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Some ecological aspects of the copepod parasites of the common hake, merluccius hubbsi, from the argentineuruguayan coasts
SOME ECOLOGICAL ASPECTS OF THE COPEPOD PARASITES OF THE COMMON HAKE, MERLUCCIUS HUBBSI, FROM THE ARGENTINEURUGUAYAN COASTS JORGE ALEJANDRO ETCHEGOIN and NORMA HAYDEE SARDELLA Parasitology Laboratory, Instituto National de Investigation y Desarrollo Pesquero (INIDEP), Casilla de Correo 175, 7600 Mar de1 Plata, Argentina (Received 14 August 1989; accepted 18 March 1990) J. A and SARDELLA N. H. 1990. Some ecological aspects of the copepod parasites of the common hake, Merluccius hubbsi, from the Argentine-Uruguayan coasts. International Journal for Parasitology 20: 1009-1014. A total of 2164 common hake Merluccius hubbsi captured in the ArgentineUruguayan Common Fishing Zone was examined for parasitic copepods. The fish were infested with Chondracanthuspalpijkr and Neobrachiella insidiosa f. lageniformis, the former parasitizing the buccal cavity and the latter the branchial arches. C. palpifer showed an increase in both prevalence and intensity in relation to the host size; infestation with N. insidiosa f. lageniformis decreased with increasing length of hake. Attachment site preferences and variations in the parasite distribution patterns as related to the host biology were observed. Evidence of negative association between copepod species and seasonal changes in the parasite composition was also found.
Abstract-~TcHEGolN
INDEX KEY WORDS: Copepod parasites; host-parasite interactions; prevalence; intensity; Merluccius hubbsi; Chondracanthuspalpzyer; Neobrachiella insidiosa f. lageniformis; Argentine-Uruguayan coasts.
INTRODUCTION of copepod parasites in the common hake Merluccius hubbsi from the Argentine Continental Shelf has been previously reported by Brian (1944), Kabata (1979), Kabata & Ho (1981), Ringuelet (1947) and Szidat (1955). Three species have been noted: Chondracanthus palpifer in the buccal cavity, Neobrachiella insidiosa f. lageniformis in the branchial cavity and Trifur tortuosus on the external body area. Except for the paper by Rey & Cascudo (1986), the data related to the existence of parasitic copepods in M. hubbsi have been mainly based upon systematic aspects. The ecological interactions of the host with each of the copepod species that parasitize it have therefore been analyzed in more detail in this paper. Distribution patterns of those parasites in hake were thus examined, together with the parasitic prevalence and intensity in relation to the size and sex of the host and the seasonal effects on copepod infestations. THE
presence
MATERIALS AND METHODS The present study is based upon parasitological examination of 2164 common hake M. hubbsi taken from the Argentine-Uruguayan Common Fishing Zone (Fig. 1) between May and November 1986. Samples were collected with bottom-trawl survey gear during cruises of R.V. Cup. Oca Eulda. Fish were measured for total length (T.L.) and sexed. The buccal cavity of each hake was checked, together with the branchial cavities and external body area; copepod
parasites were identified and quantified. A total of 1294 hake were examined in order to determine the distribution patterns of parasites on the host. The buccal cavity was divided into upper palate (roof and gum), lower palate and tongue (central, apical and lateral areas). In the left and right branchial cavities, each arch (I to IV) was subdivided into three areas: inferior, middle and superior. The body area was not subdivided. Prevalence and intensity of infestation were calculated for each copepod species as related to the body size and sex of the host. The heterogeneity G-test (GH), Chisquare test and Simultaneous Test Procedure (STP) (Sokal & Rohlf, 1979) were used for statistical analyses. RESULTS Fish were infested
with C. paz’pzjk and N. insidiosa f.
lugeniformis, the former parasitizing the buccal cavity and the latter the branchial arches. The values for prevalence and intensity in relation to the body size of the host were different for the two species (Table I). C. palpzjk showed an increase in both prevalence and intensity in relation to the increase in the size of the host (Table 1, Figs. 2 and 3). The highest prevalence was 75.9% in the S&60 cm T.L. size class and the highest intensity (3.9) occurred in the 6680 cm T.L. size class. Prevalence and intensity levels showed no significant differences in connection with the sex of the host (Chi-square test not significant at the 0.05 level). Data gathered in the transition months between the autumn and winter (May and June) and in the late spring (November) showed no seasonal effects in prevalence levels (Chi-square test not significant at the
1010
J. A. ETCHEGOIN and N. H. SARDELLA
._ -.-; I
68
620
!iP
I
*-
sip
&
520
Ftc. I. Positions (0) of bottom-trawl stations within the Argentin~U~guayan where hake were collected.
no
Common Fishing Zone
I 0
I
80
I
11
21
31
41
51
SIZE
61
~466
CLASS (in
cml
FIG. 2. Prevalence of C~o~dracanth~s pafpifer and ~e~brach~el~a insidiosa f. lage~~r~~s with regard to the length of the host ~e~lucci~ hubbsi. l -*-* Ch5ndrac~th~ paipifer; e--*--m IV. insidiosa f. ~age~t~ur~~s.
1011
Copepod parasites of the hake M. hubbsi
11
21
41
31
51
e1 SIZE
-6s CLASS
(in
3. Intensity of ChondracanzhuspalpiJk length of the host Merluccius hubbsi. .-e-e
FIG.
and N. insidiosa f. lageniformis with regard to the C. palpifer; .--a--. N. insidiosa f. lageniformis.
TABLE ~-PREVALENCE (P) AND INTENSITY(I) OF C. palpifer AND N. insidiosa f. ~ageniformis IN RELATIONTOTHESIZEOFTHE HOSTM. hubbsi
Host size class (in cm) 11-15 16-20 21-25 2630 31-35 3640 4145 4650 51-55 5660 61-65 6680
N 176 571 265 209 120 212 266 184 68 29 27 29
C. palpifer P
I
_ 0.4 1.9 6.2 15.0 13.7 19.2 36.4 47.1 75.9 51.9 68.9
1.0 1.0 1.2 1.1 1.4 1.4 1.5 2.5 2.6 3.0 3.9
N. insidiosa P I
6.3 12.3 23.0 29.7 27.5 19.3 9.8 10.3 7.4 3.5 _ 3.4
cm J
1.2 1.2 1.5 1.6 2.0 2.0 2.5 1.7 1.6 I.0 _ 1.0
N: number of fish examined.
0.05 level). In order to examine the relationship between the distribution pattern of C. pulp@ in the buccal cavity of the host and the increase in body size of the hake, parasite attachment sites were grouped into six regions: I (roof of the upper palate), II (gum of the upper palate), III (lower palate), IV (tip of the tongue), V (middle of the tongue) and VI (tongue laterals) (Table 2). In smaller sizes (1635 cm T.L.) the parasite was exclusively located in the roof of the upper palate; its distribution diversified as from intermediate sizes (41-50 cm T.L.). In intermediate and larger sizes C. palpifer was also detected in the lower palate and
tongue. The heterogeneity G-test (GH) was utilized for analyzing these results (Table 2). The G-test was highly significant in indicating that among the sizes as reviewed existed a marked heterogeneity in the distribution pattern of the parasite. An a posteriori Simultaneous Test Procedure using the G-statistic was utilized for locating heterogeneity sources and the fish were classified into three size classes: l&45,46-60 and 61-80 cm T.L. The results of the STP showed that the two sets comprising the largest size class (61-80 cm T.L.) were markedly heterogeneous whilst the set involving small and intermediate sizes (l&45 and 46 60 cm T.L.) was homogeneous (Table 2). On the basis of these results the most outstanding changes in the distribution of the parasite would seem to occur in the intermediate size class (46-60 cm T.L.) with an increase in the presence of C. palpifer in regions II, III, IV, and V. N. insidiosa f. lageniformis showed a decrease in its levels of prevalence and intensity with the body length of the fish (Table 1, Figs. 2 and 3). Its presence was not registered in hake over 71 cm in length. The highest prevalence was 29.7% in the 26-30 cm T.L. size class; the highest intensity (2.5) occurred in the 41-45 cm T.L. size class. The analysis of prevalence levels in relation to the sex of the host showed a significant difference for fish gathered during the spring. The infestation rates were 22.2 and 10.7% for male and female hake, respectively (X2 : 9.56, P < 0.05). During transition between autumn and winter, male and female hake were found to be infested in similar proportions. Infestation levels also showed seasonal fluctuations.
1012
J. A. TABLE ~-DISTRIBUTION Host size class (in cm)
C.palpifer~~
I N
16-20 21-25 2630 31-35 36-40 41-45 4650 51-55 5680
0~
368 141 165 79 63 110 94 46 61
Fi 1 3 7 8 11 17 35 25 45
a
and N. H. SARDELLA
ETCHEGOIN
THEBUCCALCAVITYINRELATIONTOTHES~ZEOFTHEHOST
Parasite attachment sites III IV a b a b
II a
b
b _ _ _
l(lO0) 3(100) 7( 100) lO(100) 1O(90.9) 20(83.3) 30(76.9) 36(65.5) 78(53.4)
V a
_ _
_ _ _ _
VI b
_ _ _ _
_
l(4.2) _
l(4.2) 2(5.1)
2(8.3) 4(10.3) 1 l(20.0) 12(8.2)
5(9.1) 29( 19.9)
b _ _ _ _ _ _
l(9.1) 2(5.1) 3(5.4) 12(8.2)
a
l(2.6) _
15(10.3)
For a description of attachment sites see text. N: Number of fish examined; Fi: number of fish infected; a: number of parasites in a region; b: percentages ofparasites in a region. GH: 45.57, P c 0.05. An aposterioriSTP determined two heterogeneous sets (1645/61-80 cm T.L. and 46-60/61-80 cm T.L.) and a homogeneous one (lC45/4660 cm T.L.).
TABLE
~-DISTRIBUTION
OF
N. insidiosa f. kZgetZifot’miS IN THE
BRANCHIALARCHES
IN
RELATIONTOTHESlZEOFTHEHOST
Host size
Parasite I
class (in cm) N 11-15 1620 21-25 2630 31-35 3&40 4145 4650 5 l-70
159 368 141 165 79 63 110 94 99
Fi 8 27 33 50 22 12 6 4 6
a 9 32 39 57 37 14 7 4 5
b (100) (91.4) (81.3) (78.1) (84.1) (50.0) (53.9) (66.7) (55.6)
attachment II a b
sites III a
b
_ 7 (14.6) 12 (16.4) 7 (15.9) 5 5 1 1
(38.5) (38.5) (16.7) (11.1)
3 (8.6) 2 (4.2) 4 (5.5) _ 9 1 1 3
(32.1) (7.7) (16.7) (33.3)
See text for description of attachment sites. N: Number of fish examined; Fi: number of fish infested; a: number of parasites in a region; b: percentages of parasites in a region. GH: 11.8, P < 0.05. An a posteriori STP determined three homogeneous sets: O-25/2&45 cm T.L.; 2&45/46-80 cm T.L. and &25/46-80 cm T.L. -
The significant difference occurred in juveniles (1 l-20 cm T.L.; X2: 25.49, P < 0.05) and in adults of intermediate sizes (41-50 cm T.L.; X2: 7.60, P < 0.05). In both cases, the levels of infestation were highest in autumn (20 and 14.2%, respectively) and declined in spring (7.2 and 5.7%, respectively) (X2 test significant, P < 0.05). The variations in the distribution pattern of N. insidiosa f. lageniformis in the branchial cavity as regards the size of the host were analyzed in a similar manner as for changes in the location of C. palpfer (Table 3). Parasite attachment sites were grouped into three regions: I (inferior area, including the hypobranchial bone and the lower portion of the ceratobranchial bone); II (middle area, including the middle portions of the ceratobranchial bone) and III (superior area, including the epibranchial bone). The results showed a higher percentage of parasites
in region I; however, with the increase in length of hake, a displacement of parasites toward regions II and III was noted. The G-test was significant (Table 3), N. insidiosa f. lagenl~ormis distribution is heterogeneous in the sizes as reviewed. The STP determined three homogeneous sets: the ones that contributed the most to heterogeneity were those comprising the smallest size class (O-25 cm T.L.). For such sizes, N. insidiosa f. lageniformis would preferably adhere to the inferior area of the branchial arch, thus marking the difference with other sizes as reviewed. The percentage of copepods found in each arch (calculated on the total number of copepods registered) showed that the parasite prefers the first arch. Copepod percentages were 80.29 for the first arch, 14.49 for the second, 4.83 for the third and 0.37 for the fourth branchial arch. For sizes between 16 and 70 cm T.L., the presence of
Copepod parasites of the hake M. hubbsi both species C. palpifer and N. insidiosa f. lageniformis parasitizing the same host was noted. In order to examine the possibility of interactions between the two species of copepods, a chi-square test was utilized. The test was not significant at the 0.05 level, thus suggesting that a positive association between the two parasites does not exist. Trifur tortuosus, the third species of copepod cited by Bellisio, Lopez & Torno (1979) and Rey & Cascudo (1986) parasitizing the common hake in the Argentine-Uruguayan Common Fishing Zone, was not found in this study. Probably, T. tortuosus is at present restricted to the Patagonia area (Etchegoin, 1988). DISCUSSION The availability of adequate space and the changes in the host’s biology seem to be determinant factors for the increase in the prevalence and intensity of C. palpifer and N. insidiosa f. lageniformis. The progressive increase in C. palpifer infestation levels coincides with the increase in the host’s buccal diameter. The growth of the buccal cavity is intensified in hake with sizes exceeding 30 cm T.L., making it easier for them to ingest larger prey (Angelescu & Prenski, 1987). This change in the size of mouth, that is related to the trophic habits of M. hubbsi (zooplanktophagous young fish transform themselves into active predators), gives C. palpzfer a larger area for attachment; thus, in the smallest fish the copepod is exclusively located in the roof of the upper palate. In the intermediate sizes and older fish, it is possible to detect the parasites in the lower palate and tongue (apical, middle and lateral areas). When the copepod is fixed to the lower palate, to the tip and lateral areas of the tongue, its body occupies the space limited by gums and tongue. It may be noted, bearing in mind the percentage of copepods found in each of the above mentioned areas, that the region C. paZpifer prefers is that of the upper palate. The roof of the upper palate, with the form of a vault, allows the parasite to withstand the pressure of food passing through the mouth of the fish. The other regions with a lower percentage are probably less adequate for the development of the copepod’s life cycle. The main risk factor for the parasite in the lower area of the buccal cavity would be that of the tongue rubbing the gums. Copepods attached to the gum of the lower palate and to the lateral and apical areas of the tongue would be subject to the rubbing. The space between the tongue and gum is narrower in the lateral areas than in the zone around the tip of the tongue; thus, the parasites attached to the lateral regions of the tongue and to the base of the gum are more exposed to rubbing; however, percentages corresponding to the lower palate are markedly higher than those for the lateral areas of the tongue (Table 2). This might be due to the fact that, for the first case (base of the gum) the attachment area remains stable and with no change in its form, whilst in the second,
1013
the attachment area (tongue) moves during the rubbing. Such a disturbance that would affect the attachment organ of the crustacean-the modified, hook-like second antennae do not penetrate deeply into the tissues of the buccal cavity-plus the rubbing, the narrowness of the space occupied by the parasites body and the pressure of food ingesta by the host, would increase the possibility that the copepods were removed from the buccal cavity. N. insidiosa f. lageniformis showed a decrease in infestation levels with the increase in the size of hake. Fernandez (1985) obtained similar results for the same species parasitizing Merluccius australis in Chile and Shotter (1973) also reported a decrease in infestation with Clavella (another member of the family Lemaeopodidae) with increasing age of whiting Odontogadus merlangus in the vicinity of the Isle of Man. The low infestation levels could result from the increase in the strength of the respiratory current in older fish or from the immunological response of adult fish (Shotter, 1973). The increase in the strength of the respiratory current would render difficult the attachment of the copepodids and they would be dislodged from branchial arches, thus preventing the necessary reinfestation to maintain the population of the parasite. On the other hand, common hake adults progressively lose the filtration capacity of the first branchial arch, thus reducing the growth rate of the distance between the gill rakers which is important for the selective and retention functions of zooplankton species in the young hake (Angelescu & Prenski, 1987). These observations coincide with the lowest prevalence and intensity values of N. insidiosa f. lageniformis, which would seem to indicate a close relationship between the hake’s filtering system and the attachment of copepods to the branchial arch. Probably, copepods are held by the filtering system of the fish, thus favoring their attachment to gill rakers and branchial arches. It should also be noted that the first branchial arch is the one that shows the highest percentage of copepods (80.29) and it is in this arch where the gill rakers of the hake’s filtering system are located. The same preference for the first branchial arch was observed by Sankurathri, Kabata & Whitaker (1983) in N. insidiosa f. pacifica parasitizing Merluccius productus. N. insidiosa f. lageniformis distribution showed a marked preference for the inferior area of the branchial arch: in that area, copepod percentages were near 100% in the smallest sizes (Table 3). In adults, the increase in the length of the branchial arch would facilitate the attachment of the parasite in the middle and superior areas (the attachment in these areas could be difficult in smaller fish due to the reduced length of the branchial arch and because of the presence of another parasite in the inferior area). In addition, the density increase could mean there is more competition for the inferior area, thus causing more copepods to move toward the superior zone of the branchial arch.
J. A. ETCHEGOIN and N. H. SARDELLA
1014
Distribution and site preferences of parasites in gill arches, gill filaments and branchial cavity have also been reported by Kabata (1959) and Rohde (1976, 1977, 1984). Seasonal effects on N. insidiosa f. lagen$ormis infestation levels might be the result of a change in the population structure of the hake due to the winter trophic migration of juveniles within the ArgentineUruguayan Common Fishing Zone (Angelescu & Prenski, 1987) and to reproductive migration of adults toward the spawning area on the Patagonia coast. Sankurathri et al. (1983) also found seasonal differences in N. insidiosa f. pac$ca. The authors related these findings to a decrease in the female population of the parasite because of mortalities during the autumn. Rey & Cascudo (1986) cite the seasonal effects on the prevalence of N. insidiosa f lageniformis but they do not mention any difference in infestation levels in relation to the sex of M. hubbsi. The differences as noted in this paper might be due to the migratory movements that were mentioned above, or to the size and sex composition of the samples. Acknowledgements-We gratefully thank Ph. D. Armand Kuris, University of California, Santa Barbara and Dr Mario George-Nascimento, Pontificia Universidad Cat6lica de Chile, Talcahuano, for their valuable suggestions. REFERENCES ANGELESCU V. & PRENSKI L. B. 1987. Ecologia
t&c8 de la merluza corntin (Merluccidae, Merluccius hubbsi). Parte 2. Dinamica de la alimentacibn analizada sobre la base de las condiciones ambientales, la estructura y las evaluaciones de 10s efectivos en su Brea de distribucibn. Contribuci6n de1 Instituto National de Investigacidn y Desarrollo Pesquero (INIDEP), Mar de1 Plata, No. 561. BELLISION. B., LOPEZ R. B. & TORNO A. 1979. Peces marinos patagbnicos. Publicaci6n de la Secretaria de Intereses Maritimos. Editorial Codex, Buenos Aires. BRIAN A. 1944. Cop&podos parasites de peces y cetaceos de1 Museo Argentino de Ciencias Naturales. Anales de1 Museo Argentina de Ciencias Naturales 41: 193-220. EXHEGOIN J. A. 1988. CopCpodos parisitos de Merluccius
hubbsi. Seminario de Investigacidn. Universidad National de Mar de1 Plata. FERNANDEZJ. 1985. Estudio parasitol6gico de Merluccius australis (Hutton, 1872) (Pisces: Merluccidae): aspectos sistemiticos, estadisticos y zoogeogr8ficos. Eoletin de la Sociedad Biolbgica de Conceptidn, Chile 56: 31-41. KABATA Z. 1959. Ecology of the genus Acanthochondria Oakley (Copepoda, Parasitica). Journal of the Marine Biological Association of the United Kingdom 38: 249-261. KABATA Z. 1979. Parasitic Copepodr of British Fishes. The Ray Society, London. KABATAZ. &Ho J. S. 1981. The origin and dispersal of hake (genus Merluccius: Pisces: Teleostei) as indicated by its copepod parasites. Oceanographical Marine Biology Annual Review 19: 381404. REY M. & CASCULXJJ. 1986. Relaciones entre parasitism0 y comportamiento biolbgico de la merluza (Merluccius hubbsi). Publicacibn de la Comisicin TPcnica Mixta del Frente Maritimo 1: 240-25 1. RINGUELET R. 1947. Anotaciones sobre coptpodos e is6podos parlsitos de peces. Notas del Museo de La Plata Zool., No. 98, Vol. 12, pp. 92-107. ROHDE K. 1976. Monogenean gill parasites of Scomberomorus commersoni Laceptde and other mackerel on the Australian East Coast. Zeitschrift fiir Parasitenkunde 51: 49-69. ROHDE K. 1977. A non-competitive mechanism responsible for restricting niches. Zoologischer Anzeiger 199: 164172. ROHDE K. 1984. Ecology of marine parasites. Helgolander Meeresunters 37: 5-33. SANKURA~HRIC. S., KABATA Z. & WHITAKER D. J. 1983. Parasites of the Pacific hake, Merluccius productus (Ayres, 1855) in the Strait of Georgia, in 19741975. Syesis 16: 522. SHOTTERR. A. 1973. Changes in the parasitic fauna of the whiting, Odontogadus merlangus L. with the age and sex of the host, season, and from different areas in the vicinity of the Isle of Man. Journal of Fish Biology 5: 559-573. SOKAL R. R. & ROHLF F. J. 1979. Biometria. Principios y metodos estadisticos en la investigacicin biokigica. Editorial Blume, segunda Edicibn, Madrid. SZIDAT L. 1955. La fauna de parisitos de Merluccius hubbsi Mar. coma caracter auxiliar para la soluci6n de problemas sistematicos y zoogeogrLficos de1 ginero Merluccius. Comisidn National de Investigacidn de Ciencias Naturales “B. Rivadavia”, Zoo1 3: 54.
Abstract-~TcHEGolN
INDEX KEY WORDS: Copepod parasites; host-parasite interactions; prevalence; intensity; Merluccius hubbsi; Chondracanthuspalpzyer; Neobrachiella insidiosa f. lageniformis; Argentine-Uruguayan coasts.
INTRODUCTION of copepod parasites in the common hake Merluccius hubbsi from the Argentine Continental Shelf has been previously reported by Brian (1944), Kabata (1979), Kabata & Ho (1981), Ringuelet (1947) and Szidat (1955). Three species have been noted: Chondracanthus palpifer in the buccal cavity, Neobrachiella insidiosa f. lageniformis in the branchial cavity and Trifur tortuosus on the external body area. Except for the paper by Rey & Cascudo (1986), the data related to the existence of parasitic copepods in M. hubbsi have been mainly based upon systematic aspects. The ecological interactions of the host with each of the copepod species that parasitize it have therefore been analyzed in more detail in this paper. Distribution patterns of those parasites in hake were thus examined, together with the parasitic prevalence and intensity in relation to the size and sex of the host and the seasonal effects on copepod infestations. THE
presence
MATERIALS AND METHODS The present study is based upon parasitological examination of 2164 common hake M. hubbsi taken from the Argentine-Uruguayan Common Fishing Zone (Fig. 1) between May and November 1986. Samples were collected with bottom-trawl survey gear during cruises of R.V. Cup. Oca Eulda. Fish were measured for total length (T.L.) and sexed. The buccal cavity of each hake was checked, together with the branchial cavities and external body area; copepod
parasites were identified and quantified. A total of 1294 hake were examined in order to determine the distribution patterns of parasites on the host. The buccal cavity was divided into upper palate (roof and gum), lower palate and tongue (central, apical and lateral areas). In the left and right branchial cavities, each arch (I to IV) was subdivided into three areas: inferior, middle and superior. The body area was not subdivided. Prevalence and intensity of infestation were calculated for each copepod species as related to the body size and sex of the host. The heterogeneity G-test (GH), Chisquare test and Simultaneous Test Procedure (STP) (Sokal & Rohlf, 1979) were used for statistical analyses. RESULTS Fish were infested
with C. paz’pzjk and N. insidiosa f.
lugeniformis, the former parasitizing the buccal cavity and the latter the branchial arches. The values for prevalence and intensity in relation to the body size of the host were different for the two species (Table I). C. palpzjk showed an increase in both prevalence and intensity in relation to the increase in the size of the host (Table 1, Figs. 2 and 3). The highest prevalence was 75.9% in the S&60 cm T.L. size class and the highest intensity (3.9) occurred in the 6680 cm T.L. size class. Prevalence and intensity levels showed no significant differences in connection with the sex of the host (Chi-square test not significant at the 0.05 level). Data gathered in the transition months between the autumn and winter (May and June) and in the late spring (November) showed no seasonal effects in prevalence levels (Chi-square test not significant at the
1010
J. A. ETCHEGOIN and N. H. SARDELLA
._ -.-; I
68
620
!iP
I
*-
sip
&
520
Ftc. I. Positions (0) of bottom-trawl stations within the Argentin~U~guayan where hake were collected.
no
Common Fishing Zone
I 0
I
80
I
11
21
31
41
51
SIZE
61
~466
CLASS (in
cml
FIG. 2. Prevalence of C~o~dracanth~s pafpifer and ~e~brach~el~a insidiosa f. lage~~r~~s with regard to the length of the host ~e~lucci~ hubbsi. l -*-* Ch5ndrac~th~ paipifer; e--*--m IV. insidiosa f. ~age~t~ur~~s.
1011
Copepod parasites of the hake M. hubbsi
11
21
41
31
51
e1 SIZE
-6s CLASS
(in
3. Intensity of ChondracanzhuspalpiJk length of the host Merluccius hubbsi. .-e-e
FIG.
and N. insidiosa f. lageniformis with regard to the C. palpifer; .--a--. N. insidiosa f. lageniformis.
TABLE ~-PREVALENCE (P) AND INTENSITY(I) OF C. palpifer AND N. insidiosa f. ~ageniformis IN RELATIONTOTHESIZEOFTHE HOSTM. hubbsi
Host size class (in cm) 11-15 16-20 21-25 2630 31-35 3640 4145 4650 51-55 5660 61-65 6680
N 176 571 265 209 120 212 266 184 68 29 27 29
C. palpifer P
I
_ 0.4 1.9 6.2 15.0 13.7 19.2 36.4 47.1 75.9 51.9 68.9
1.0 1.0 1.2 1.1 1.4 1.4 1.5 2.5 2.6 3.0 3.9
N. insidiosa P I
6.3 12.3 23.0 29.7 27.5 19.3 9.8 10.3 7.4 3.5 _ 3.4
cm J
1.2 1.2 1.5 1.6 2.0 2.0 2.5 1.7 1.6 I.0 _ 1.0
N: number of fish examined.
0.05 level). In order to examine the relationship between the distribution pattern of C. pulp@ in the buccal cavity of the host and the increase in body size of the hake, parasite attachment sites were grouped into six regions: I (roof of the upper palate), II (gum of the upper palate), III (lower palate), IV (tip of the tongue), V (middle of the tongue) and VI (tongue laterals) (Table 2). In smaller sizes (1635 cm T.L.) the parasite was exclusively located in the roof of the upper palate; its distribution diversified as from intermediate sizes (41-50 cm T.L.). In intermediate and larger sizes C. palpifer was also detected in the lower palate and
tongue. The heterogeneity G-test (GH) was utilized for analyzing these results (Table 2). The G-test was highly significant in indicating that among the sizes as reviewed existed a marked heterogeneity in the distribution pattern of the parasite. An a posteriori Simultaneous Test Procedure using the G-statistic was utilized for locating heterogeneity sources and the fish were classified into three size classes: l&45,46-60 and 61-80 cm T.L. The results of the STP showed that the two sets comprising the largest size class (61-80 cm T.L.) were markedly heterogeneous whilst the set involving small and intermediate sizes (l&45 and 46 60 cm T.L.) was homogeneous (Table 2). On the basis of these results the most outstanding changes in the distribution of the parasite would seem to occur in the intermediate size class (46-60 cm T.L.) with an increase in the presence of C. palpifer in regions II, III, IV, and V. N. insidiosa f. lageniformis showed a decrease in its levels of prevalence and intensity with the body length of the fish (Table 1, Figs. 2 and 3). Its presence was not registered in hake over 71 cm in length. The highest prevalence was 29.7% in the 26-30 cm T.L. size class; the highest intensity (2.5) occurred in the 41-45 cm T.L. size class. The analysis of prevalence levels in relation to the sex of the host showed a significant difference for fish gathered during the spring. The infestation rates were 22.2 and 10.7% for male and female hake, respectively (X2 : 9.56, P < 0.05). During transition between autumn and winter, male and female hake were found to be infested in similar proportions. Infestation levels also showed seasonal fluctuations.
1012
J. A. TABLE ~-DISTRIBUTION Host size class (in cm)
C.palpifer~~
I N
16-20 21-25 2630 31-35 36-40 41-45 4650 51-55 5680
0~
368 141 165 79 63 110 94 46 61
Fi 1 3 7 8 11 17 35 25 45
a
and N. H. SARDELLA
ETCHEGOIN
THEBUCCALCAVITYINRELATIONTOTHES~ZEOFTHEHOST
Parasite attachment sites III IV a b a b
II a
b
b _ _ _
l(lO0) 3(100) 7( 100) lO(100) 1O(90.9) 20(83.3) 30(76.9) 36(65.5) 78(53.4)
V a
_ _
_ _ _ _
VI b
_ _ _ _
_
l(4.2) _
l(4.2) 2(5.1)
2(8.3) 4(10.3) 1 l(20.0) 12(8.2)
5(9.1) 29( 19.9)
b _ _ _ _ _ _
l(9.1) 2(5.1) 3(5.4) 12(8.2)
a
l(2.6) _
15(10.3)
For a description of attachment sites see text. N: Number of fish examined; Fi: number of fish infected; a: number of parasites in a region; b: percentages ofparasites in a region. GH: 45.57, P c 0.05. An aposterioriSTP determined two heterogeneous sets (1645/61-80 cm T.L. and 46-60/61-80 cm T.L.) and a homogeneous one (lC45/4660 cm T.L.).
TABLE
~-DISTRIBUTION
OF
N. insidiosa f. kZgetZifot’miS IN THE
BRANCHIALARCHES
IN
RELATIONTOTHESlZEOFTHEHOST
Host size
Parasite I
class (in cm) N 11-15 1620 21-25 2630 31-35 3&40 4145 4650 5 l-70
159 368 141 165 79 63 110 94 99
Fi 8 27 33 50 22 12 6 4 6
a 9 32 39 57 37 14 7 4 5
b (100) (91.4) (81.3) (78.1) (84.1) (50.0) (53.9) (66.7) (55.6)
attachment II a b
sites III a
b
_ 7 (14.6) 12 (16.4) 7 (15.9) 5 5 1 1
(38.5) (38.5) (16.7) (11.1)
3 (8.6) 2 (4.2) 4 (5.5) _ 9 1 1 3
(32.1) (7.7) (16.7) (33.3)
See text for description of attachment sites. N: Number of fish examined; Fi: number of fish infested; a: number of parasites in a region; b: percentages of parasites in a region. GH: 11.8, P < 0.05. An a posteriori STP determined three homogeneous sets: O-25/2&45 cm T.L.; 2&45/46-80 cm T.L. and &25/46-80 cm T.L. -
The significant difference occurred in juveniles (1 l-20 cm T.L.; X2: 25.49, P < 0.05) and in adults of intermediate sizes (41-50 cm T.L.; X2: 7.60, P < 0.05). In both cases, the levels of infestation were highest in autumn (20 and 14.2%, respectively) and declined in spring (7.2 and 5.7%, respectively) (X2 test significant, P < 0.05). The variations in the distribution pattern of N. insidiosa f. lageniformis in the branchial cavity as regards the size of the host were analyzed in a similar manner as for changes in the location of C. palpfer (Table 3). Parasite attachment sites were grouped into three regions: I (inferior area, including the hypobranchial bone and the lower portion of the ceratobranchial bone); II (middle area, including the middle portions of the ceratobranchial bone) and III (superior area, including the epibranchial bone). The results showed a higher percentage of parasites
in region I; however, with the increase in length of hake, a displacement of parasites toward regions II and III was noted. The G-test was significant (Table 3), N. insidiosa f. lagenl~ormis distribution is heterogeneous in the sizes as reviewed. The STP determined three homogeneous sets: the ones that contributed the most to heterogeneity were those comprising the smallest size class (O-25 cm T.L.). For such sizes, N. insidiosa f. lageniformis would preferably adhere to the inferior area of the branchial arch, thus marking the difference with other sizes as reviewed. The percentage of copepods found in each arch (calculated on the total number of copepods registered) showed that the parasite prefers the first arch. Copepod percentages were 80.29 for the first arch, 14.49 for the second, 4.83 for the third and 0.37 for the fourth branchial arch. For sizes between 16 and 70 cm T.L., the presence of
Copepod parasites of the hake M. hubbsi both species C. palpifer and N. insidiosa f. lageniformis parasitizing the same host was noted. In order to examine the possibility of interactions between the two species of copepods, a chi-square test was utilized. The test was not significant at the 0.05 level, thus suggesting that a positive association between the two parasites does not exist. Trifur tortuosus, the third species of copepod cited by Bellisio, Lopez & Torno (1979) and Rey & Cascudo (1986) parasitizing the common hake in the Argentine-Uruguayan Common Fishing Zone, was not found in this study. Probably, T. tortuosus is at present restricted to the Patagonia area (Etchegoin, 1988). DISCUSSION The availability of adequate space and the changes in the host’s biology seem to be determinant factors for the increase in the prevalence and intensity of C. palpifer and N. insidiosa f. lageniformis. The progressive increase in C. palpifer infestation levels coincides with the increase in the host’s buccal diameter. The growth of the buccal cavity is intensified in hake with sizes exceeding 30 cm T.L., making it easier for them to ingest larger prey (Angelescu & Prenski, 1987). This change in the size of mouth, that is related to the trophic habits of M. hubbsi (zooplanktophagous young fish transform themselves into active predators), gives C. palpzfer a larger area for attachment; thus, in the smallest fish the copepod is exclusively located in the roof of the upper palate. In the intermediate sizes and older fish, it is possible to detect the parasites in the lower palate and tongue (apical, middle and lateral areas). When the copepod is fixed to the lower palate, to the tip and lateral areas of the tongue, its body occupies the space limited by gums and tongue. It may be noted, bearing in mind the percentage of copepods found in each of the above mentioned areas, that the region C. paZpifer prefers is that of the upper palate. The roof of the upper palate, with the form of a vault, allows the parasite to withstand the pressure of food passing through the mouth of the fish. The other regions with a lower percentage are probably less adequate for the development of the copepod’s life cycle. The main risk factor for the parasite in the lower area of the buccal cavity would be that of the tongue rubbing the gums. Copepods attached to the gum of the lower palate and to the lateral and apical areas of the tongue would be subject to the rubbing. The space between the tongue and gum is narrower in the lateral areas than in the zone around the tip of the tongue; thus, the parasites attached to the lateral regions of the tongue and to the base of the gum are more exposed to rubbing; however, percentages corresponding to the lower palate are markedly higher than those for the lateral areas of the tongue (Table 2). This might be due to the fact that, for the first case (base of the gum) the attachment area remains stable and with no change in its form, whilst in the second,
1013
the attachment area (tongue) moves during the rubbing. Such a disturbance that would affect the attachment organ of the crustacean-the modified, hook-like second antennae do not penetrate deeply into the tissues of the buccal cavity-plus the rubbing, the narrowness of the space occupied by the parasites body and the pressure of food ingesta by the host, would increase the possibility that the copepods were removed from the buccal cavity. N. insidiosa f. lageniformis showed a decrease in infestation levels with the increase in the size of hake. Fernandez (1985) obtained similar results for the same species parasitizing Merluccius australis in Chile and Shotter (1973) also reported a decrease in infestation with Clavella (another member of the family Lemaeopodidae) with increasing age of whiting Odontogadus merlangus in the vicinity of the Isle of Man. The low infestation levels could result from the increase in the strength of the respiratory current in older fish or from the immunological response of adult fish (Shotter, 1973). The increase in the strength of the respiratory current would render difficult the attachment of the copepodids and they would be dislodged from branchial arches, thus preventing the necessary reinfestation to maintain the population of the parasite. On the other hand, common hake adults progressively lose the filtration capacity of the first branchial arch, thus reducing the growth rate of the distance between the gill rakers which is important for the selective and retention functions of zooplankton species in the young hake (Angelescu & Prenski, 1987). These observations coincide with the lowest prevalence and intensity values of N. insidiosa f. lageniformis, which would seem to indicate a close relationship between the hake’s filtering system and the attachment of copepods to the branchial arch. Probably, copepods are held by the filtering system of the fish, thus favoring their attachment to gill rakers and branchial arches. It should also be noted that the first branchial arch is the one that shows the highest percentage of copepods (80.29) and it is in this arch where the gill rakers of the hake’s filtering system are located. The same preference for the first branchial arch was observed by Sankurathri, Kabata & Whitaker (1983) in N. insidiosa f. pacifica parasitizing Merluccius productus. N. insidiosa f. lageniformis distribution showed a marked preference for the inferior area of the branchial arch: in that area, copepod percentages were near 100% in the smallest sizes (Table 3). In adults, the increase in the length of the branchial arch would facilitate the attachment of the parasite in the middle and superior areas (the attachment in these areas could be difficult in smaller fish due to the reduced length of the branchial arch and because of the presence of another parasite in the inferior area). In addition, the density increase could mean there is more competition for the inferior area, thus causing more copepods to move toward the superior zone of the branchial arch.
J. A. ETCHEGOIN and N. H. SARDELLA
1014
Distribution and site preferences of parasites in gill arches, gill filaments and branchial cavity have also been reported by Kabata (1959) and Rohde (1976, 1977, 1984). Seasonal effects on N. insidiosa f. lagen$ormis infestation levels might be the result of a change in the population structure of the hake due to the winter trophic migration of juveniles within the ArgentineUruguayan Common Fishing Zone (Angelescu & Prenski, 1987) and to reproductive migration of adults toward the spawning area on the Patagonia coast. Sankurathri et al. (1983) also found seasonal differences in N. insidiosa f. pac$ca. The authors related these findings to a decrease in the female population of the parasite because of mortalities during the autumn. Rey & Cascudo (1986) cite the seasonal effects on the prevalence of N. insidiosa f lageniformis but they do not mention any difference in infestation levels in relation to the sex of M. hubbsi. The differences as noted in this paper might be due to the migratory movements that were mentioned above, or to the size and sex composition of the samples. Acknowledgements-We gratefully thank Ph. D. Armand Kuris, University of California, Santa Barbara and Dr Mario George-Nascimento, Pontificia Universidad Cat6lica de Chile, Talcahuano, for their valuable suggestions. REFERENCES ANGELESCU V. & PRENSKI L. B. 1987. Ecologia
t&c8 de la merluza corntin (Merluccidae, Merluccius hubbsi). Parte 2. Dinamica de la alimentacibn analizada sobre la base de las condiciones ambientales, la estructura y las evaluaciones de 10s efectivos en su Brea de distribucibn. Contribuci6n de1 Instituto National de Investigacidn y Desarrollo Pesquero (INIDEP), Mar de1 Plata, No. 561. BELLISION. B., LOPEZ R. B. & TORNO A. 1979. Peces marinos patagbnicos. Publicaci6n de la Secretaria de Intereses Maritimos. Editorial Codex, Buenos Aires. BRIAN A. 1944. Cop&podos parasites de peces y cetaceos de1 Museo Argentino de Ciencias Naturales. Anales de1 Museo Argentina de Ciencias Naturales 41: 193-220. EXHEGOIN J. A. 1988. CopCpodos parisitos de Merluccius
hubbsi. Seminario de Investigacidn. Universidad National de Mar de1 Plata. FERNANDEZJ. 1985. Estudio parasitol6gico de Merluccius australis (Hutton, 1872) (Pisces: Merluccidae): aspectos sistemiticos, estadisticos y zoogeogr8ficos. Eoletin de la Sociedad Biolbgica de Conceptidn, Chile 56: 31-41. KABATA Z. 1959. Ecology of the genus Acanthochondria Oakley (Copepoda, Parasitica). Journal of the Marine Biological Association of the United Kingdom 38: 249-261. KABATA Z. 1979. Parasitic Copepodr of British Fishes. The Ray Society, London. KABATAZ. &Ho J. S. 1981. The origin and dispersal of hake (genus Merluccius: Pisces: Teleostei) as indicated by its copepod parasites. Oceanographical Marine Biology Annual Review 19: 381404. REY M. & CASCULXJJ. 1986. Relaciones entre parasitism0 y comportamiento biolbgico de la merluza (Merluccius hubbsi). Publicacibn de la Comisicin TPcnica Mixta del Frente Maritimo 1: 240-25 1. RINGUELET R. 1947. Anotaciones sobre coptpodos e is6podos parlsitos de peces. Notas del Museo de La Plata Zool., No. 98, Vol. 12, pp. 92-107. ROHDE K. 1976. Monogenean gill parasites of Scomberomorus commersoni Laceptde and other mackerel on the Australian East Coast. Zeitschrift fiir Parasitenkunde 51: 49-69. ROHDE K. 1977. A non-competitive mechanism responsible for restricting niches. Zoologischer Anzeiger 199: 164172. ROHDE K. 1984. Ecology of marine parasites. Helgolander Meeresunters 37: 5-33. SANKURA~HRIC. S., KABATA Z. & WHITAKER D. J. 1983. Parasites of the Pacific hake, Merluccius productus (Ayres, 1855) in the Strait of Georgia, in 19741975. Syesis 16: 522. SHOTTERR. A. 1973. Changes in the parasitic fauna of the whiting, Odontogadus merlangus L. with the age and sex of the host, season, and from different areas in the vicinity of the Isle of Man. Journal of Fish Biology 5: 559-573. SOKAL R. R. & ROHLF F. J. 1979. Biometria. Principios y metodos estadisticos en la investigacicin biokigica. Editorial Blume, segunda Edicibn, Madrid. SZIDAT L. 1955. La fauna de parisitos de Merluccius hubbsi Mar. coma caracter auxiliar para la soluci6n de problemas sistematicos y zoogeogrLficos de1 ginero Merluccius. Comisidn National de Investigacidn de Ciencias Naturales “B. Rivadavia”, Zoo1 3: 54.