You are on page 1of 37

ANISAKIS INFECTION OF MACKERELS (Scomber spp.

) BOUGHT AT THE
DALAHICAN FISH PORT COMPLEX, LUCENA CITY, QUEZON

By

TRAZARAH HANOOF ELPEDES ARGARIN

An undergraduate thesis proposal presented to the faculty of the College of Fisheries in partial
fulfilment of the requirements for the degree of

BACHELOR OF SCIENCE IN FISHERIES

COLLEGE OF FISHERIES
CENTRAL LUZON STATE UNIVERSITY
Science City of Muñoz, Nueva Ecija

2015

0
INTRODUCTION

Background of the Study

Mackerel is a common name mostly applied to a number of different species of pelagic

fishes from the family Scombridae (http://en.wikipedia.org). They are found in both temperate

and tropical seas, mostly living along the coast or offshore in the oceanic environment

(http://en.wikipedia.org). The subfamily Scombrinae, belongs to the family Scombridae and is

composed of two groups with two tribes each (Collette and Nauen, 1983). The first group

comprises the tribes Sardini and Thunnini, and the second and more primitive group is composed

of the tribes Scombrini and Scomberomorini (Collette and Nauen, 1983). The tribe Scombrini

contains two genera of mackerels, Scomber and Rastrelliger and the characteristics

distinguishing both genera have been given by Matsui (1967).

Different species of Scomber are recognized: S. scombrus (Atlantic mackerel), S.

japonicus (Chub mackerel), and S. australasicus (Spotted Chub mackerel) (Collette and Nauen,

1983). Mackerel (Scomber spp.) is commercially fished in both sides of the Atlantic and its early

life history is intensely studied (Lockwood et al., 1981; Ware and Lambert, 1985; Coombs et al.,

2001).

Fishes like mackerel (Scomber spp.) are important hosts of parasites in aquatic

ecosystems, harboring wide variety of adult and immature forms and acting either as sole host or

as one in a series of hosts (Barber and Poulin, 2002).

Duffu and Hay (2001) stated that information on the food habits of marine fishes, such as

the predator-prey relationship, is useful in order to assess the role of marine fishes in the

1
ecosystem. This encouraged the present researcher to study the prevalence and intensity rate of

endoparasites found in Scomber species.

Parasites are organisms that live on or in an organism of another species known as the

host from where nutrients are obtained and gain benefits at the expense of the host

(http//www.dictionary.com). According to Barber and Poulin (2002), some parasites are

responsible for the outbreaks of diseases in fish populations and few (e.g., anisakid nematodes)

are capable of infecting humans. Adams et al. (1997) added that economically, parasites can

devaluate fish market value as it can cause spoilage and it is transmittable to humans. On the

other hand, prevalence of parasites in one habitat is indicative of the health of an ecosystem

(Adams et al., 1997; Hudson et al., 2006) and also determinant of the status of fish stocks

(Barber and Poulin, 2002).

Parasites have also been used as biological tag to investigate population structure of

commercially important species of fish (McKenzie, 2002; McKenzie et al., 2008), as indicator of

historical dispersal through migration (Rohde, 2002), as pollution indicator (Aloo et al., 2004)

and as important driver of biodiversity (Hudson et al., 2006).

Parasites influence individual host survival and reproduction, alter fish behavior and

migration patterns, and they can even regulate fish populations and affect fish community

structure (Garnick and Margolis, 1990; Barber and Poulin, 2002).

Statement of the Problem

Marine fishes constitute an important reserve as a food source for human consumption.

Mackerel (Scomber spp.) is one of the most preferred sources of food among Filipinos

(http://en.wikipedia.org/). It has a high demand in the market because it is affordable to

consumers (Roberts et al., 2001). But these fishes are susceptible to damage caused by parasites;

2
therefore, securing its quality is very important (http://en.wikipedia.org/). The common parasites

present in this species are still unidentified in Tayabas Bay, Quezon and thus, there is no

scientific basis on its present quality or condition.

Significance of the Study

The inventory of the anisakid nematodes present in mackerel will be a great help in

assessing the present quality of this species in Philippine water. Also, its possible effect to

human health and its corresponding treatments could be evaluated. Moreover, the use of these

parasites as biological indicators for fish stock assessment will be important for the possible

management of this fish stocks in Tayabas Bay. Additionally, the study will benefit the Bureau

of Fisheries and Aquatic Resources (BFAR) for the promotion of proper and sustainable fish

production. With the increasing interests in fish production, parasitic infestations are becoming

threats for fish health management. Thus, the outcome of this study could also be a basis of

future researchers in this species of fish.

Objectives of the Study

The main objectives of the study will be to identify the parasitic nematodes infecting

mackerels (Scomber spp.) bought at the Dalahican Fish Port Complex, Lucena City, Quezon.

Specifically, the study aims to:

a.) identify at the genus level (if possible up to species level) the parasitic nematodes

infecting the mackerels bought at the Dalahican Fish Port Complex, Lucena City,

Quezon, and;
b.) correlate the prevalence and intensity of the parasitic nematode with the size of the

fish.

Scope and Limitation of the Study

3
Parasites that live internally in the host are endoparasites, thus, it cannot be studied

without knowing the hosts in which they live (Roberts and Janovy, 2009). This study will focus

mainly on the identification, counting and grouping of Anisakis spp. in the intestine of mackerels

(Scomber spp.) bought at the Dalahican Fish Port Complex, Lucena City, Quezon. To assure that

the fishes to be bought at the Dalahican Fish Port Complex in Lucena City will be strictly caught

in Tayabas Bay, the fish samples will be collected by the fishermen residing nearby and assisted

by the local workers from BFAR in Quezon.

The fish samples will then be measured in millimeters (mm) for their total length from

the tip of the snout to the longest caudal ray and the wet weight to the nearest gram (g). The sex

of the fish (if possible) will also be recorded. A compound microscope will be used in the

identification of parasites that will be identified up to genera level (if possible, up to species

level).

Time and Place of the Study

The study will be conducted from July - August 2015. Mackerel samples will be bought

at the Dalahican Fish Port Complex in Lucena City. Five hundred fish samples will be dissected

and brought to the Freshwater Aquaculture Center, Central Luzon State University for the

examination of fish endoparasites (intestinal gut) for the prevalence and intensity rate of

infection.

4
REVIEW OF RELATED LITERATURE

Mackerel (Scomber spp.)

Mackerels inhabit the epipelagic waters, both inshore and offshore (Trinidad et al., 1993).

They are of moderate to large size and are characterized by their streamlined, spindle-shaped

bodies (Trinidad et al., 1993).

Four species of mackerel are caught in Philippine waters: Rastrelliger brachysoma, R.

kanagurta, R. faughni and Scomber australasicus (Dalzell et al., 1990). The authors mentioned

that the latter tends to be associated with subtropical and warm temperate waters Rastrelliger

brachysoma. Rastrelliger brachysoma is a coastal or inshore species subsisting principally on

microplankton while Rastrelliger kanagurta is an open sea species and feeds mostly on

macroplankton such as larval shrimps and fishes (Manacop, 1956). The growth parameter

estimates for R. kanagurta and R. brachysoma suggest that the life span of these mackerel

species is between 1.5 and 2 years (Ingles and Pauly, 1984; Dalzell and Ganaden, 1987).

The front and hind margins of the eyes of Scomber spp. are covered by an adipose eyelid

(Collette, 1986 as cited by Castro Fernandez and Santana Ortega, 2000). It is a primarily coastal

species, found from the surface down to 300 m depth (Collete and Nauen, 1983). The commonly

used fishing gears to catch mackerels are the purse seines and the pelagic pair trawls (Collette

and Nauen, 1983; Cochrane, 2002). They are marketed fresh, frozen, canned, smoked and salted

(Collette and Nauen, 1983).

Currently, the genus Scomber (Teleostei: Scombridae) comprises only 4 valid species:

Scomber australasicus (Blue mackerel), Scomber colias (Atlantic Chub mackerel), Scomber

japonicus (Chub mackerel) and Scomber scombrus (Atlantic mackerel) (Froese and Pauly, 2011).

5
The chub mackerel, Scomber japonicus, also known as the Pacific mackerel or Pacific

chub mackerel, is another species which closely resembles the Atlantic chub mackerel

(http://en.wikipedia.org/). It is also a temperate-water species, but generally in warmer areas than

S. scombrus (Matsui, 1967 as cited by Al-Zubaidy, 2010). Moreover, populations of S. japonicus

from the Pacific, Western Atlantic and Eastern Atlantic, show recognizable differences in their

morphological characteristics below the species level (Matsui, 1967 as cited by Al-Zubaidy,

2010).

Figure 1 shows the external morphology of Scomber japonicus. It has an elongated and

rounded body, pointed snout, and slim caudal peduncle (Collete and Nauen, 1983). The head is

small and the lower jaw slightly prominent (Collete and Nauen, 1983). The mouth is wide and

the teeth of the adult are thin, thinner on the vomer, conical projections situated in a single line

on each of the premaxillaries and mandibles (Collete and Nauen, 1983).

Atlantic chub mackerel, Scomber colias (Figure 2), is a coastal pelagic fish species,

occurring at depths of 250-300 meters and shows schooling and migratory behaviors (Collette

and Nauen, 1983; Collette, 1986 as cited by Castro Fernandez and Santana Ortega, 2000). This

6
species plays a key role in the food web of the Atlantic Ocean ecosystems, being an essential

element of the diet of larger pelagic fishes and mammals (Zardoya et al., 2004).

Figure 2.
Atlantic
chub
mackerel,
Scomber
colias
(Source:
Collette,
1986 as
cited by
Castro
Fernandez
and
Santana Ortega, 2000).

Atlantic mackerel, Scomber scombrus (Figure 3) is a fast swimming pelagic schooling

species abundant in temperate waters of the North Atlantic Ocean, and it is an economically

important species in this area (Matsui, 1967 as cited by Al-Zubaidy, 2010). Just like S. colias, S.

scombrus, is a coastal pelagic fish species, but occurring in lower depths, ranging from 200 to

250 meters (Collette and Nauen, 1983). This species also show schooling and migratory

behaviors (Collette, 1986 as cited by Castro Fernandez and Santana Ortega, 2000). Regarding

the diet of Scomber scombrus, they feed mainly on pelagic crustaceans including crab larvae,

amphipods and young fishes (Collette, 1986 as cited by Castro Fernandez and Santana Ortega,

2000; Zardoya et al., 2004).

7
Figure 3. Atlantic mackerel, Scomber scombrus (Source: Collette, 1986 as cited by Castro
Fernandez and Santana Ortega, 2000).

Concerning the morphological characteristics of S. colias, it shows 9 or 10 spines in the

first dorsal fin with the space between the first and the second dorsal fin is approximately equal

to the length of the first dorsal fin, swim bladder is present and the belly is clearly marked with

spotting (Collette and Nauen, 1983; Collette, 1986 as cited by Castro Fernandez and Santana

Ortega, 2000).

Scomber australasicus is found in waters of the Southeast Pacific Ocean, Australia and

Tasmania and it is frequent in Hawaii and in the eastern Pacific Ocean near Mexico (Matsui,

1967 as cited by Al-Zubaidy, 2010). According to Baker and Collette (1998), it is also present in

the Red Sea and in the northern Indian Ocean (Gulf of Aden and Oman).

The morphology of both Atlantic mackerels is very similar, so that they can be easily

misidentified at the landing auction (Collette and Nauen, 1983). In accordance to the

morphological descriptions of Collette and Nauen (1983) and the species identification key of

(Collette 1986 as cited by Castro Fernandez and Santana Ortega, 2000), a number of

characteristics, including, the number of spines in the first dorsal fin and the belly pigmentation,

are needed to carefully observe to efficiently differentiate between both atlantic mackerels.

Although the size of the eyes was not considered in the key characteristics, the empirical

8
knowledge of the fishermen suggests that the size of the eyes can be useful in specimens’

identification to the species level (Erguden et al., 2009).

Fish Parasitism

Parasitism is a symbiotic relationship between two organisms in which the parasite,

depends on the host, and either harms or lives on the host (Rohde, 2005). Parasites may cause

mechanical injury, such as boring a hole into the host or digging into its skin or other tissues,

stimulate a damaging inflammatory or immune response (Rohde, 2005). Most parasites inflict a

combination of these conditions on their hosts (Taliaferro, 2009). This relationship also plays a

significant role in fish biology and ecology (Hudson et al., 2006; Luque and Poulin, 2008). Also,

parasite infections on fish are a usual ecological event because parasites are natural component

of the aquatic environment and fish serves as important part of their life cycle (Barber and

Poulin, 2002).

The parasitism and diseases are important factors affecting the viability of natural

populations and communities (Morand and Arias-Gonzalez, 1997). In the marine environment, it

has been demonstrated that individual fish may suffer from parasitic attacks (Sasal et al., 1996).

The authors have shown the conspicuous role of parasites on fish in marine reserves.

According to Alves and Luque (2001), the feeding habits and the wide diet spectrum of

fishes puts them into contact with several potential intermediate hosts of parasites. This might be

increasing the presence of endoparasites in these fishes (Alves and Luque, 2001). The diet of the

host species is the main factor affecting to the parasite community structure, especially for the

trematodes, acanthocephalans and nematodes transmitted to their host through a predator-prey

relationship (Sasal et al., 1999). Parasite species might accumulate along food chain (Aho and

Bush, 1993).

9
Endoparasite

Endoparasites are parasites that are located within the flesh and cavities of the host

organism (Roberts and Janovy, 2005). These parasites can be found within the muscles, organs,

and membrane linings of the cavities of the host organism (Hoffman, 1998). The increased

potential for infecting humans with a fish parasite is more common for endoparasites since

tapeworms and roundworms can be passed to humans who eat undercooked or raw meat

(Hoffman, 1998).

Scomber japonicus showed a parasite community with dominance by endoparasites

(Alves et al., 2003). Dominance of endoparasites has been recorded in other fishes from Rio de

Janeiro (Silva et al., 2000; Alves, 2002; Luque, 2001), and this situation would be related with

the feeding behavior of S. japonicus which have a diet composed by fishes, euphausiids and

cephalopods. The presence of larval stages of cestodes, acanthocephalans and nematodes suggest

that S. japonicus might be occupying an intermediate trophic level at the marine food web

(Zavala-Camin, 1982; Seckendorff, 1985). For instance, Navone et al. (1998) described the life

c1ycle of Hysterothylacium aduncum and suggested that S. japonicus is an intermediate and

definitive host of this nematode.

Nematodes

Parasites transferred by marine fish to human by consumption of poorly cooked infected

fish are found rarely among the acanthocephalans (Bolbosoma sp.), occasionally among the

digeneans (Diplogonoporus spp.) and more frequently among the nematodes (Petersen et al.,

1993). Larval stages of Anisakid nematodes (super family: Ascaridioidea, Family: Anisakidae) of

some genera such as Anisakis; Contracaecum; Pseudoterranova; and Hysterothylacium are

commonly found in the viscera and musculature of many species of teleost fish (Costa et al.,

10
2003), since they are swallowed when fish eat their prey, which are the intermediate hosts of

these worms that are encapsulated in viscera or muscles (Smith, 1983; Mattiucci et al., 1997) and

can infect humans causing significant clinical disease (i.e. anisakiasis) in a number of countries

(Zhou et al., 2008).

Parasites of Scomber spp.

Some of the parasites of Scomber spp. include worms, coccidia, and blood parasites

(http//www.dictionary.com). Parasite is an organism that lives in or on another organism (its

host) and benefits by deriving nutrients at the host's expense (http://www.cdc.gov/parasites/)

According to Yeh (2002), it is different from predators and parasitoids (which also derive

benefits from certain interspecific interactions while harming the other participant) in that the

host of a parasite is not necessarily killed instead it only derives benefits from their host. Though,

it also often causes important disease to animals and humans which may cause death to its host

(Bogitsh et al., 2005).

During a survey of parasites of the chub mackerel, a camallanid nematode provisionally

assigned to the genus Oncophora was found (Nematoda, Camallanidae) (Oliva et al., 2008).

Camallanid nematodes are gastrointestinal parasites of fishes and other aquatic vertebrates

(Rigby, 1999).

Table 1 shows the helminth parasites which include digenetic trematodes (flukes),

cestodes (tapeworms), nematodes (roundworms), and acanthocephalans (spiny headed worms)

were reported in Scomber spp. (Bell and Burt, 1991). However, a comparison of the helminth

composition of this fish species showed differences in intensity and prevalence of the parasites

(Oliva et al., 2008). Investigations on the parasites of Atlantic chub mackerel, in particular

11
anisakid nematodes and monogeneans, have already highlighted interesting differences in both

prevalence and abundance data (Costa et al., 2003).

12
Table 1. Helminthic parasites reported in Scomber species (Source: Collette, 1986 as cited by Castro Fernandez and Santana Ortega,
2000).

Host Parasites Species References


Scomber japonicus Trematodes
Tergestia lati collis Florida Silas (1967)
T. acanthocephalan Silas (1967)
Nematobothniutn sp. Diaz-Ocamp (1991); Cremonte and Sardella (1997)
Aphallus tubaium Silas (1967)
Lepocnadiuin retrusum Silas (1967)
L. inisakiense sp. Shimazu (1986)
Opechona olssoni Silas (1967); Shimazu (1986)
O. onientalis Silas (1967)
O. bacillanis Silas (1967)
O. scombni Silas (1967); Shimazu (1989)
Opechona spp. Cremonte and Sardella (1997)
Dinurus scornbni Silas (1967)
Ectenurus Lepidus Silas (1967)
Lecithocladium excisum Silas (1967); Belyaev and Ryabov (1987)
L. gulosum Silas (1967)

Cestodes
Hepatoxylon trichiuni Wysokinski et al. (1987)
Scolex pleuronectis Cremonte and Sardella (1997)

Acanthocephalans
Corynosoma austral Cremonte and Sardella (1997)
Acantocephalus Atli (1960)

Nematodes
Anisakis spp. Wysokinski et al. (1987); Belyaev and Rayabov (1987); Sizheng et al. (1993);
Cremonte and Sardell (1997)

13
A. simplex sensu stricto Quiazon et al. (2011)
A. pegreffii Quiazon et al. (2011)
Thynnascaris Sakaguchi et al. (1980)
Histerothylacium spp. Cremonte and Sardella (1997)
Contnacaecum spp. Cremonte and Sardella (1997)

Scomber colias Monogeneans


Grubea cochlear Rohde (1986)
Kuhnia scombri Sproston (1945)
Pseudokuhnia minor Rohde and Watson (1985)
Kuhnia scombercolias
K. sprostonae
K. abarica Nasir and Fuentes-Zambrano (1983)

Digeneans
Prodistomum orientalis Layman (1930)

Nematodes
Anisakis pegreffii Campana-Rouget and Biocca (1955)
A. nascettii Mattiucci et al. (2009)
Pseudoterranova ceticola Deardorff and Overstreet (1981)

Copepod
Clavellisa scombri Cressey and Cressey (1980); Somdal and Schram (1992); Alves et al. (2003);
Öktenerand Trilles (2009)

Acanthocephalan
Rhadinorhynchus pristis Navone et al. (1998); Rudolphi (1802)

Scomber scrombus Monogeneans


Grubea cochlear Rohde (1989)

14
Kuhnia scombri Rohde (1989)
Kuhnia sprostonae Rohde (1989)

Copepodes
Caligus pelamydis Cressey and Cressey (1980); Somdal and Schram (1992); Alves et al. (2003);
Öktenerand Trilles (2009)
Clavellisa scombri Cressey and Cressey (1980); Somdal and Schram (1992); Alves et al. (2003);
Öktenerand Trilles (2009)

15
Anisakis spp.

The genus Anisakis (Dujardin, 1845) (Family Anisakidae) nematodes are parasites of the

alimentary tract of aquatic vertebrates with worldwide distribution (Mattiucci and Nascetti,

2008) (Figure 4). These parasites can be also found in cephalopods and act as paratenic or

transport hosts (Eissa, 2002; Choi et al., 2011; Tantanasi et al., 2012). According to Yoon et al.

(2008), Scomber japonicus feeds on planktonic crustaceans, particularly euphausiids and small

fish such as anchovy (Engraulis japonicus). Many of these prey items are known as intermediate

hosts of anisakid nematodes (Hays et al., 1998; Rello et al., 2009), and several studies have

shown that mackerel (Scomber spp.) in different areas are infected with diverse species of

anisakid nematodes (Abattouy et al., 2011; Shukhgalter, 2004; Suzuki et al., 2010; Quiazon et

al., 2011).

The life cycle of these parasites involve various hosts at different levels in food webs

(Mattiucci and Nascetti, 2008). According to Audicana and Kennedy (2008), commercially

important species which serves as hosts of Anisakis spp. include herring (Clupea spp.), cod

(Gadus spp.), salmon (Oncorhynchus spp), mackerel (Scomber spp.) and anchovy (Engraulis

spp.). The infective third stage larvae (L3) of Anisakis are common in commercially important

marine fishes and its presence is of great concern for both public health and economic reasons

(Choi et al., 2011; Tantanasi et al., 2012). The infective larval stage of Anisakis simplex is the

most important etiologic agent of anisakidosis in humans (Choi et al., 2011).

15
Figure 4. Anisakis spp.

Parasites as Biological Indicators

Parasites have been successfully used as tools to understand several aspects of their hosts’

biology, namely; identify and discriminate fish stocks (Timi, 2007; Santos et al., 2009), study

population structures (Pozdnyakov and Vasilenko, 1994) and clarify taxonomic relations (Luque

and Poulin, 2008; Oliva et al., 2008). The use of parasites with these purposes is based on the

fact that the host can only become infected with a particular parasite species within the endemic

area of that parasite (MacKenzie and Abaunza, 1998). However, not all parasites can be useful

as biological indicators. In order to be a good one, there are certain criteria that should be met

according to MacKenzie and Abaunza (1998) and Rohde (2005) and these are: (a) the parasite

should have significantly different levels of infection in different parts of the study area.

16
Prevalence, abundance and infection data, as defined by Bush et al. (1997), should be used

(MacKenzie and Abaunza, 1998); (b) the parasite should have a long life span in the target host,

at least long enough to cover the time scale of the investigation (Williams et al., 1992); (c)

parasites with direct single-host life cycles are easier to use as tags, but those with two or more

hosts can be useful, since there is information on biotic and abiotic factors influencing parasites

transmission (MacKenzie and Abaunza, 1998; Rohde, 2005); (d) the parasite should have

constant levels of infection from year to year (Rohde, 2005); (e) the parasite should be easily

detected and identified, and the examination of the host should involve the minimum of

dissection (MacKenzie and Abaunza, 1998; Rohde, 2005); (f) the parasite should not cause high

pathogenicity in the host nor changes in host behavior (Williams et al., 1992, MacKenzie and

Abaunza, 1998).

Several authors have consistently highlighted the utility of parasitological surveys in

understanding and differentiating fish populations, and have successfully demonstrated that

indeed parasites are good biological indicators or fish populations (MacKenzie, 2002;

Hemmingsen et al., 1991; George-Nascimento and Arancibia, 1992; Williams et al., 1992;

Santos et al., 2009).

Biological indicators for fish stock assessments

One of the major goals from the last decade in the study of the parasite fauna of aquatic

organisms has been, among the others, the assessment of fish stocks, their movement, and

recruitment (Quiazon, 2015). Nowadays, the modern concept of “fish stock” integrates all the

information gathered from a broad spectrum of techniques, ranging from morphology

(morphometrics, meristic, otolith microchemistry) to biology (life-history characteristics, mark-

17
recapture, and parasites) and genetic structure (allozymes, microsatellites, DNA sequences) of

fish host throughout their geographical range (Quiazon, 2015).

A parasite can be used as suitable biological tag for fish stock identification when its

geographical distribution and life-cycle are known, and when the parasite’s residence time in the

host is long enough compared to the life span of the fish host (Quiazon, 2015). In this sense, the

parasite as biological indicator reflects the geographic origin of the fish population on a spatial

scale (Quiazon, 2015). Indeed, the genetic/molecular markers define the stock on the

evolutionary temporal scale, while the parasite taxa characterize the stock on a

spatial/geographical scale (Mattiucci et al., in press).

Anisakid nematode (Anisakis) for stock assessment

Infection by Anisakids can affect the commercial value of fish, particularly when larvae

are located in the musculature and thus represent some economical loss for the fisheries industry

(Angot and Brasseur, 1995 as cited by Al-Zubaidy, 2010). The worms in flesh reduce the market

value of fish, and thus represent some economical loss of the fisheries industry (Angot and

Brasseur, 1995 as cited by Al-Zubaidy, 2010). In addition, nematode genera Anisakis, Terranova,

and Contracaecum spp. found in fish may cause the most severe problems for human health,

Anisakiasis, that humans acquire by eating fish subject to little heat treatment or fish that is

smoked, soaked in vinegar, pickled with spices and other raw fish specialities (Petersen et al.,

1993; Beran and Steel, 1994).

The fish inhabiting nematode stages show a remarkable resistance to low temperature,

but are destroyed readily by heating to 70C° or freezing at -20C° for more than 24 hours (Moller,

1991). The time to kill the nematodes by marinating depends on the degree of acidity,

18
temperature and salt addition (Moller, 1991). It produces severe lesions in human stomach and is

associated with gastric neoplasia (Mattiucci et al., 1997). If larvae are loose or attached to

digestive tract, they may produce irritation, inflammation and ulceration (Mattiucci et al., 1997).

Anisakid parasites are an integral part of aquatic ecosystems as they play key roles in

population dynamics and community structure and can provide important information about the

general biodiversity of the ecosystem (Quiazon, 2015). Recent data on the possible use of

anisakid nematodes have been presented as biological indicators of: a) the definition of fish

stocks within a multidisciplinary approach, b) integrity and stability of trophic webs, and c)

habitat disturbance (Mattiucci et al., 2008). Among the parasite species that have been used in

fish stock definition is the larval anisakid nematodes of the genus Anisakis which represent one

of the best biological indicators (MacKenzie, 2002).

19
MATERIALS AND METHODS

Fish samples

Some BFAR personnels in Quezon will assure that the mackerel (Scomber spp.) will be

randomly collected from Tayabas Bay and then five hundred of fish samples will be bought from

fishermen at the Dalahican Fish Port Complex in Dalahican, Quezon.

Description of the Dalahican Fish Port Complex

One of the important fish landing sites in Quezon province is in Dalahican, a small town

located at the northwestern part of Tayabas Bay (Figure 5). The Dalahican Fish Port Complex

located in Dalahican was built along the fishing village of Brgy. Talao-Talao

(http://www.pdosoluz.com.ph/port-of-lucena-updated.html) which is one kilometer away to the

east of Dalahican Fish Port Complex (http://www.ppa.com.ph/batangas/about_lucena.html). The

Dalahican Fish Port Complex is equipped with an ice plant capable of producing 10 tons of ice

(Trinidad et al., 1993).

Figure 5. The map of Tayabas Bay (Source: Google Earth, 2015)

20
Dalahican, Lucena City, Quezon is about 5 km from the city proper of Lucena. The

Dalahican Fish Port Complex (Figure 6) is the fourth fish port complex managed and operated

by the Philippine Fisheries Development Authority (PFDA) (http://en.wikipedia.org).

The strategic location of the Dalahican Fish Port Complex and its proximity to some of

the major fishing grounds in the Philippines such the Tayabas Bay, Ragay Gulf and other fishing

grounds contiguous to the southern Tagalog region, have made the port a major fish landing

center of the province (http://en.wikipedia.org).

The bulk of pelagic catch landed at Dalahican consists of anchovies and roundscads

(Trinidad et al., 1993). They added that other species which are landed although in minor

quantities includes sardines and mackerels. According to Trinidad et al. (1993), fish landing and

trading usually start at 4:00 a.m. and last for four to five hours and where the selling of fish is

usually carried out by brokers who are stationed in the area through whisper bidding. Moreover,

brokers who sell fish in behalf of fish producers get a commission in the gross sales (Trinidad et

al., 1993). Aside from their marketing function, these brokers also provide capital to fishers

particularly those who are engaged in municipal fishing (Trinidad et al., 1993). Dalahican

basically supplies the fish needs of its residents and that of the nearby towns and a significant

proportion of the catch is also brought to Manila (Trinidad et al., 1993).

21
Figure 6. Dalahican Fish Port Complex

Dissection of fish samples

The total length of each fish sample will be measured before dissection. The fish samples

after collection will be immediately documented via digital images. All fish samples will be

stored in an ice box prior to travel to FAC, CLSU, Nueva Ecija for dissection and identification

of parasites. Fish samples will be dissected in the laboratory. Ecological parameters such as

prevalence (percentage of infested hosts in a sample), abundance and mean intensity (mean

number of parasites per infected host) in accordance to various criteria will be estimated

following the formula proposed and recommended by Margolis et al. (1982) and Bush et al.

(1997).

Identification of parasites will be based on total mounts in glycerine (Nematoda) or

benzyl alcohol (other parasites) (Zdzitowiecki, 1991; 1997; Rocka, 2003; 2004).

22
Internal examination

The body surface of the fish samples will be disinfected with 70% alcohol and then the

body cavity will be opened using either sterile scissors or a scalpel flamed in alcohol. An incision

will be made above the pectoral fin and will be cut along the swim bladder to the vent. The body

wall may be held back or completely removed. Thorough care will be exercised when cutting in

order not to damage or rupture any internal organs.

After opening the fish, the viscera will be removed by cutting the esophagus at the

anterior end and the intestine at the vent. The small intestines will be placed in a petri dish with

saline solution and will be placed in vials with glycerin. Parasites or abnormal tissue will be

placed on a microscope slide and will be examined more closely under the low power objective

then, under the high power objective.

Morphological identification groups of Anisakis spp.

Berland (1961) stated that Anisakis spp. could only be categorized morphologically

into Anisakis type I and type II, in which the former has a longer ventriculus and a mucron, while

the latter has short ventriculus and no mucron.

Taxonomic keys for nematodes will be used to confirm the initial morphological

classification, as well as to determine the larval stages of Anisakis spp. Recent studies showed

that molecular diagnostic techniques could be used to identify Anisakis to a species level (Abe et

al., 2006). PCR-RFLP has been widely used to identify Anisakis spp. in different fish species

(Abe et al., 2006; Pontes et al., 2005; Quiazon et al., 2009; Setyobudi et al., 2011; Umehara et

al., 2010). Thus, this study will be focuses only on the morphological identification groups of

Anisakis spp.

23
Molecularly, the previous Anisakis type I is known to consist of 6 species (A.

ziphidarum, A. nascettii, A. typica, and 3 sibling species of A. simplex complex, namely A.

simplex (sensu stricto) (s.s.), A. pegreffii, and A. simplex C, whereas type II consists of 3 species

(A. paggiae, A. brevispiculata, and A. physeteris) (Mattiucci et al., 2008; Mattiucci et al., 2009).

Recent studies in Japan showed that L3, L4, and adult of A. simplex (s.s), belong to type I and A.

pegreffii, classified as type II could be distinguished morphologically based on the ventriculus

length, in which the former has a longer (0.90-1.50 mm) ventriculus than the latter (0.50-0.78

mm) (Quiazon et al., 2008).

Prevalence of parasites

Pearson’s correlation coefficient r will be used as an indication of the relationship

between the host‘s total body length and the prevalence of parasites, with previous arcsine

transformation of the prevalence data (Zar, 1996). Spearman’s rank correlation coefficient r will

be calculated to determine possible correlations between the host’s total body length and

abundance of parasites. The possible influence of host sex on abundance and prevalence of

parasites will be tested using the Z normal approximation to the Mann-Whitney test and the Chi-

square test, respectively.

A higher prevalence of Anisakid nematode infestation depends on the availability of the

final hosts in the region and the parasites’ ability to complete its life cycle (Palm, 1999). It also

may be related to the food ingested and to the layer of the water column inhabited (bottom versus

pelagic) (Palm et al., 2007). The infestation dynamic is strongly fish species and area specific

(Rokicki et al., 2009). The high loads of Anisakis found in fish host, and the fact that Anisakid

24
larvae were seen penetrating muscles, may point to a possible health problem for consumers

(Costa et al., 2003).

Statistical analysis

The prevalence and mean intensity of parasites present in Scomber spp. will be calculated

using the following formula proposed by Margolis et al. (1982) as follows:

Prevalence = Number of infected fish X 100


Total fish examined

Intensity = Number of parasites


Infected Fish

Correlation

Prevalence Intensity vs. Weight

Prevalence Intensity vs. Length

25
LITERATURE CITED

Abattouy, N., A. Valero, M.H. Benajiba, J. Lozano and J. Martin-Sanchez. 2011. Anisakis
simplex s.l. parasitization in mackerel (Scomber japonicus) caught in the north of
Morocco- prevalence and analysis of risk factors. Int. J. Food Microbiol., 150: 136–139.

Abe, N., K. Tominaga and I. Kimata. 2006. Usefulness of PCR-restriction fragment length
polymorphism analysis of the internal transcribed spacer region of rDNA for
identification of Anisakis simplex complex. Japan J. Infec. Dis., 59: 60–62.
Adams, A.M. and K.D. Murrell and J.H. Cross. 1997. Parasites of fish and risks to public
health. Rev. Sci. Tech. Off. Int. Epiz., 16 (2): 652-660.

Aho, J.M. and A.O. Bush. 1993. Community richness in parasites of some freshwater fishes
from North America. p. 185–193. In: Ricklefs, R.E. and Schluter, D. (eds.). Species
Diversity in Ecological Communities: Historical and Geographical Perspectives,
University of Chicago Press. 414 p.

Aloo, P.A., R.O. Anam and J.N. Mwang. 2004. Metazoan parasites of some commercially
important fish along the Kenyan Coast. Western Indian Ocean Journal of Marine Science.
3(1): 71-78.

Alves, D.R., Luque, J.L. and A.R. Paraguassú. 2002. Community ecology of the metazoan
parasites of pink cusk-eel, Genypterus brasiliensis (Osteichthyes: Ophidiidae), from the
coastal zone of the state of Rio de Janeiro, Brazil. Retrieved from
http://www.ncbi.nlm.nih.gov/pubmed/12219136 on February 21, 2015.

Alves, D.R., Luque, J.L. 2001. Community ecology of the metazoan parasites of the white
croaker Micropogoniasfurnieri (Osteichthyes: Sciaenidae) from the coastal zone of the
State of Rio de Janeiro, Brazil. Retrieved from
http://www.ncbi.nlm.nih.gov/pubmed/11285488 on February 21, 2015.

Alves, D. R., J.L. Luque, V.D. Abdallah. 2003. Metazoan parasites of chub mackerel, Scomber
japonicas (Osteichthyes: Scombridae), from the coastal zone of the State of Rio de
Janeiro, Brazil. Rev. Bras. Parasitol. Vet., 12(4): 164-170.

Atli, M. 1960. Further information on the biology of Scomber japonicus (Gmelin). Retrieved
from www.fao.org/docrep/017/x4287e/x4287e.pdf on February 28, 2015.

Al-Zubaidy, A.B. 2010. Third-stage larvae of Anisakis simplex (Rudolphi, 1809) in the Red Sea
fishes, Yemen Coast. Journal of King Abdulaziz University Marine Sciences, 21(1): 95-
112.

26
Audicana, M.T. and M.W. Kennedy. 2008. Anisakis simplex: from obscure infectious worm to
inducer of immune hypersensitivity. Clin. Microbiol. Rev., 21: 360–379.

Baker, E.A. and B.B. Collette. 1998. Mackerel from the northern Indian Ocean and the Red Sea
are Scomber australasicus, not Scomber japonicus. Ichthyol. Res., 45(1):29-33.

Barber, I. and R. Poulin. 2002. Interactions between fish, parasites and disease. Volume 1. Fish
Biology. p. 359 – 389. In: Hart, P.J.B. and J.D. Reynolds (eds.). Handbook of fish
biology and Fisheries. Blackwell Publishing Ltd. Oxford, UK. 413 p.

Baylis, H.A. 1923. Report on a collection of parasitic nematodes mainly from Egypt. Part I.
Ascaridae and Heterakidae. Part II. Oxyuridae Part III. Camallanidae etc., with a note on
prostmayria and an appendix on Acanthocephala. Retrieved from
http://journals.cambridge.org/action/displayAbstract?
fromPage=online&aid=1671364&fileId=S0031182000014451 on February 7, 2015.

Begg, G.A. and J.R. Waldman. 1999. A holistic approach to fish stock identification. Fisheries
Res., 43: 35-44.

Bell, G. and A. Burt. 1991. The comparative biology of parasite species diversity: internal
helminths of freshwater fish. Journal of Animal Ecology, 60: 1047-1063.

Belyaev, V.A. and V.S. Ryabov. 1987. Population structure of chub mackerel, Scomber
japonicus, in the northwestern Pacific Ocean. J. Ichthyol., 27: 73-79.

Beran, G.W. and J.H. Steel. 1994. CRC. Handbook Series in Zoonoses. CRC Press. England.
608 p.

Berland, B. 1961. Nematodes from some Norwegian marine fishes. Sarsia, 2:1–50.

Bogitsh, B.J., C.E. Carter and T.N. Oeltmann. 2005. Human Parasitology, 3rd edition. Elsevier,
Oxford, U.K. p. 1-3.

Bray, R.A. and D.I. Gibson. 1997. The Lepocreadiidae Odhner, 1905 (Digenea) of fishes from
the north-east Atlantic: summary paper, with keys and checklists. Systematic
Parasitology, 36(3): 223-228.

Bush, A.O., J.M. Aho and C.R. Kennedy. 1990. Ecological versus phylogenetic determinants of
helminth parasite community richness. Evolutionary Ecology, 4: 1-20.

Bush, A.O., K.D. Lafferty, J.M. Lotz and A.W. Shostak. 1997. Parasitology meets ecology on
its own terms: Margolis et al revisited. Journal of Parasitology, 83: 575-583.

Castro Hernandez, J.J. and A.T. Santana Ortega. 2000. Synopsis of biological data on the chub
mackerel (Scomber japonicus Houttuyn, 1782). FAO Fisheries Synopsis No. 157. Rome,
Italy. 77 p.

27
Choi Seon, H., K. Jung, J. Jin Ok, C. Min Kyung, Y. Hak Sun, C. Hee Jae and O. Mee Sun.
2011. Anisakis simplex larvae: infection status in marine fish and cephalopods purchased
from the Cooperative Fish Market in Busan, Korea. Korean J. Parasitol., 49(1): 39–44.

Cochrane, K.L. 2002. A fishery manager's guidebook. Management measures and their
application. The Food and Agriculture Organization of the United Nations and Wiley-
Blackwell. Food and Agriculture Organization. Rome, Italy. 231 p.

Collete, B. and E. Nauen. 1983. FAO species catalogue. Vol. 2. Scombrids of the world. An
annotated and illustrated catalogue of tunas, mackerels, bonitos and related species
known to date. FAO Fish. Synopsis No. 125. 137 p.

Coombs, S.H., D. Morgans and N.C. Halliday. 2001. Seasonal and ontogenetic changes in the
vertical distribution of eggs and larvae of mackerel (Scomber scombrus L.) and horse
mackerel (Trachurus trachurus L.). Fish. Res., 50(1–2): 27–40.

Costa, G., N. Freitas, T.H. Dellinger and K. MacKenzie. 2007. Gill monogeneans of the chub
mackerel, Scomber japonicus from Madeiran waters of the Atlantic Ocean, Portugal.
Journal of Helminthology, 81: 33-38.

Costa, G., Pontes, T., Mattiucci, S. and Amelio, S.D. 2003. The occurrence and infection
dynamics of anisakis larvae in the black-scabbard fish, Aphanopus carbo, chub
mackerel, Scomber japonicas, and Oceanic horse mackerel, Trachurus picturatus from
Adeira, Portugal. Journal of Helminthology, 77: 163-166.

Cressey, R.F. and H.B. Cressey. 1980. Parasitic copepods of mackerel- and tuna-like fishes
(Scombridae) of the world. Smithsonian Institution Press. Washington, USA. 311 p.

Cremonte, F. and N.H. Sardella. 1997. The parasite fauna of Scomber japonicus, Houttuyn 1782
(Pisces: Scombridae) in two zones of the Argentine Sea. Fish. Res., 31(1-2): 1-9.

Dalzell, P. and D. Pauly. 1990. Assessment of the fish resources of Southeast Asia, with emphasis
on the Banda and Arafura Seas. Neth. J. Sea Res., 25(4): 641-650.

Davey, J.T. 1971. A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridata).
Journal of Helminthology, 25: 51-72.

Díaz-Ocampo, M.A. 1991. Efectos de la parasitosis interna de ovarios en la caballa Scomber


japonicus peruanus Jordan y Hubbs 1925 sobre aspectos reproductivos en el periodo de
maximo desove de verano (1989-1990). Mem. de Tesis de Licenciatura en Biología
Pesquera. Universidad Arturo Prat, Iquique, Chile. Retrieved from
http://www.fao.org/docrep/017/x4287e/x4287e.pdf on February 22, 2015.

Duffy, J.M. and M.E. Hay. 2001. The ecology and evolution of marine consumer prey
interaction. p. 131-157. In: M.D. Bertness, S.D. Gaines and M.E. Hay (eds.). Marine

28
community ecology. Retrieved from
http://www.vims.edu/research/units/labgroups/marine_biodiversity/publications/_pdf/Duf
fy_Hay_2001_book_chapter.pdf on June 8, 2015.

Erguden, D., B. Oeztuerk, Z.A. Erdogan and C. Turan. 2009. Morphologic structuring between
populations of chub mackerel Scomber japonicus in the Black, Marmara, Egean, and
Northeastern Mediterranean Seas. Fisheries Science, 75: 129-135.

Faliex, E. and S. Morand. 1994. Population dynamics of the metacercarial stage of the
bucephalid trematode, Labatrema minimus (Stossich, 1887) from Salses-Leucate Lagoon
(France) during the cercarial shedding period. J. Helminthol., 68: 35-40.

Froese, R. and D. Pauly (eds.). 2011. Fish Base. World Wide Web electronic publication.
Retrieved from www.fishbase.org on February 7, 2015.

Garnick, E. and L. Margolis. 1990. Influence of four species of helminth parasites on


orientation of seaward migrating sockeye salmon (Onchorhynchus nerka) smolts.
Canadian Journal of Fisheries and Aquatic Science, 47: 2380–2389.

George-Nascimento M., Arancibia H. 1992. Stocks ecológicos del jurel (Trachurus symmetricus
murphyi Nichols) en três zonas de pesca frente a Chile, detectados mediante comparación
de su fauna parasitaria e morfometria. Revista Chilena Historia Natural, 65, 453–470.
(With English abstract).

Gibson, D.I., A. Jones and R.A. Bray. 2002. Keys to the Trematoda. Vol. 1. CABI Publishing,
Wallingford, U.K. 521 p.

Hemmingsen, W., I. Lombardo and K. MacKenzie. 1991. Parasites as biological tags for cod,
Gadus morhua in northern Norway: a pilot study. Fisheries Research, 12: 365–373.

Hoffman, G.L. 1998. Parasites of North American Freshwater Fishes. Second edition Cornell
University Press. Ithaca, New York, USA. 70:821-838.

Houttuyn, M. 1782. Beschrijving van eenige Japansche visschen, en andere zeeschepselen.


Retrieved from http://www.fao.org/docrep/017/x4287e/x4287e.pdf on November 17,
2014.

Hays, R., Measures, L.N., Hout, J., 1998. Euphausiids as intermediate hosts of Anisakis simplex
in the St. Lawrence estuary. Can. J. Zool. 76, 1226–1235.

Hudson, P.J., A.P. Dobson and K.D. Lafferty. 2006. Is a healthy ecosystem one that is rich in
parasites? Trends in Ecology and Evolution, 21(7): 381-385.

Ingles, J. and D. Pauly. 1984. An atlas of the growth, mortality and recruitment of Philippine
fishes. ICLARM Tech. Rep. 13. lnstitute of Fisheries Developnment and Research and
International Center for Living Aquatic Resources Management. 127 p.

29
Koyama, T., A. Kobayashi, M. Kumada, Y. Komiya, T. Oshima, N. Kagei, T. Ishii and M.
Machida. 1969. Morphological and taxonomical studies on Anisakidae larvae found in
marine fishes and squids. Japanese Journal of Parasitology, 18: 446- 487.

Lockwood, S.J., J.H. Nichols and W.A. Dawson. 1981. The estimation of a mackerel (Scomber
scombrus L.) spawning stock size by plankton survey. J. Plankton Res., 3: 217–233.

Ludwig, J.A. and J.F. Reynolds. 1988. Statistical Ecology: a primer on methods and computing.
Wiley-Interscience Publications. New York, USA. 337 p.

Luque, J.L. and D.R. Alves. 2001. Community ecology of metazoan parasites of the crevalle
jack, Caranx hippos (Linnaeus) and the horse-eye jack, Caranx latus Agassiz
(Osteichthyes, Carangidae) from the coastal zone of the State of Rio de Janeiro, Brazil.
Rev. Bras. Zool., 18: 399-410.

Luque, J.L. and R. Poulin. 2008. Linking ecology with parasite diversity in Neotropical fishes.
Journal of Fish Biology, 72: 189-204.

MacKenzie, K. 2002. Parasites as biological tags in population studies of marine organisms: an


update. Parasitology, 124: 153-163.

MacKenzie, K. and P. Abaunza. 1998. Parasites as biological tags for stock discrimination of
marine fish: a guide to procedures and methods. Fisheries Research, 38: 45-56.

Manacop, P.R. 1956. A preliminary systematic study of the Philippine chub mackerels, family
Scombridae, genera Pneumatophorus and Rastrelliger. Philippine J. Fish., 4(2): 79-101.

Margolis, L., W.G. Esch, J.M. Holmes, A.M. Kuris and G.A. Shad. 1982. The use of ecological
terms. J. Parasitol., 68: 131-133.

Mattiucci, S., R. Cimmaruta, P. Cipriani, P. Abaunza, and B. Bellisario. In press. Integrating


Anisakis spp. parasites data and host genetic structure in the frame of a holistic approach
for stock identification of selected Mediterranean Sea fish species. Retrieved from
http://journals.cambridge.org/action/displayAbstract?
fromPage=online&aid=9535094&fileId=S0031182014001103# on February 7, 2015.

Mattiucci, S., G. Nascetti, R. Cianchi, L. Paggi, P. Arduino, L. Margolis, J. Brattey, S.C. Webb,
S.D. Amelio, P. Orecchia and L. Bullini. 1997. Genetic and ecological data on the
Anisakis simplex complex with evidence for a new species (Nematoda, Ascaridoidea,
Anisakidae). J. Parasitol., 83: 401-416.

Mattiucci, S., P. Abaunza, S. Damiano, A. Garcia and M.N. Santos. 2007. Distribution of
anisakis larvae identified by genetic markers and their use for stock characterization of
demersal and pelagic fish from European waters: an update. J. Helminthol., 81: 117-127.

30
Mattiucci, S., V. Farina, N. Campbell, K. McKenzie and P. Ramos, 2008. Anisakis spp. larvae
(Nematode: Anisakidae) from Atlantic horse mackerel: their genetic identification and
use as biological tags for host stock characterization. Fisheries Science, 89: 146-151.

Mattiucci, S. and G. Nascetti. 2008. Advances and trends in the molecular systematics of
anisakid nematodes, with implications for their evolutionary ecology and host–parasite
co-evolutionary processes. Adv. Parasitol., 66: 49–148.

McKenzie, K., N. Campbell, S. Mattiucci, P. Ramos, A.L. Pintod and P. Abaunza, 2008. Parasites
as biological tags for stock identification of Atlantic horse mackerel Trachurus trachurus
L. Fisheries Research, 89(2): 136-145.

Moller, H. 1991. Prevention of human anisakiasis. Retrieved from


http://www.kau.edu.sa/Files/320/Researches/57309_27540.pdf on February 6, 2015.

Morand, S. and E.A. Gonzalez. 1997. Is parasitism a missing ingredient in model ecosystems.
Retrieved from Ecol Model. Mar. Ecol. Prog. Ser., 6: 52-61.

Murata, R., J. Suzuki, K. Sadamasu and A. Kai. 2011. Morphological and molecular
characterization of Anisakis larvae (Nematoda: Anisakidae) in Beryx splendens from
Japanese waters. Parasitol. Int., 60: 193–198.

Navone, G.T., N.H. Sardella and J.T. Timi. 1998. Larvae and adults of Hysterothylacium
aduncum (Rudolphi, 1802) (Nematoda: Anisakidae) in fishes and crustaceans in the
South West Atlantic. Parasite, 5(2): 127-136.

Oliva, M.E., I.M. Valdivia, G. Costa, N. Freitas, M.A. Pinheiro De Carvalho, L. Sánchez and J.
L. Luque. 2008. What can metazoan parasites reveal about the taxonomy of Scomber
japonicus Houttuyn in the coast of South America and Madeira Islands. Journal of Fish
Biology, 72: 545-554.

Palm, H. W. 1999. Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda:


Anisakidae) from Antarctic waters. Parasitology Research, 85: 638-646.

Palm, H.W., S. Klimpel and T. Walter. 2007. Demersal fish parasite fauna around the South
Shetland Islands: high species richness and low host specificity in deep Antarctic waters.
Polar Biology, 30: 1513-1522.

Petersen, F., H. Palm, H. Moller and M.A. Cuzi. 1993. Flesh parasites of fish from Central
Philippine waters. Diseases of Aquatic Organisms, 15: 81-86.

Pontes T., S. D'Amelio, G. Costa and L. Paggi. 2005. Molecular characterization of larval
anisakid nematodes from marine fishes of Madeira by a PCR-based approach, with
evidence for a new species. J. Parasitol., 91: 1430–1434.

31
Pozdnyakov, S.E. and A.V. Vasilenko. 1994. Distribution, migration, and the helminth fauna of
the Japanese mackerel, Scomber japonicus, in the northwestern Pacific Ocean. J.
Ichthyol., 34(4): 74-91.

Quiazon, K.M.A., T. Yoshinaga, K. Ogawa, and R. Yukami, 2008. Morphological differences


between larvae and in vitro-cultured adults of Anisakis simplex (sensu stricto) and
Anisakis pegreffii (Nematodes: Anisakidae). Parasitol. Int., 57(4): 483-489.

Quiazon, K.M.A., Y. Tomoyoshi and O. Kazuo. 2011. Experimental challenge of Anisakis


simplex sensu stricto and Anisakis pegreffii (Nematoda: Anisakidae) in rainbow trout and
olive flounder. Parasitology International, 60: 126-131.

Quiazon, K.M.A. 2015. Updates on aquatic parasites in fisheries: implications to food safety,
food security and environmental protection. J. Coast Zone Manag., 18:397

Rello, F.J., F.J. Adroher, R. Benítez and A. Valero, 2009. The fishing area as a possible indicator
of the infection by anisakids in anchovies (Engraulis encrasicolus) from southwestern
Europe. Int. J. Food Microbiol., 129: 277–281.

Roberts, L.S., and J. Janovy, Jr. 2005. Foundations of Parasitology. Seventh edition. McGraw-
Hill. New York, USA. 702 p.

Roberts, L.S., and J. Janovy, Jr. 2009. Foundations of Parasitology. Eighth edition. McGraw-
Hill, Dubuque, IA. 701 p.

Rocka, A. 2003. Cestodes of the Antarctic fishes. Polish Polar Research, 24: 261–276.

Rocka, A. 2004. Nematodes of the Antarctic fishes. Polish Polar Research, 25: 135–152.

Rohde, K. 1986. Grubea australis n. sp. (Monogenea, Polyopisthocotylea) from Scomber


australasicus in Southeastern Australia, and Grubea cochlear Diesing, 1858 from S.
scombrus and S. japonicus in the Mediterranean and Western Atlantic. Systematic
Parasitology, 9: 29-38.

Rohde, K. 1989. Kuhnia sprostonae Price, 1961 and Kuhnia scomber colias Nasir and Fuentes
Zambrano, 1983 (Monogenea, Mazocraeidae) and their microhabitats on the gills of
Scomber australasicus (Teleostei, Scombridae), and the geographical distribution of 7
species of gill Monogenea of Scomber spp. Systematic Parasitology, 14: 93-100.

Rohde, K. 2002. Ecology and biogeography of marine parasites. Advances in Marine Biology,
43: 1-86.

Rohde, K. 2005. Latitudinal. Longitudinal and depth gradients". In: Marine Parasitology (Ed. K.
Rohde) pp. 348–351. CSIRO Publishing, Melbourne and CABI, Wallingford, Oxon.

32
Rohde, K., C. Hayward and M. Heap, 1995. Aspects of the ecology of metazoan ectoparasites of
marine fishes. International Journal for Parasitology, 25: 945-970.

Rokicki, J. 2009. Effects on climatic changes on anisakid nematodes in Polar Regions. Polar
Sci., 3: 197–201.

Santos, M.J., A. Saraiva, C. Cruz, J. C. Eiras, M. Hermida, C. Ventura and J. P. Soares. 2009. Use
of parasites as biological tags in stock identification of the black scabbardfish,
Aphanopus carbo Lowe, 1839 (Osteichthyes: Trichiuridae) from Portuguese waters.
Scientia Marina, 73(2): 55-62.

Sasal, P., E. Faliex and S. Morand, 1996. Parasitism of Gobius bucchichii Steindachner, 1870
(Teleostei, Gobiidae) in protected and unprotected marine environment. J. Wildlife Dis.,
32: 607-613.

Sasal, P., N. Niquil and P. Bartoli, 1999. Community structure of digenean parasites of sparid and
labrid fishes of the Mediterranean Sea: a new approach. J. Parasitol., 119: 635-648.

Seckendorff, R.W. and L.A. Zavala-Camín. 1985. Reproduction, growth and distribution of
mackerel (Scomber japonicus) in the Southeast and South of Brazil. Bol. Inst. Fishing
São Paulo, 12 (2): 1-13. (with Englsh translation).

Setyobudi, E., C.H. Jeon, C.H. Lee, K.B. Seong and J.H. Kim. 2011. Occurrence and
identification of Anisakis spp. (Nematoda: Anisakidae) isolated from chum salmon
(Oncorhynchus keta) in Korea. Parasitol Res., 108: 585–592.

Silas, E.G. 1967. Parasites of scombroid fishes. Part I. Monogenetic trematodes, digenetic
trematodes, and cestodes. Marine Biology Association. India, Symp. Ser., 1:799-868.

Silva, L.G.O., J.L Luque, D.R. Alves and A.R. Paraguassú. 2000. Ecology parasite community
of swordfish Trichiurus lepturus (Osteichthyes: Trichiuridae) from the coast of the state
of Rio de Janeiro, Brazil. Journal of Zoociências, 2(2): 115-133.(with English
translation).

Shimazu, T. 1986. Lepocreadium misakiense sp.n. and Neopechona olssoni (Yamaguti, 1934),
comb.n. (Trematoda: Lepocreadiidae), parasites of a Japanese marine fish, Scomber
japonicus. Zooi. Sci., 3(3): 569-571.

Shimazu, T. 1989. Taxonomic notes on Cephalolepidapedon saba and Opechona orientalis


(Trematoda: Lepocreadiidae) of the marine fish, Scomber japonicus (Teleostei:
Scombridae). Jap. J. Parasitol., 38(4): 232-235.

Shukhgalter, O.A. 2004. The parasite fauna of the chub mackerel (Scombridae: Scomber
japonicus Houttuyn, 1782) in the central-eastern Atlantic (Atlantic coast of northern
Africa and the Azores Archipelago banks). Parasitological, 38: 160–170 (in Russian with
English summary).

33
Suzuki, J., R. Murata, M. Hosaka and J. Araki. 2010. Risk factors for human anisakis infection
and association between the geographic origins of Scomber japonicus and anisakid
nematodes. Int. J. Food Microbiol., 137: 88–93.

Taliaferro, W. 2009. Chapter 2. Basic Principles and Concepts I: Parasite Systematic, Ecology,
and Evolution. p. 11-24. In: Roberts, L.S. and Ovy, J.R. (eds.). Foundation of
Parasitology, Eighth Edition. Encyclopedia of Life Support Systems (EOLSS). Retrieved
from http://www.eolss.net/sample-chapters/c03/e5-25-52.pdf on February 6, 2015.

Tantanasi, J., A. Diakou, A. Tamvakis and L.E.B. Atjakas. 2012. Anisakis spp. burden in
Trachurus trachurus. Helmintholgia, 49: 1:16-20.

Timi, J.T. 2007. Parasites as biological tags for stock discrimination in marine fish from south
American Atlantic waters. Journal of Helminthology, 81: 107-111

Trinidad, A.C., R.S. Pomeroy, P.V. Corpuz and M. Aguero. 1993. Bioeconomics of the
Philippine small pelagics fishery. ICLARM Tech. Rep. 38. Makati, Metro Manila,
Philippines. 74 p.

Umehara, A., Y. Kawakami, H.K. Ooi, A. Uchida, H. Ohmae and H. Sugiyama. 2010. Molecular
identification of anisakis type I larvae isolated from hairtail fish off the coasts of Taiwan
and Japan. Int J. Food Microbiol., 143: 161–165.

Ware, D.M. and T.C. Lambert. 1985. Early life history of Atlantic mackerel (Scomber
scombrus) in the southern Gulf of St. Lawrence. Can. J. Fish. Aquat. Sci., 42: 577-592.

Williams, H.H., K. MacKenzie and A.M. McCarthy. 1992. Parasites as biological indicators of
the population biology, migrations, diet, and phylogenetics of fish. Reviews in Fish
Biology and Fisheries, 2: 144-176.

Wysokinski, A., E. Bóberski, H. Czykieta and J. Myzykiewicz. 1987. The results of


preliminary observations of the parasitism of fish along Namibian coast. Retrieved from
www.fao.org/docrep/017/x4287e/x4287e.pdf on November 17, 2014.

Yeh, J. 2002. Parasitism: an entry from Macmillan Reference USA's Macmillan Reference USA
Science Library: Animal Sciences (digital document). Retrieved from
http://www.eolss.net/sample-chapters/c03/e5-25-52.pdf on February 6, 2015.

Yoon, S.J., D.H. Kim, G.W. Baeck and J.W. Kim, 2008. Feeding habits of chub mackerel
(Scomber japonicus) in the south Sea of Korea. J. Korean Fish. Soc., 41: 26–31 (in
Korean with English summary).

Zar, J.H. 1996. Biostatistical Analysis, Third Edition. Prentice-Hall, Inc. USA. 662 p.

34
Zardoya, R., R. Castilho, C. Grande, L. Favre-Krey, S. Caetano, S. Marcato, G. Krey and T.
Patarnello. 2004. Differential population structuring of two closely related fish species,
the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the
Mediterranean Sea. Molecular Ecology, 13: 1785-1798.

Zavala-Camin, L.A. and R.W. Seckendorif. 1980. Ocurrencia de jovenes de caballa (Scomber
japonicas Houttuyn, 1780) en el sudeste del Brasil (20°S-27°S), obtenida por medio de
colectas de contenido estomacal de atunes y afines (informe preliminar). Retrieved from
www.fao.org/docrep/017/x4287e/x4287e.pdf on November 15, 2014.

Zavala-Camin, L.A. 1982. Distribución vertical y estacional de tunideos y otras especies


pelágicas en el Sudeste y Sur de Brasil, obtenida por medio de análisis de contenido
estomacal. Retrieved from www.fao.org/docrep/017/x4287e/x4287e.pdf on November 15,
2014.

Zhou, P., N. Chen, R.L. Zhang, R.Q. Lin and X.Q. Zhu. 2008. Food borne parasitic zoonoses in
China: perspective for control. Trends Parasitol., 24: 190-196.

http://www.cdc.gov/parasites/

http//www.dictionary.com

http://en.wikipedia.org

https://en.wikipedia.org/wiki/Chub_mackerel

http://en.wikipedia.org/wiki/Mackerel

http://www.ppa.com.ph/batangas/about_lucena.html

http://www.pdosoluz.com.ph/port-of-lucena-updated.html

35

You might also like