768

J. Parasitol., 86(4), 2000, p. 768–772q American Society of Parasitologists 2000

PROGENESIS IN PROCTOECES LINTONI (FELLODISTOMIDAE), A PARASITE OFFISSURELLA CRASSA (ARCHAEOGASTROPODA) IN A LATITUDINAL GRADIENT IN THEPACIFIC COAST OF SOUTH AMERICA

Marcelo E. Oliva and Laura G. Huaquin*Instituto de Investigaciones Oceanologicas, Facultad de Recursos del Mar, Universidad de Antofagasta, P.O. Box 170, Antofagasta, Chile

ABSTRACT: The fellodistomid Proctoeces lintoni is a common parasite of the gonads of key-hole limpets Fissurella spp. (Ar-chaeogastropoda). It has also been found in the mantle of Octopus vulgaris and as an intestinal parasite of haemulid and gobiesocidfishes. Fissurella crassa, a host for progenetic P. lintoni, can be found from Huarmey, Peru (108S) to Chiloe, Chile (428S).Proctoeces lintoni has been found parasitizing fishes and molluscs from Callao, Peru (128S) to Valdivia, Chile (398S). Progenesisis thought to be a latitude-dependent phenomenon, and high progenesis is expected at higher latitude. In the present article, theassociation between latitude and progenesis was examined over a latitudinal gradient of about 3,000 km. Data suggest thatprogenesis of P. lintoni infecting F. crassa was not associated with latitude. Low levels of progenesis found in the Peruvianpopulation could be a consequence of parasite-induced mortality rather than of low latitude, as would be predicted by the latitudedependence hypothesis.

Proctoeces lintoni Siddiqi and Cable, 1960 is a fellodistomiddigenean that, as an adult, inhabits the gonads of key-hole lim-pets Fissurella spp. (Archaeogastropoda). Adult worms mayalso be found parasitizing the intestine of fishes such as Sicy-aces sanguineus (Gobiesocidae) in Chile and Isacia concep-tionis and Anisotremus scapularis (Haemulidae) in Chile andPeru. Metacercariae have been found in Octopus vulgaris eitherunencysted or encysted in the mantle cavity (Reategui et al.,1989). Proctoeces lintoni (5 P. humboldti and P. chilensis, seeOliva and Zegers, 1988) has been found in Fissurella spp. asfar as 398S latitude.

Almost all the specimens (more than 90%) of P. lintoni hadviable eggs in their uteri and the worm is always progenetic inkey-hole limpets. Although the life cycle of P. lintoni has notbeen elucidated, no developmental stages other than the adultare found in the key-hole limpets; however, sporocysts and en-cysted metacercaria of Proctoeces sp. have been reported in themuricid gastropod Concholepas concholepas from northernChile (Oliva et al., 1999). The plasticity of P. lintoni is com-parable to that of Proctoeces maculatus, which has been foundin at least 59 species of teleosts, 14 species of gastropods, 3species of bivalves, and 1 polychaete (Bray, 1983). Progenesisis defined as the production of viable eggs in specimens inhab-iting an organism that would normally be considered an inter-mediate host. This ability to reach precocious maturity caneliminate the necessity of the normal fish host, allowing matureindividuals to parasitize a wide variety of predatory fishes, in-creasing the opportunities for adaptation to new fish hosts(Manter, 1967; Bray, 1983). Progenesis has been hypothesizedto be a latitude-dependent phenomenon; that is, progenesis ofProctoeces in invertebrate hosts should increase from low tohigh latitudes and may represent a mechanism that enables thespecies to extend into cold waters without dependence on theusual warm-water host (Prevot, 1965; Lang and Dennis, 1976).

If progenesis increases with latitude, then infection of F.crassa by progenetic P. lintoni (measured as intensity and prev-alence) should increase with latitude. Most published demo-

Received 22 February 1999; revised 9 August 1999; accepted 12 No-vember 1999.

* Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile,P.O. Box 2-15, Santiago, Chile.

graphic information on P. lintoni infections in Chilean fissurel-lids does not include host body size. Because prevalence andintensity of infection are closely related to host length, at leastfor F. crassa and F. limbata, (Oliva and Dıaz, 1988, 1992),attempts to correlate latitude and parasitic burden are inade-quate if host size is not considered. In the present article, prev-alence and intensity of infection in F. crassa obtained fromAncon and Ilo (Peru) and Antofagasta and Montemar (Chile)in a latitudinal gradient of more than 3,000 km are analyzedwith consideration of the effect of host body size.

MATERIALS AND METHODS

Samples of F. crassa were obtained directly from local fishermen atAncon (ca. 128S) and Ilo (ca. 178S) in Peru. Chilean samples werecollected by hand from the rocky intertidal zone near Antofagasta(238309S) and Montemar (338S). Twelve samples from Antofagasta weretaken monthly between October 1983 and December 1984. Seven sam-ples from Montemar taken on a monthly basis between July 1996 toJanuary 1997. Five samples were taken from Ancon and 6 from Ilo,both between July 1989 and August 1990 (Fig. 1). In the laboratory,maximum length of host (hereafter HBS) was measured to the nearest0.1 mm. Gonads were isolated and individuals were sexed macroscop-ically according to gonad coloration (Oliva and Dıaz, 1992). Gonadswere dissected and the presence of worms was quantified.

ANOVA was applied to evaluate if HBS and mean intensity differbetween localities; ANCOVA was used to test if trends of intensity ofinfections (log10[n 1 1]) differ in a latitudinal gradient. Differences inprevalence of infection among localities were evaluated with a G-test.Influence of the HBS on prevalence (previous arcsine transformation)was analyzed with the Pearson product–moment correlation coefficient.The statistical criteria for significance was defined at a 5 0.05. Bushet al. (1997) was followed for ecological terminology and SYSTAT(Wilkinson, 1990) was used as the statistical tool.

RESULTS

Key-hole limpets Fissurella crassa (843) were studied. TableI shows date, location of collection, and characteristics of thesamples. The mean HBS differed significantly among localities(F3, 839 5 340.5, P K 0.0001). A Tukey test indicated that spec-imens from Montemar were significantly larger than those fromthe other localities and that they, in turn, do not significantlydiffer in size among themselves. Prevalences differ among the4 localities (x2 5 215.7, P K 0.001, 2 df; pairwise comparison:all significantly different at P , 0.001). ANOVA (F2, 498 533.26, P , 0.001) and a post hoc Tukey test for mean intensity

OLIVA AND HUAQUIN—PROGENESIS IN PROCTOECES LINTONI FROM SOUTH AMERICA 769

TABLE 1. Summary statistics of Fissurella crassa and infection of Proctoeces lintoni in F. crassa.*

F. crassa

Collectiondate Locality n

Body size

x SD

P. lintoni infection of F. crassa

Prevalence (%) CI x SD

Oct 1983Nov 1983Dec 1983Jan 1984Feb 1984

ANTANTANTANTANT

2623252623

41.035.236.646.642.9

8.93.87.0

10.36.5

76.978.384.0

10091.3

16.216.914.4

0.011.5

12.63.88.5

26.210.8

13.52.87.0

26.28.6

Mar 1984Apr 1984May 1984Jun 1984Jul 1984Aug 1984Sep 1984

ANTANTANTANTANTANTANT

24212732293031

43.747.144.548.256.453.844.7

4.97.66.46.16.18.85.6

100100

74.165.686.286.774.2

0.00.0

16.516.512.612.215.4

13.19.15.66.0

14.216.09.1

9.58.45.67.2

21.718.614.8

Oct 1984Nov 1984Dec 1984Jul 1989Sep 1989Feb 1990

ANTANTANTANCANCANC

18341115

913

44.447.356.646.047.444.8

10.06.48.17.58.87.1

72.2100100

0.00.00.0

20.70.00.00.00.00.0

7.421.018.10.00.00.0

7.518.414.60.00.00.0

Apr 1990Jun 1990Jul 1989Feb 1990Apr 1990Jun 1990

ANCANCILOILOILOILO

14214322

581

48.942.443.951.649.345.1

9.35.66.54.73.46.1

0.00.0

27.94.5

80.023.5

0.00.0

13.48.7

35.19.2

0.00.03.81.01.51.7

0.00.04.30.00.61.9

Aug 1990Jul 1996Aug 1996Sep 1996

ILOMONMONMON

30263028

47.465.365.368.2

6.811.412.96.4

16.757.793.371.4

13.319.0

8.916.7

3.04.5

17.06.3

3.96.3

23.611.5

Oct 1996Nov 1996Dec 1996Jan 1997

MONMONMONMON

30353524

69.170.069.365.8

7.68.28.16.9

46.774.351.466.7

17.914.516.618.9

8.15.24.7

10.8

12.15.74.7

16.8Pooled ANT

ANCILOMON

38072

181208

45.845.546.167.6

9.17.76.59.2

85.40

22.664.6

5.106.17.0

12.802.48.5

15.703

14.4

* CI, confidence interval; ANC, Ancon (Peru); ANT, Antofagasta (Chile); ILO, Ilo (Peru); MON, Montemar (Chile).

indicate that mean intensities differ significantly among locali-ties, with a lower value for Ilo and a higher value for Antofa-gasta.

Prevalence was positively and significantly correlated withHBS for Antofagasta (r 5 0.95, P K 0.001, 9 df; Fig. 2a), butnot for Montemar (r 5 0.042, P 5 0.27, 6 df; Fig. 2b) and Ilo(r 5 0.1, P 5 0.85, 4 df; Fig. 2c). Intensity of infection wassignificantly and positively correlated with HBS for Antofagas-ta (r 5 0.32, P K 0.001, 321 df; Fig. 3a) and Montemar (r 50.29, P 5 0.0006, 135 df; Fig. 3b) but not for Ilo (r 5 0.0024,P 5 0.98, 39 df; Fig. 3c).

Key-hole limpets from the northernmost locality (Ancon)were devoid of parasites. As a rule, all parasites found in theother localities were mature forms with viable eggs in utero.ANCOVA demonstrated that intensity of infection does not dif-fer between Antofagasta and Montemar (HBS 3 Locality in-teraction: F1, 456 5 0.028, P 5 0.868). Ilo was not considered in

the ANCOVA because of the lack of correlation between HBSand the intensity of infection.

DISCUSSION

There is no evidence of long-term changes in parasitic pop-ulations (measured as prevalence or mean intensity), at least inthe mollusks infected by progenetic worms such as P. lintoniand P. maculatus. Thus, we do not consider that differences inthe year of collection affected the results. Esch et al. (1997)were unable to detect changes in prevalence of infection duringa 13-yr period in a freshwater guild of larval digeneans. Chang-es of prevalence on a seasonal scale have also been described,mainly for larval forms, but such changes are closely associatedwith behavior of the definitive hosts, such as migratory birds(Lemly and Esch, 1984; Fernandez and Esch, 1991; Galaktion-ov and Bustnes, 1995). These changes are expected when larval

770 THE JOURNAL OF PARASITOLOGY, VOL. 86, NO. 4, AUGUST 2000

FIGURE 1 Approximate position of the 4 localities (Chile and Peru)where samples of F. crassa were obtained. 1, Ancon; 2, Ilo; 3, Anto-fagasta; 4, Montemar

FIGURE 2. Prevalence of infection of Proctoeces lintoni in Fissurellacrassa as a function of host body size in various localities.

forms (but not progenetic worms with viable eggs in utero) arestudied, because their demography depends directly on ecolog-ical characteristics of the definitive host (Huxham et al., 1993).An important environmental factor that must be considered isthe potential biological effect of ENSO (El Nino–Southern Os-cillation) about which little is known (Barber and Chavez,1983). Available information about parasites and ENSO for thePacific coast of South America refers only to the presence ofparasites (Digenea and Monogenea) that invade this zone withtheir fish hosts (Oliva, 1984; Oliva and Munoz, 1985; Luqueand Oliva, 1993).

If we only consider data on prevalence and mean intensityfor the Peruvian samples plus Antofagasta, an association be-tween degree of progenesis (measured as increased prevalenceand mean intensity) and latitudinal gradient is evident. Inclusionof the Montemar data, however, results in a reversal of thistrend because the prevalence and mean intensity of infectionfrom Montemar is significantly lower than in Antofagasta. Be-cause the key-hole limpets of Montemar are significantly largerthan those of Antofagasta, Ilo, and Ancon and HBS is signifi-cantly and positively associated with prevalence and intensityof infection, the highest infection, according to the latitude-dependent progenesis hypothesis, should be observed in Mon-temar. Strong correlation between HBS and prevalence and in-tensity has been reported not only for P. lintoni in fissurellids,but also for many digeneans in molluscs (larvae or progeneticworms) (Shimura, 1980; Sousa, 1983; Jokela and Lively, 1995).In contrast to trends of infection at Antofagasta, those for Mon-

temar and Ilo do not agree with patterns that correlate HBSwith prevalence of infection (Fig. 2a–c). A possible explanationof this phenomenon for Ilo is that this may be a consequenceof the expected low level of infection predicted by the latitude-dependent progenesis hypothesis, but the decreased prevalencein larger individuals also may be considered as indirect evi-dence of parasite-induced mortality, as inferred by Rousset et

OLIVA AND HUAQUIN—PROGENESIS IN PROCTOECES LINTONI FROM SOUTH AMERICA 771

FIGURE 3. Intensity of infection of Proctoeces lintoni in Fissurellacrassa as a function of host body size in various localities.

al. (1996). Thus, low values of prevalence and intensity of in-fection for Ilo could not be associated with the low degree ofprogenesis expected for a latitudinal gradient but probably re-sult from parasite-induced mortality. Alternatively, the parasitemay eventually die after attainment of sexual maturity and dis-appear from the host. Characteristics of infection from Monte-mar do not agree with those expected for the latitude-dependent

progenesis hypothesis. According to the hypothesis, higher val-ues of prevalence and mean intensity would be expected fromthis southern locality. Moreover, according to the correlationbetween HBS and prevalence and mean intensity of infection,higher values may occur, again, in Montemar. Absence of suchdepartures from hypothesized values could be a consequenceof the presence of a suitable fish host for P. lintoni, the gobie-socid Syciases sanguineus, along the latitudinal gradient. Thus,mechanisms to enable the species to extend into cold waterswithout dependence on the usual warm-water fishes are not re-quired.

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