sagittatus food and parasite relations and its place in the waters of the northwestern

African ecosystem (Cap Blanc upwelling zone) and their conditionality by squid size.

MATERIAL AND METHODS

The studied squids were collected during 14 expeditions of AtlantNIRO in 1969-

2000 at the shelf and continental slope of Northwest Africa between 16-24° N at a depth

from 110 to 600 m and in the pelagic water column between 0 and 500 m (the depth of

places – from 200 to 1500 m). Most of squids (481 specimens) were collected from

catches of bottom and pelagic trawls, and 10 young squids – at light station near surface.

Altogether stomach contents were studied in 491 squids of mantle length (ML) 5-

31 cm including 210 squids with full stomachs (fullness degree 3-5). Prey were identified

from tests of eye form, mandibules, tip of rostrums, chitinous integuments of crustaceans;

radular hooks of heteropods; beaks, hooks, suckers and horny rings of cephalopods;

otoliths, scales and bones of teleost fishes (Zuev et al., 1985). To estimate the role of each

food component, frequency of occurrence (percentage of stomachs containing given food,

N%, used all stomachs with food) and proportion in stomach contents (percentage of

virtual volume of stomach, V%, used only full stomachs) were calculated (Zuev et al.,

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1985). In addition there was distinguished special food group – transit food (Nigmatullin,

Toporova, 1982; Nigmatullin, 2005) that introduced into studied squid stomach from the

stomachs of prey, mainly plankton-eating fishes. There was also distinguished other

artifact – “trawl food items”: they were fresh, not or slightly digested remains. This type of

food is presented mainly by pieces of fresh meat with skin coverings of fish or squid trawl

food (Nigmatullin, 2005).

For identification predator of Todarodes sagittatus the stomach contents were

studied of 560 fishes belonging to 38 species that were caught in same area in 1970-1988.

The samples for helminth examination were collected from squids that were fished

at the northwestern African coast between 21° and 23° N in June 1995. 181 specimens of

squids (105 females of ML 12.0-24.4 cm, 43 males of ML 12.4-20.6 cm and 33 juveniles

of ML 9.4-12 cm) were studied with complete helminth analysis. All worms were

collected from frozen squid. Trematodes and cestodes were fixed in 10% formalin and

stored in 70% alcohol. These worms were stained in alum carmine and mounted in Canada

balsam. Nematodes were preserved in formalin and cleared in a mixture of glycerol and

milk acid. The ecological terms – prevalence (P), intensity (I), mean intensity (MI) and

abundance (A) – were used in accordance with the recommendations of Margolis et al.

(1982).

RESULTS AND DISCUSSION

Food composition. Food spectrum is very wide and includes 54 food groups of

chaetognats, different groups of salps, crustacean (mysids, euphausiids, amphipods,

isopods, shrimps, munids, stomatopods, larvae of decapods), heteropods, sepiolids and

sepiids, different kinds of squids and teleosts (Table 1).

Most of Todarodes sagittatus remains in stomachs of studied squids were typical

“trawl food”. Transit food items includes small planktonic animals: copepods

(Nannocalanus minor, Eucalanus crassuss, Calanoides carinatus etc., length 0.6-1.6 mm),

ostracods (0.7-0.9 mm), amphipods-hypereids (3-11 mm), isopods (2.3-12 mm),

euphausiids (3.5-9.6 mm), crab megalops (1-1.8 mm) and larvae of bivalves and

gastropods mollusks (0.8-1.2 mm). The numbers of transit food organisms were within the

limits of 1-30. Their sizes were significantly smaller than the proper food organisms. Most

of transit food organisms were from myctophid and another fish stomachs, and more

infrequently – from squid stomachs.

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Main proper foods were myctophids, squids, shrimps and euphausiids. The

composition of main and secondary food groups in the diet of same-sized males and

females was similar (Table 2).

Most evident changes in the food composition were revealed during life cycle with

increasing squid ML. In this connection there is a need to stress that studied Todarodes

sagittatus population has one year life cycle with habitat ontogenetic shifts and spawns

with a clear winter peak (Nigmatullin et al., 1998, 2002). Thus, ontogenetic and seasonal

variabilities of Todarodes sagittatus food relations are coocurrence. Therefore here is

described the ontogenetic food composition variations on the seasonal background (Table

2).

Young squids of ML 5-15 cm inhabit the pelagic waters in the slope zone where

they fed on euphausiids and young myctophids as a main food in March. Small squids had

secondary importance (Table 2). In May immature squids of ML 10-19 cm migrate to

upper slope zone and edge of shelf, and in day time these squids have “contact” with near

bottom layers and theirs inhabitants. In this period main food items were shrimps (mainly

demersal Plesionica heterocarpus) and myctophids (mainly Myctophum punctatum), and

secondary food – euphausiids and different squids including inshore Sepietta, Alloteuthis

and slope-oceanic oegopsids. In June-July subadult squids of ML 15-25 cm shifted to shelf

where they formed the feeding aggregations. Main food was myctophids, and secondary -

euphausiids and squids. Occasionally squids fed predominantly on euphausiids that

formed very dense concentrations. In prespawning period (November-December) adult

squids of ML 23-31 cm migrated back to slope. Here they fed on pelagic and near bottom

layers where they fed mainly on myctophids and different kind of pelagic and demersal

fishes. Secondary food include shrimps (mainly Plesionica heterocarpus), cephalopods

(both pelagic enoploteuthid squids and demersal sepiids). Euphausiids were absent in food

of these squids.

Predators. The data on known predators of this squid in the North African coast

are scanty. They are common demersal and pelagic squids, skates, sharks, teleosts (our

data) and shortfin pilot whale Globicephala macrorhynchus (Hernandes-Garsia, Martin,

1994). For most of these predators Todarodes sagittatus is accidental food. They are

squids Todaropsis eblanae and Ommastrephes bartramii, skate Raja montagui, sharks

Scyliorhinus canicula, Prionace glauca, teleosts Trachurus trachurus, Scomber colias,

Katsuwonus pelamis, Thunnus albacares, Lepidopus caudatus, Zeus faber and

Haplosteuthus mediterraneus. With the exception of Prionace glauca all these predators

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fed mainly fry and young squids. Two species of Merlucius (M. merlucius and M.

senegalensis) fed on this squid of ML 10-22 cm more often. Adult squid in autumn-winter

seasons at the slope zone between 16-22° N was the main or secondary food for swordfish

Xiphias gladius.

Helminths. Eight different species and larvae forms of cestodes, trematodes and

nematodes were found (Table 3, Fig. 1-4). Metacercaria of didymozoids and larvae of

cestodes are dominated in a quantitative sense. Larvae of nematodes Spinitectus sp. occur

in arrow squid very seldom as well as in other squid species (Gaevskaya, 1977). The total

infestation was 66.1%. The level of infestation with different parasite species was the

same for females and males (Table 4).

Ontogenetic variations were studied by examining data for four size groups of squid

(Table 5). The level of total infestation was high. Indices of infestation with Spinitectus sp.

were low for squids of all studied groups. But there were revealed the differences in

prevalence value for metacercaria of didymozoids and larvae of Scolex pleuronectis (Fig.

5). Didymozoid metacercaria were dominant in helminth fauna of the smallest squid (9-12

cm of ML). These metacercaria are recorded in pelagic gastropod mollusks,

siphonophores, copepods and euphausiids (review: Hochberg, 1990). There was also found

out a decrease in infection by metacercaria and increase in infection by larvae of Scolex

pleuronectis in the next three squid size groups. These ontogenetic changes were due to the

limited life time of metacercaria commonly around 4-6 months (Gaevskaya, Nigmalullin,

1981; Naidenova et al., 1985) and were connected with feeding of this young Todarodes

sagittatus on the small fishes.

CONCLUDING REMARKS

The food organisms of studied Todarodes sagittatus are the representatives of very

different ecological and trophic groups including from meso- and macroplankton to micro-

and eunekton, demersal and typical pelagic neritic, slope and oceanic forms that occupied

the niches of consumers from I-II to IV orders. Same wide diversity of ecological forms

probably is characteristic for predators of this squid. By food and parasite data there are

well-marked multistage squid life cycle that is conditional on predator-prey size relations.

All revealed helminth are in the larval stage, have broad specificity. They use as

intermediate and transport hosts various planktonic invertebrates, small fishes and squids

at same stages of life cycles (Hochberg, 1990). Their life cycles are realized on trophic

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chains of the demersal and pelagic communities and squid are infected by eating infected

prey - intermediate and transport hosts. Most important sources for squid infestation with

larvae of cestodes, nematodes and trematodes are myctophids and other plankton-eating

fishes, squids, euphausiids and shrimps (Zuev et al., 1985; Hochberg, 1990). Studied squid

is a transport host for these helminths, with scombroid (trematodes) and xiphoid fishes

(nematodes), skates and sharks (cestodes) as the definitive hosts.

The northwestern African population of Todarodes sagittatus is member of

specific community of Cap Blanc upwelling zone that situated mainly between 18 and 23°

N. In that community this squid is “strong interactor” that organizes community structure

at the consumer levels from II-III to IV-V orders and direct energy and matter flows.

During its daily vertical (up to 200-800 meters) and ontogenetic bathymetric (from slope

to shelf and back) migrations squid cross through diversity vertical zones and local shelf-

slope ecosystems. Hence Todarodes sagittatus is significant element in the “rigid

framework” of high mobile predators which integrate local ecosystems including demersal

and pelagic communities. This species is typical r-strategist. Its stock size was estimated to

be 10-30 thousand tons in years of low abundance to 80-120 thousand tons and more in

years of high abundance (Nigmatullin et al., 2002). Therefore the annual “flow” of matter,

energy and helminths passing via squid population and its ecosystem integrator role must

be significantly variable in the long-term aspect.

ACKNOWLEGEMENTS

We cordially thank the staffs of Laboratory of Commercial invertebrates of

AtlantNIRO for samples collecting that used in this paper. Special thanks to S.S.

Shulman, K.N. Nesis, A.A. Kovaleva and A.V. Gaevskaya for helpful discussions and

consultations and to Abdelkarim Muhitdin and Hassan Moustahfid for technical

assistance. This study was supported by the Russian Foundation for Basic Research,

project No 06-04-49806.

.

REFERENCES

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Arkhipkin A.I., Laptikhovsky V.V., Golub A.N. 1999. Population structure and

growth of the squid Todarodes sagittatus (Cephalopoda: Ommastrephidae) in north-west

African waters. J. Mar. Biol. Ass. U. K., 79 (3): 467-477.

Gaevskaya A.V. 1977. Helminth fauna of the Atlantic squid Sthenoteuthis pteropus

(Steenstrup). Sci. Rep. Higher School., ser. Biol. Sci., 8: 47-52 (In Russian).

Gaevskaya A.V., Nigmatullin Ch.M. 1978. The helminth fauna of Atlantic squids of

the family Ommastrephidae (Cephalopoda: Oegopsida). Malacological Review, 11: 134-

135.

Gaevskaya A.V., Nigmatullin Ch.M. 1981. Several ecological aspects of the

parasitic relationships of the flying squid Sthenoteuthis pteropus (Steenstrup, 1855).

Biologicheskie Nauki, Ser. Biol. (Moscow), 1: 52-57 (In Russian with English abstract).

Hernandes-Garsia V. 1992. Preliminary notes about feeding of three species of

flying squids (Cephalopoda, Ommastrephidae) in the Northwest Africa (CECAF Area).

ICES C.M. /K: 24. 13 p.

Hernandes-Garsia V. 1995. Contribucion al conocimiento bioecologico de la

Familia Ommastrephidae Steenstrup, 1857 en el Atlantico Centro-Oriental. Tesis Doctoral

en Ciencias del Mar. Universidad de Las Palmas de Gran Canaria. 307 p.

Hernandes-Garsia V., Martin V. 1994. Stomach contents of two short-finned pilot

whale (Globicephala macrorhynchus Gray, 1846) (Cetacea, Delphinidae) off the Canary

Islands: A preliminary note. ICES C.M. /N: 16. – 9 p.

Hochberg F.G. 1990. Diseases of Mollusca: Cephalopoda. In: Diseases of marine

animals, vol. III. Cephalopoda to Urochordata (Kinne O., ed.). Biologisches Anstalt.

Helgoland, Hamburg: 47-227.

Margolis L., Esch G.W., Holmes J.M., Kuris A.M., Shad G.A. 1982. The use of

ecological terms. J. Parasitol., 68: 131-133.

Naidenova N.N., Nigmatullin Ch.M., Gaevskaya A.V. 1985. The helminth fauna and

host-parasite relations of squids Sthenoteuthis oualaniensis (Lesson) (Cephalopoda,

Ommastrephidae) in the Indian Ocean and the Red Sea. In: Hargris, W.J.Jr., (ed.).

Parasitology and pathology of marine organisms of the World Ocean. NOAA Technical

Reports, NMFS 25: 113-116.

Nesis K.N. 1987. Cephalopods of the world. T.F.H. Publications, Neptune City,

New Jersey. 351 p.

Nigmatullin Ch.M. 1972. Feeding of ommastrephids off North West African coast.

Kaliningrad: AtlantNIRO Publ., Trudy AtlantNIRO, 42: 152-155 (In Russian).

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Nigmatullin Ch.M. 2005. Towards the correct methodology of cephalopod feeding

study: review of some neglected problems. Libro de resumenes III Simposio Internacional

sobre calamares del Pacifico y II Taller Internacional sobre calamares (28 Noviembre - 2

Deciembre 2005, Lima, Peru). Resumen No 34. – IMARPE, Callao, Peru. 3 p.

Nigmatullin Ch.M. Laptikhovsky V.V., Moustahfid H. 1998. Population biology and

fishery of arrow squid Todarodes sagittatus (Lamarck) (Cephalopoda: Ommastrephidae) in

coast of northwestern Africa. Sushin V.A. (ed.). Fishery and biological researches carried

out by AtlantNIRO in 1996-1997. Trudy AtlantNIRO. Kaliningrad: AtlantNIRO Publ.: 72-

95 (In Russian with English abstract).

Nigmatullin Ch.M., Laptikhovsky V.V., Moustahfid H. 2002. Brief review on the

ecology in the North African population of arrow squid Todarodes sagittatus (Cephalopoda:

Ommastrephidae). Bull. Mar. Sci. 71 (2): 581-590.

Nigmatullin Ch.M., Toporova N.M. 1982. Feeding spectrum of squid Sthenoteuthis

pteropus (Steenstrup, 1880) in the epipelagic of the Tropical Atlantic. Kuhorenko, K.G.

(ed.), Food and food relations of fishes and invertebrates in the Atlantic. AtlantNIRO Press,

Kaliningrad: 3-8 (In Russian).

Piatkovski U., Hernandes-Garsia V., Clarke M.R. 1998. On the biology of the

European flying squid Todarodes sagittatus (Lamarck, 1798) (Cephalopoda,

Ommastrephidae) in the Central Eastern Atlantic. S. Afr. J. Mar. Sci. 20: 375-383.

Zuev G.V., Nigmatullin Ch.M., Nikolsky V.N. 1985. Nektonic oceanic squids

(Genus Sthenoteuthis). Agropromizdat Publ. House, Moscow. 224 p. (In Russian, English

contents).

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Fig. 1.Larvae of Cestoda: А - Scolex pleuronectis unilocularis; B - Scolex pleuronectis bilocularis

Fig. 2. Didymozoidae gen.sp.l.: A – I type; B - II type

Fig. 3. Hirudinella ventricosa

Fig. 4. Spinitectus sp. l.:

А –heard part of body; В –tail part of body;

С – heard part of body

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10

0

20

40

60

80

100

9-12 cm 13-16 cm 17-20 cm 21-24 cm

P, %

Didymozoidae gen.sp.mtc. (I,II) Scolex pleuronectisSpinitectus sp.l. Total infestation

Fig. 5. Ontogenetic variability in prevalence values for four size groups of Todarodes sagittatus

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Table 1. The list of known preys of Todarodes sagittatus off Northwestern African coast (1 – by Hernandes-Garcia, 1992, 1995 and Piatkowski et al., 1998; without numerals – our data) Chaetognata Crustacea Misidacea Euphausiacea Euphausia sp. Thysanopoda sp. Meganyctiphanes norvegica Isopoda (1) Amphipoda Phronima sedentaria Phrosina semilunata Decapoda Parapenaeus longirostris Sergestes sp. Plesionica martia (1) Plesionica edwardsii (1) Plesionica heterocarpus Parapandalus sp. Pasiphaea sivado Pasiphaea sp. Oplophorus spinosus Zoea of Decapoda Munida sp. Galatheidae gen.sp. (1) Squilla sp. Anomura gen. sp. Larvae of hermit crabs Gastropoda, Heteropoda Carinaria sp.

Cephalopoda Sepiola sp. Sepietta oweniana Sepia elegans Sepiella ornata Alloteuthis africana Abraliopsis sp. Onychoteuthis banksi Illex coindetii Todaropsis eblanae Todarodes sagittatus Brachioteuthis? Riisei Heliocranchia sp. (1) Leachia sp. (1) Thaliacea (salps) Pisces Myctophum punctatum Diaphus dumerelii (1) Lampanyctus sp. (1) Hygophum sp. (1) Notoscopelus sp. Belonidae gen. sp. Scomberesox saurus Trichiurus lepturus Chlorophtalmus atlantica Synagrops microlepis Dentex sp. Capros aper (1) Epigonus telescopes (1) Microchirus boscanion Macrourinae jv.. (1) Paralepididae jv.

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Table 2. Sex and ontogenetic / seasonal variability of food items of Todarodes sagittatus at the Northwestern African coast

March 1971 May 1971 June-July

1974, 1995, 1997

November-December

1969 ML 5-15 cm ML 10-19 cm ML 15-25 cm ML 23-31 cm

females males total total total total

Food groups

N% V% N% V% N% V% N% V% N% V% N% V% Crustacea, including 100 49 96 49 98 49 85 61 44 8 44 21 Amphipoda - - - - - - 2 - - - - - Euphausiids 100 49 96 49 97 49 31 8 32 1 - - Mysids - - - - - - - - 1 - - - Shrimps 2 - - - 1 - 62 53 3 1 39 10 Plesionica heterocarpus 2 - - - 1 - 55 50 - - 38 10 Parapenaeus longirostris - - - - - - - - - - 6 - Sergestes sp. - - - - - - - - 1 - - - Oplophorus spinosus - - - - - - - - 1 - - - Pasiphaea sp. - - - - - - - - 1 - - - Larvae of crabs - - - - - - 4 1 - - - - Squilla sp. - - - - - - 2 - - - 6 11 Cephalopoda, including. 20 - 16 2 18 1 40 3 12 1 22 22 Sepietta oweniana - - - - - - 4 - - - - - Sepia elegans - - - - - - - - - - 6 - Alloteuthis africana - - - - - - 2 - - - - - Todaropsis eblanae - - - - - - 2 - - - - - Illex coindetii - - - - - - 2 - - - - - Todarodes sagittatus 2 - 1 - 2 - - - 2 - - - Brachioteuthis sp. - - 1 - 1 - 8 1 - - - - Enoploteuthidae 4 - - - 2 - - - 1 - 17 22 Onychoteuthis banksi - - - - - - 2 - - - 6 - Pisces, including. 94 51 87 49 90 50 51 36 81 81 94 57 Myctophidae 77 43 65 40 70 41 36 33 59 70 61 57 Paralepididae - - - - - - - - - - - - Apogonidae - - - - - - - - - - 6 - Sparidae - - - - - - - - - - 11 - Chlorophtalmidae - - - - - - - - - - 6 - Beloniformes - - - - - - 2 - - - - - Chlorophtalmus sp. - - - - - - - - - - 6 - Dentex sp. - - - - - - - - - - 6 - Synagrops microlepis - 9 - - - 4 - - - - 6 - Predatory fishes, jv - - - - - - - - 5 5 - - Fishes indet. 16 - 22 2 19 5 11 3 17 6 22 - Trawl food, including - - - - - - - - 33 10 - - Todarodes sagittatus - - - - - - - - 33 10 - - Transit food 27 - 17 - 21 - 8 - 20 - 11 - Trawler’s offals 2 - - - 1 - - - - - - - Number of stomachs 49 17 69 23 118 40 48 28 193 89 18 9

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Table 3. Helminth fauna and infestation rates of Todarodes sagittatus

ML 9.4-24.4 cm Parasites P,%* I, sp. MI, sp. A, sp. Phyllobothrium sp. l. 1.1 (0-5.9) 1 0.9 0.01 Scolex pleuronectis bilocularis 3.2 (0-9.8) 1 0.9 0.03 Scolex pleuronectis unilocularis 22.3 (10.6-35.2) 1-2 3.1 0.7 Didymozoidae gen.sp. mtc(I,II) 49,1 (34.4-63.8) 1-14 2.6 1.3 Hirudinella ventricosa 0.6 (0-4.8) 1 1.0 0.01 Porrocaecum sp. l. 0.6 (0-4.8) 1 1.0 0.01 Spinitectus sp.l. 4.2 (0-11.4) 1-2 1.9 0.08 Total infestation 66.1 (51.8-79.6) *Prevalence (P) with confidence limits (p=0.95) Table 4. Helminth infeststion of females and males of Todarodes sagittatus. Prevalence (P) with confidence limits (p=0.95), and abundance (A) of infection in squid by sex

Female

105 spec. ML 11.5-24.4cm

Males 43 spec.

ML 12.4-20.6cm

Parasites P, %* MI,

sp. A, sp.

P, % MI, sp.

A, sp.

Scolex pleuronectis (unilocularis and bilocularis)

27.6 (8.3-40.9)

3.3 0.9 23.3 (0-46.4)

1.3 0.3

Didymozoidae gen.sp. mtc(I,II) 48.6 (29.3-67.3)

2.5 1.2 44.2 (15.6-73.4)

3.4 1.5

Spinitectus sp.l. 2,9 (0-11,8)

3.8 0.1 9.3 (0-31.0)

0.8 0.1

Total infestation 64.8 (45.6-81.9)

65.1 (35.8-91.4)

*Prevalence (P) with confidence limits (p=0.95) Table 5. Ontogenetic variability in helminth composition and indices of Todarodes sagittatus infestation

ML, cm 9-12 13-16 17-20 21-24 n, spec. 26 17 72 18

P, %* MI,sp A,sp. P, %* MI,sp A,sp. P, %* MI,sp A,sp. P, %* MI,sp A,sp. Scolex pleuronectis (unilocularis and bilocularis)

7.7 (0-35.8) 2.6 0.2

14.3 (0-52.8) 0.7 0.1

37.5 (2.5-73.5) 2.9 1.1

33.3 (0-76.9) 3.0 1.0

Didymozoidae gen.sp.mtc. (I,II)

73.1 (37.0-100) 3.3 2.4

53.1 (9.8-96) 2.8 1.5

40.3 (5.9-75.4) 2.5 1.0

38.9 (0-82.6) 3.1 1.25

Spinitectus sp.l. 7.7 (0-35.8) 1.3 0.1

6.9 (0-52.4) 1.4 0.1

Total infestation 76.9 (41.7-100)

59.2 (14.4-100)

66.7 (39.3-91.7)

56.7 (12.1-96.9)

*Prevalence (P) with confidence limits (p=0.95)