Parasites of South African Sardines, Sardinops Sagax, and an Assessment of Their Potential As Biological Tags

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

Abstract The 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 aempted 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.

Introduction The South African sardine Sardinops sagax of at least three putative stocks (Coetzee et (Jenyns, 1842) is an economically valuable al., 2008; van der Lingen and Hugge, 2003; and ecologically important ﬁsh species. Pres- van der Lingen et al., 2010; Wessels et al., in ently the possible existence of multiple stocks review, Idris et al., in review). Sardines occur in this population is under investigation using a along the entire coast of South Africa (Beckley variety of methods, with studies of distribution and van der Lingen, 1999), occupying habitats and spawning areas, meristic characteristics that are inﬂuenced by two major ocean cur- and morphometrics suggesting the existence 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 provide ideal drivers for changes in distribution Hutchings et al., 2009). The Agulhas Current paerns of less tolerant marine species, and for brings warm water from the western Indian their associated parasites. Ocean southwards along the east coast, whilst the Benguela Current moves cold water from Parasites have been used as biological tags for the South Atlantic Ocean northwards along stock discrimination of marine fish in many the west coast (Figure 1). The Agulhas Bank parts of the world, but this approach has not off the south coast displays characteristics of yet been aempted in South Africa. The main both an upwelling and a temperate shallow principle underlying the use of fish parasites shelf system, whereas the west coast shows as biological tags is that fish can only become seasonal, wind-driven coastal upwelling at dis- infected with a parasite within the endemic crete centres. The Orange River, with its huge area of that parasite (MacKenzie and Abaunza, catchment area, pours sediments and freshwater 2005). In the Southwest Atlantic, seven studies into the sea along the west coast, further alter- involving the use of parasites as biological tags ing local environmental conditions towards have been published (Timi, 2007). These studies Namibia. Whereas sardines are able to tolerate have been successful largely due to the specific these very different environmental conditions marine environment on the Atlantic continental along the South African coast, such differences 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. Bull. Eur. Ass. Fish Pathol., 32(2) 2012, 43 bution paerns of marine parasites are mainly total length (TL, cm) measured, and all organs determined by temperature-salinity profiles and initially examined for parasitic infections under their association with specific masses of water. a dissection microscope at magnifications of 10x to 63x, or under a compound microscope at 40x Given the contrast in water masses off South to 1000x. Later, only eyes, gills, viscera, testes Africa’s coast and that the distributions of some and muscle were examined. Parasite species parasite species associated with sardines will were preserved in either 70% ethanol or 10% likely be determined largely by local environ- buffered neutral formalin for later identification. mental conditions, we considered the likelihood Selected specimens were stained with Mexican that studies of one or more sardine parasites Red textile stain to clarify details of internal could provide information to assess the pos- anatomy (Berland, 2005). sibility of stock structure was high. Accord- ingly, we conducted a preliminary survey of The terms used to describe levels of infection the parasite fauna of S. sagax off South Africa are as defined by Bush et al. (1997). Prevalence with the aim of identifying parasites of potential is the number of fish infected divided by the use as biological tags in population studies of number of fish examined, here expressed as a these sardines. The only previous survey of percentage. Mean intensity is the total number the parasite fauna of these sardines from this of parasites of a particular taxon divided by the region is that of Parukhin (1975). number of infected fish.

Methods Results Sardines were collected from seven localities Seven samples, totalling 102 sardines, ranging around the South African coast, six from DAFF in total length from 12.0 to 23.0 cm, were ex- research cruises and one from a commercial amined (Table 1). Seven diﬀerent parasite taxa catch (Figure 1). Fish were labeled, bagged and were recorded (Table 2). frozen immediately aVer capture, apart from the commercial sample, which was examined The highest prevalence of infection was of di- fresh. In the laboratory ﬁsh were thawed, their 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. 04/06/2010 15 22.2 (21.0-23.0) 2. 20/10/2010 15 20.8 (18.0-22.0) 3. 16/06/2010 18 17.6 (12.0-20.5) 4. 16/11/2010 10 15.5 (14.5-16.6) 5. 19/11/2010 14 15.5 (14.0-16.5) 6. 19/11/2010 15 14.2 (13.5-14.8) 7. 24/06/2010 15 14.7 (12.0-23.0) 44, Bull. Eur. Ass. Fish Pathol., 32(2) 2012 found in the humours of the eyes of 46% of all the testes of 40% of all male fish examined, fish examined (Figure 2a and b). Prevalences with west coast localities showing the highest ranged from 0 to 93%, with samples from the prevalences. Fewer male fish were examined west coast having the highest values, whereas from south coast localities, where no infections in south coast samples prevalences were much were recorded. This appears to be a new host lower (Table 3). record for E. sardinae.

The testicular coccidian protozoan Eimeria sar- The myxozoan Kudoa thyrsites (Gilchrist, 1924) dinae (Thélohan, 1890) Reichenow, 1921 infected 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 (%) MI Coccidia *Eimeria sardinae (Thélohan, 1890) Testes #40 - Myxosporea Kudoa thyrsites (Gilchrist, 1924) Musculature 17 - Monogenea Mazocraes sardinopsi (Lebedev and Parukhin, 1969) Gill ﬁlaments 1 1.0 Digenea “Tetracotyle” metacercariae Eyes 46 3.5 Cestoda *Tentacularia coryphaenae Bosc, 1802 Musculature 1 1.0 Copepoda Parasitica Clavellisa ilishae Pillai, 1963 Gill rakers 10 1.2 *Nothobomolochus fradei (Marques, 1965) Gill cavity, operculum 10 1.2

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

Sample number Prevalence (%) Mean intensity (range) 1 60 1.9 (1-3) 2 93 4.6 (1-11) 3 78 4.2 (1-10) 4 20 1.0 (1) 5 33 1.0 (1) 6 20 1.3 (1-2) 7 0 0 Bull. Eur. Ass. Fish Pathol., 32(2) 2012, 45

a b

Figure 2. “Tetracotyle” metacercaria: fresh specimen in situ (a) and fresh specimen stained with Mexican Red textile stain (b). of all fish examined. Prevalence was generally ously reported from the eyes of S. sagax by highest at west coast localities, with larger fish Parukhin (1975). They are characteristic of the having the highest infection levels. digenean family Strigeidae and have life-cycles involving gastropod first intermediate hosts The parasitic copepod Clavellisa ilishae Pillai, and fish-eating bird final hosts (Niewiadomska, 1963 was found aached to the gill rakers of 10% 2002). The gastropod and bird host species of of all sardines examined, with the highest preva- this particular digenean are still unknown. Timi lence of 40% recorded at Mossel Bay (Sample 4, et al. (1999) described “tetracotyle” metacercar- Table 1). A second species of parasitic copepod, iae from the eyes of anchovy Engraulis anchoita Nothobomolochus fradei (Marques, 1965), was also off the coast of Argentina as Cardiocephaloides found infecting the gill cavity and operculum sp. Based on the geographical distribution and of 10% of all fish examined. This is a new host trophic relationships of different hosts, Timi et record for N. fradei. al. (1999) considered that their metacercariae probably belong to the species Cardiocephaloides A single sardine from a sample taken off Port physalis (Lutz, 1926), a parasite of penguins Sphe- Elizabeth harboured one specimen of the niscus spp. C. physalis was reported from jackass monogenean gill parasite Mazocraes sardinopsi penguins Spheniscus demersus in South Africa (Lebedev and Parukhin, 1969). A single plerocer- by Randall and Bray (1983) and more recently coid of the trypanorhynch cestode Tentacularia by Horne et al. (2011).The metacercariae from coryphaenae Bosc, 1802 was found encysted in the our sardines may be of this species. muscle of one fish from near Cape Point. This is a new host record for T. coryphaenae. Kudoa thyrsites, originally described from Cape snoek (Thyrsites atun) by Gilchrist (1924), is a Discussion notorious cosmopolitan parasite causing post “Tetracotyle” type metacercariae were previ- mortem tissue myoliquefaction (Moran et al., 46, Bull. Eur. Ass. Fish Pathol., 32(2) 2012

1999). In South Africa sardines are amongst two other clupeid species in the Mediterranean the most heavily infected fish, causing much (El-Rashidy and Boxshall, 2010). frustration and economic loss in the canning industry. This parasite species has also been The trypanorhynch cestode T. coryphaenae has reported from several other fish species in South been reported as an adult from 11 species of Africa (Webb, 1990). shark and as a plerocercoid from many species of teleost fish around the world (Palm, 2004). Eimeria sardinae infects clupeoid fishes in many parts of the world. Its occurrence can Of the seven parasite species found in the have serious effects on the reproduction of an present study, we consider the “tetracotyle” affected population and in extreme cases in- digenean to have the most potential as a bio- fections may result in sterility of the host due logical tag, as it fulfils most of the established to parasitic castration (Pinto, 1956). That 40% criteria for a good tag parasite (MacKenzie of male S. sagax examined in this study were and Abaunza, 2005). Specifically, preliminary infected with this parasite is therefore a cause results suggest that it has a discontinuous dis- for concern. tribution in the study area, is site specific and is likely to have a long life span in sardines. The monogenean M. sardinopsi was previously “Tetracotyle” metacercariae of the genus Car- recorded by Parukhin (1975), as Neomazocraes diocephaloides were among the tag parasites sardinopsi Lebedev and Parukhin, 1969, on four used by Timi (2003) to help identify stocks of S. sagax caught in Walvis Bay off the coast of Argentine anchovy E. anchoita in the south-west Namibia. This species was reassigned to the Atlantic. Freshwater forms were also used as genus Mazocraes Hermann, 1782 by Mamaev tags in an earlier study by Pronin (1965) of the (1982). stock structure of whitefish in a freshwater system in Russia. Further samples of sardines The parasitic copepod C. ilishae was originally will be examined to determine the geographical described by Pillai (1964) from Tenualosa ilisha distribution of the sardine metacercariae and in the Bay of Bengal and subsequently reported their occurrence in different sizes and ages of from two other clupeoid species in the same sardine. Their specific identity and life cycle region (Pillai, 1985). It was previously recorded will also be investigated. from S. sagax off South Africa, as Clavellissa cf. ilishae, by Kensley and Grindley (1973), and Acknowledgements more recently from another clupeoid host, We thank the National Research Founda- Sardinella aurita, in the Mediterranean by El- tion’s Thuthuka Programme Visiting Scholars Rashidy and Boxshall (2010). The other copepod Fund of the University of Cape Town URC found in this study, N. fradei, was originally for funding the visit of K. MacKenzie. We also described from the clupeid Sardinella maderensis thank Prof. G.A. Boxshall of the Natural History in the Gulf of Guinea by Marques (1965). It has Museum, London for confirming the identity since been reported from an atherinid fish in of Nothobomolochus fradei, and Ms T. Lamont the Arabian Gulf (Ho and Sey, 1996), and from of the Department of Environmental Affairs, Bull. Eur. Ass. Fish Pathol., 32(2) 2012, 47

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