parasites of south african sardines, - eafp · parasites of south african sardines, ... map of the...

Bull. Eur. Ass. Fish Pathol., 32(2) 2012, 41

Parasites of South African sardines, Sardinops sagax, and an assessment of

their potential as biological tags

C. Reed1*, K. MacKenzie2 and C. D. van der Lingen3

1Department of Zoology, University of Cape Town, Private Bag X3, Rondebosch, 7701, South Africa; 2Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen,

AB24 2TZ, United Kingdom; 3Fisheries Management, Department of Agriculture, Forestry and Fisheries, Private Bag X2, Rogge Bay 8012, Cape Town; Marine Research Institute,

University of Cape Town, Private Bag X3, Rondebosch, 7701, South Africa

AbstractThe use of parasites as biological tags for stock identification of marine fish has been successfully implemented in many parts of the world but has not previously been a�empted in South Africa. The present study was designed to assess the potential of the method in addressing questions concerning stock structure of the local population of sardines Sardinops sagax (Jenyns, 1842). Seven samples, totaling 102 sardines, were examined from localities ranging from south of Cape Columbine on the west coast to east of Algoa Bay on the east coast. Seven parasite taxa were recorded, including six identified to species level and three new host records. Digenean “tetracotyle” metacercariae infected the eyes at an overall prevalence of 46%, the myxozoan Kudoa thyrsites (Gilchrist, 1924) infected the musculature of 17%, while the parasitic copepods Clavellisa ilishae (Pillai, 1962) and Nothobomolochus fradei (Marques, 1965) each infected the gills of 10%. The coccidian Eimeria sardinae (Thélohan, 1890) Reichenow, 1921 infected the testes of 40% of male sardines. One sardine caught off Port Elizabeth harboured a single specimen of the monogenean gill parasite Mazocraes sardinopsi (Lebedev and Parukhin, 1969), and the muscle of another from Cape Point harboured a single plerocercoid of the trypanorhynch cestode Tentacularia coryphaenae Bosc, 1802. Initial indications are that the “tetracotyle” metacercariae have the greatest potential as biological tags.

IntroductionThe South African sardine Sardinops sagax (Jenyns, 1842) is an economically valuable and ecologically important fish species. Pres-ently the possible existence of multiple stocks in this population is under investigation using a variety of methods, with studies of distribution and spawning areas, meristic characteristics and morphometrics suggesting the existence

of at least three putative stocks (Coetzee et al., 2008; van der Lingen and Hugge�, 2003; van der Lingen et al., 2010; Wessels et al., in review, Idris et al., in review). Sardines occur along the entire coast of South Africa (Beckley and van der Lingen, 1999), occupying habitats that are influenced by two major ocean cur-rents that create distinct gradients of changing

* Corresponding author’s e-mail: [email protected]

42, Bull. Eur. Ass. Fish Pathol., 32(2) 2012

environmental conditions around the coast (see Hutchings et al., 2009). The Agulhas Current brings warm water from the western Indian Ocean southwards along the east coast, whilst the Benguela Current moves cold water from the South Atlantic Ocean northwards along the west coast (Figure 1). The Agulhas Bank off the south coast displays characteristics of both an upwelling and a temperate shallow shelf system, whereas the west coast shows seasonal, wind-driven coastal upwelling at dis-crete centres. The Orange River, with its huge catchment area, pours sediments and freshwater into the sea along the west coast, further alter-ing local environmental conditions towards Namibia. Whereas sardines are able to tolerate these very different environmental conditions along the South African coast, such differences

provide ideal drivers for changes in distribution pa�erns of less tolerant marine species, and for their associated parasites.

Parasites have been used as biological tags for stock discrimination of marine fish in many parts of the world, but this approach has not yet been a�empted in South Africa. The main principle underlying the use of fish parasites as biological tags is that fish can only become infected with a parasite within the endemic area of that parasite (MacKenzie and Abaunza, 2005). In the Southwest Atlantic, seven studies involving the use of parasites as biological tags have been published (Timi, 2007). These studies have been successful largely due to the specific marine environment on the Atlantic continental shelf of South America and because the distri-

Figure 1. Map of the South African coast showing sardine sampling locations (black circles) superimposed on a sea surface temperature image (°C, scale on right) composited for November 2010 from satellite data. The insert shows the image area relative to Southern Africa, and the approximate locations of the Agulhas and Benguela Currents, the 200m depth isobath (thin dashed line) and the locations of places mentioned in the text are given.


bution pa�erns of marine parasites are mainly determined by temperature-salinity profiles and their association with specific masses of water.

Given the contrast in water masses off South Africa’s coast and that the distributions of some parasite species associated with sardines will likely be determined largely by local environ-mental conditions, we considered the likelihood that studies of one or more sardine parasites could provide information to assess the pos-sibility of stock structure was high. Accord-ingly, we conducted a preliminary survey of the parasite fauna of S. sagax off South Africa with the aim of identifying parasites of potential use as biological tags in population studies of these sardines. The only previous survey of the parasite fauna of these sardines from this region is that of Parukhin (1975).

MethodsSardines were collected from seven localities around the South African coast, six from DAFF research cruises and one from a commercial catch (Figure 1). Fish were labeled, bagged and frozen immediately a�er capture, apart from the commercial sample, which was examined fresh. In the laboratory fish were thawed, their

total length (TL, cm) measured, and all organs initially examined for parasitic infections under a dissection microscope at magnifications of 10x to 63x, or under a compound microscope at 40x to 1000x. Later, only eyes, gills, viscera, testes and muscle were examined. Parasite species were preserved in either 70% ethanol or 10% buffered neutral formalin for later identification. Selected specimens were stained with Mexican Red textile stain to clarify details of internal anatomy (Berland, 2005).

The terms used to describe levels of infection are as defined by Bush et al. (1997). Prevalence is the number of fish infected divided by the number of fish examined, here expressed as a percentage. Mean intensity is the total number of parasites of a particular taxon divided by the number of infected fish.

ResultsSeven samples, totalling 102 sardines, ranging in total length from 12.0 to 23.0 cm, were ex-amined (Table 1). Seven different parasite taxa were recorded (Table 2).

The highest prevalence of infection was of di-genean metacercariae of the “tetracotyle” type

Table 1. Sampling details, with samples ordered from the westernmost (#1) to the easternmost (#7).

Sample number and date No. of sardines examined Mean total length (cm, range)1. 04/06/20102. 20/10/20103. 16/06/20104. 16/11/20105. 19/11/20106. 19/11/20107. 24/06/2010

15151810141515

22.2 (21.0-23.0)20.8 (18.0-22.0)17.6 (12.0-20.5)15.5 (14.5-16.6)15.5 (14.0-16.5)14.2 (13.5-14.8)14.7 (12.0-23.0)


found in the humours of the eyes of 46% of all fish examined (Figure 2a and b). Prevalences ranged from 0 to 93%, with samples from the west coast having the highest values, whereas in south coast samples prevalences were much lower (Table 3).

The testicular coccidian protozoan Eimeria sar-dinae (Thélohan, 1890) Reichenow, 1921 infected

the testes of 40% of all male fish examined, with west coast localities showing the highest prevalences. Fewer male fish were examined from south coast localities, where no infections were recorded. This appears to be a new host record for E. sardinae.

The myxozoan Kudoa thyrsites (Gilchrist, 1924) was found infecting the musculature of 17%

Table 2. Parasites recorded from South African sardines. Pr (%) = percentage prevalence of infection; MI = mean intensity of infection. Prevalence only is given for protozoans and myxozoans. * denotes new host record, # indicates only males were included in prevalence calculation.

Parasite Site of infection Pr (%) MICoccidia *Eimeria sardinae (Thélohan, 1890)Myxosporea Kudoa thyrsites (Gilchrist, 1924)Monogenea Mazocraes sardinopsi (Lebedev and Parukhin, 1969) Digenea “Tetracotyle” metacercariaeCestoda *Tentacularia coryphaenae Bosc, 1802Copepoda Parasitica Clavellisa ilishae Pillai, 1963 *Nothobomolochus fradei (Marques, 1965)

Testes

Musculature

Gill filaments

Eyes

Musculature

Gill rakersGill cavity, operculum

#40

17

1

46

1

1010

-

-

1.0

3.5

1.0

1.21.2

Table 3. Infections with “tetracotyle” metacercariae in sardines from different samples (see Figure 1).

Sample number Prevalence (%) Mean intensity (range)1234567

6093782033200

1.9 (1-3)4.6 (1-11)4.2 (1-10)

1.0 (1)1.0 (1)

1.3 (1-2)0


of all fish examined. Prevalence was generally highest at west coast localities, with larger fish having the highest infection levels.

The parasitic copepod Clavellisa ilishae Pillai, 1963 was found a�ached to the gill rakers of 10% of all sardines examined, with the highest preva-lence of 40% recorded at Mossel Bay (Sample 4, Table 1). A second species of parasitic copepod, Nothobomolochus fradei (Marques, 1965), was also found infecting the gill cavity and operculum of 10% of all fish examined. This is a new host record for N. fradei.

A single sardine from a sample taken off Port Elizabeth harboured one specimen of the monogenean gill parasite Mazocraes sardinopsi (Lebedev and Parukhin, 1969). A single plerocer-coid of the trypanorhynch cestode Tentacularia coryphaenae Bosc, 1802 was found encysted in the muscle of one fish from near Cape Point. This is a new host record for T. coryphaenae.

Discussion“Tetracotyle” type metacercariae were previ-

ously reported from the eyes of S. sagax by Parukhin (1975). They are characteristic of the digenean family Strigeidae and have life-cycles involving gastropod first intermediate hosts and fish-eating bird final hosts (Niewiadomska, 2002). The gastropod and bird host species of this particular digenean are still unknown. Timi et al. (1999) described “tetracotyle” metacercar-iae from the eyes of anchovy Engraulis anchoita off the coast of Argentina as Cardiocephaloides sp. Based on the geographical distribution and trophic relationships of different hosts, Timi et al. (1999) considered that their metacercariae probably belong to the species Cardiocephaloides physalis (Lutz, 1926), a parasite of penguins Sphe-niscus spp. C. physalis was reported from jackass penguins Spheniscus demersus in South Africa by Randall and Bray (1983) and more recently by Horne et al. (2011).The metacercariae from our sardines may be of this species.

Kudoa thyrsites, originally described from Cape snoek (Thyrsites atun) by Gilchrist (1924), is a notorious cosmopolitan parasite causing post mortem tissue myoliquefaction (Moran et al.,

Figure 2. “Tetracotyle” metacercaria: fresh specimen in situ (a) and fresh specimen stained with Mexican Red textile stain (b).

a b


1999). In South Africa sardines are amongst the most heavily infected fish, causing much frustration and economic loss in the canning industry. This parasite species has also been reported from several other fish species in South Africa (Webb, 1990).

Eimeria sardinae infects clupeoid fishes in many parts of the world. Its occurrence can have serious effects on the reproduction of an affected population and in extreme cases in-fections may result in sterility of the host due to parasitic castration (Pinto, 1956). That 40% of male S. sagax examined in this study were infected with this parasite is therefore a cause for concern.

The monogenean M. sardinopsi was previously recorded by Parukhin (1975), as Neomazocraes sardinopsi Lebedev and Parukhin, 1969, on four S. sagax caught in Walvis Bay off the coast of Namibia. This species was reassigned to the genus Mazocraes Hermann, 1782 by Mamaev (1982).

The parasitic copepod C. ilishae was originally described by Pillai (1964) from Tenualosa ilisha in the Bay of Bengal and subsequently reported from two other clupeoid species in the same region (Pillai, 1985). It was previously recorded from S. sagax off South Africa, as Clavellissa cf. ilishae, by Kensley and Grindley (1973), and more recently from another clupeoid host, Sardinella aurita, in the Mediterranean by El-Rashidy and Boxshall (2010). The other copepod found in this study, N. fradei, was originally described from the clupeid Sardinella maderensis in the Gulf of Guinea by Marques (1965). It has since been reported from an atherinid fish in the Arabian Gulf (Ho and Sey, 1996), and from

two other clupeid species in the Mediterranean (El-Rashidy and Boxshall, 2010).

The trypanorhynch cestode T. coryphaenae has been reported as an adult from 11 species of shark and as a plerocercoid from many species of teleost fish around the world (Palm, 2004).

Of the seven parasite species found in the present study, we consider the “tetracotyle” digenean to have the most potential as a bio-logical tag, as it fulfils most of the established criteria for a good tag parasite (MacKenzie and Abaunza, 2005). Specifically, preliminary results suggest that it has a discontinuous dis-tribution in the study area, is site specific and is likely to have a long life span in sardines. “Tetracotyle” metacercariae of the genus Car-diocephaloides were among the tag parasites used by Timi (2003) to help identify stocks of Argentine anchovy E. anchoita in the south-west Atlantic. Freshwater forms were also used as tags in an earlier study by Pronin (1965) of the stock structure of whitefish in a freshwater system in Russia. Further samples of sardines will be examined to determine the geographical distribution of the sardine metacercariae and their occurrence in different sizes and ages of sardine. Their specific identity and life cycle will also be investigated.

Acknowledgements We thank the National Research Founda-tion’s Thuthuka Programme Visiting Scholars Fund of the University of Cape Town URC for funding the visit of K. MacKenzie. We also thank Prof. G.A. Boxshall of the Natural History Museum, London for confirming the identity of Nothobomolochus fradei, and Ms T. Lamont of the Department of Environmental Affairs,


Cape Town, for providing the satellite image used in Figure 1.

ReferencesBeckley LE and van der Lingen CD (1999).

Biology, fishery and management of sardines (Sardinops sagax) in southern African waters. Marine and Freshwater Research 50, 955-978.

Berland B (2005). “Whole Mounts”. Occasional Publication No.1, Institute of Oceanography, KUSTEM, Malaysia, 54 pp.

Bush AO, Lafferty KD, Lotz JM and Shostak AW (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575-583.

Coetzee JC, van der Lingen CD, Hutchings L and Fairweather TP (2008). Has the fishery contributed to a major shi� in the distribution of South African sardine? ICES Journal of Marine Science 65, 1676-1688.

El-Rashidy HH and Boxshall GA (2010). Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Systematic Parasitology 76, 19-38.

Gilchrist JDF (1924). A protozoal parasite Chloromyxum thyrsites sp.n. of the Cape sea fish, the “snoek” (Thyrsites atun, Euplin). Transactions of the Royal Society of South Africa 11, 263-273.

Ho J-S and Sey O (1996). Parasitic copepods of marine fishes from Kuwait: a preliminary report. Kuwait Journal of Science & Engineering 23, 61-69.

Horne EC, Bray RA and Bousfield B (2011). The presence of the trematodes Cardiocephaloides physalis and Renicola sloanei in the African penguin Spheniscus demersus on the east coast of South Africa. Ostrich 82, 157-160.

Hutchings L, van der Lingen CD, Shannon LJ, Crawford RJM, Verheye HMS, Bartholomae CH, van der Plas AK, Louw D, Kreiner A, Ostrowski M, Fidel Q, Barlow RG, Lamont

T, Coetzee J, Shillington F, Veitch J, Currie JC and Monteiro PMS (2009). The Benguela Current: An ecosystem of four components. Progress in Oceanography 83, 15–32.

Idris I, Moloney CL and van der Lingen CD (In review). Spatial variability in branchial basket meristics and morphology of southern African sardine (Sardinops sagax). African Journal of Marine Science.

Kensley B and Grindley JR (1973). South African Parasitic Copepoda. Annals of the South African Museum 62, 69-130.

MacKenzie K and Abaunza P (2005). Parasites as biological tags. In “Stock Identification Methods: Applications in Fisheries Science” (S.X. Cadrin, K.D.Friedland, and J.R.Waldman, eds.), p. 211-226. Elsevier Academic Press.

Mamaev YL (1982). Notes on the systematics of mazocraeid monogeneans with a redescription of some poorly studied taxa. Helminthologia 19, 25-39.

Marques E (1965). Copépodes parasitas de peixes marinhos de S. Tomé. Gracia de Orta (Lisboa) 13, 185-192.

Moran JDW, Whitaker DJ and Kent ML (1999). A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172, 163-196.

Niewiadomska K (2002). Family Strigeidae Railliet, 1919. In “Keys to the Trematoda, Vol. 1” (D. I. Gibson, A. Jones and R.A. Bray, eds.), p. 231-241. CAB International and The Natural History Museum, London.

Palm HW (2004). “The Trypanorhyncha Diesing, 1863”. PKSPL-IPB Press, Bogor, Indonesia, 710 pp.

Parukhin AM (1975). Special features of the helminth fauna of Clupeiformes in Southern Seas. Trudy Biologo-pochvennogo institute, Novaya Seriya 26, 143-151 [In Russian].

Pillai NK (1964). Copepods parasitic on South Indian fishes: Family Anthosomidae-I.


Journal of the Bombay Natural History Society 60, 655-670.

Pillai NK (1985). “Fauna of India. Parasitic copepods of marine fishes”. Zoological Survey of India, Calcu�a, India, 900 pp.

Pinto JS (1956). Parasitic castration in males of Sardina pilchardus (Walb.) due to testicular infestation by the coccidia Eimeria sardinae (Thélohan). Revista de la Faculdade de Ciencias de la Universidade de Lisboa Serie C 5, 209-214.

Pronin NM (1965). The parasite fauna of the whitefish as an indicator of local lake and river forms in the basin of the Charya river. Izvestia Zabaikal’skogo Otdeleniya Vsesoyuznogo Gel’mintologii Obschestvo 1, 74-77 [In Russian].

Randall RM and Bray RA (1983). Mortalities of jackass penguin Spheniscus demersus chicks caused by trematode worms Cardiocephaloides physalis. South African Journal of Zoology 18, 45-46.

Timi JT (2003). Parasites of Argentine anchovy in the south-west Atlantic: latitudinal pa�erns and their use for discrimination of host populations. Journal of Fish Biology 63, 90-107.

Timi JT (2007). Parasites as biological tags for stock discrimination in marine fish from South American Atlantic waters. Journal of Helminthology 81, 107-112.

Timi JT, Martorelli SR and Sardella NH (1999). Digenetic trematodes parasitic on Engraulis anchoita (Pisces: Engraulidae) from Argentina and Uruguay. Folia Parasitologica 46, 132-138.

van der Lingen CD and Hugge� JA (2003). The role of ichthyoplankton surveys in recruitment research and management of South African anchovy and sardine. In ”The Big Fish Bang. Procedings of the 26th Annual Larval Fish Conference” (HI Browman and AB Ski�esvik, eds.), p. 308-343. Institute of Marine Research, Bergen, Norway, ISBN 82-7461-059-8.

van der Lingen CD, Hendricks M, Durholtz MD, Wessels G and Mtengwane C (2010). Biological characteristics of sardine caught by the beach-seine fishery during the KwaZulu-Natal sardine run. African Journal of Marine Science 32, 309-330.

Webb SC (1990). Pap pilchards and Protozoa. South African Shipping News & Fishing Industry Review 45(4), 35.

Wessels G, Moloney CL and van der Lingen CD (In review). Spatial variation in meristic and morphometric characteristics of sardine Sardinops sagax around the coast of southern Africa. Journal of Fish Biology.

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