The recruitment of gill-infesting copepods as a categorical predictor of size-at-age data in squid populations

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1 ICES Journal of Marine Science, 62: 629e633 (25) doi:1.116/j.icesjms The recruitment of gill-infesting copepods as a categorical predictor of size-at-age data in squid populations S. Pascual, A. F. González, and A. Guerra Pascual, S., González, A. F., and Guerra, A. 25. The recruitment of gill-infesting copepods as a categorical predictor of size-at-age data in squid populations. e ICES Journal of Marine Science, 62: 629e633. The independent effects of host age and size on the recruitment of the gill-infesting copepod parasite Pennella sp. were examined in the short-finned squid (Illex coindetii) from Galician waters (ICES Areas VIIIceIXa). Older and larger squid had larger parasite infrapopulations, but in general the age of squid described the parasite recruitment to the host population better than did mantle length or body weight of squid. Parasite infrapopulations were markedly clumped or overdispersed in those squid hatchling groups with greater parasite recruitment, indicating close adjustment of host/parasite life cycles. Moreover, the gill infestation did moderate the relationship between age and body weight of squid, though the strength or importance of the variation associated with the relationships is not known. The results show that infestation by pennellids contributes to the variability in squid growth, being one of the multiple categorical predictors of size-at-age data in several infested cephalopod species commercially exploited in European waters. Ó 24 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. Keywords: cephalopod, parasitic copepod, Pennella sp., size-at-age data. Received 17 August 24; accepted 18 December 24. S. Pascual, A. F. González, and A. Guerra: ECOBIOMAR, Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, 3628 Vigo, Spain. Correspondence to S. Pascual: tel: C , ext 183; fax: C ; spascual@iim.csic.es. Introduction Cephalopods are one of the most important commercial marine resources worldwide, with a world capture production of t in 22 (FAO, 24). Stock biomasses fluctuate widely on an annual basis, for many different reasons, some of which are still poorly understood. Cephalopod growth is influenced markedly by environmental conditions, both abiotic and biotic. In the past decade, the study of parasite-induced pathology in wild and cultured populations of ommastrephid squid, octopus, and cuttlefish has improved our knowledge of host/parasite interactions and therefore enabled us to evaluate the effects of parasites on cephalopod productivity. Heavy infestations of enteric coccidians and gill-infesting copepods impair the well-being of cephalopod populations by affecting their condition at molecular, cellular, tissue, and individual levels (Pascual and Guerra, 21). Pascual et al. (1998) estimated an annual economic loss of more than.5 million euros in short-finned squid (Illex coindetii and Todaropsis eblanae) populations taken off Galicia (ICES Areas VIIIceIXa) attributable to heavy infestation by the post-embryonic stages of the siphonostomid crustacean Pennella sp. Size-at-age data are crucial to fisheries stock assessment and management and are also considered to be among the most important population parameters required to monitor fishery performance. Therefore, we believe there may be value in checking whether historical data for a short-finned squid population off Galicia (González et al., 1996) are influenced by the recent knowledge of the recruitment dynamics of its parasites. The hypothesis is evaluated to determine if the prevalence and intensity of the gill-infesting Pennella sp. can be integrated as a categorical predictor for studying sizeeage relationships in squid populations. Material and methods For the analysis, host and parasite sampling is as described by Pascual et al. (21) in their study of the epidemiology of Pennella sp. in post-recruiting Illex coindetii in the northeastern Atlantic. The age of the squid was estimated by reading daily increments in statoliths, following González et al. (1996). Linear equations were fitted to the relationships between squid size (ML, mantle length;, body weight), estimated age (), and infestation intensity (I) estimated at an infrapopulation level from parasite Downloaded from at Pennsylvania State University on March 5, /$3. Ó 24 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.

2 63 S. Pascual et al. counts (). We also calculated parasite intensity in male (n Z 246) and female squid (n Z 191) for each seasonal hatchling group, to ascertain whether parasite infestation correlates with the seasonal differences in growth observed by González et al. (1996). An analysis of covariance (ANCOVA; Zar, 1999) was used to determine whether the gill infestation by Pennella sp. moderates the relationships between age () and size (ML and ) in the exploited squid population. Squid groups were defined as uninfested (group ), lightly infested (1e5 parasites: group 1), moderately infested (51e1 parasites: group 2), and heavily infested (O1 parasites: group 3). Descriptive infestation statistics are as defined by Bush et al. (1997): prevalence of infestation is the number of hosts infested with 1 or more individuals of a particular parasite species divided by the number of hosts examined for that parasite species; mean intensity of infestation is the average intensity (number of individuals of a particular parasite species in a single infested host) of a particular species of parasite among the infested members of a particular host species. A parasite infrapopulation includes all individuals of a species in an individual host at a particular time. Results Recruitment of Pennella sp. to the squid population There were marked sex differences in the accumulation of parasite infrapopulations as squid age increased (p!.5): age-dependent parasite recruitment was more notable in male squid than in females (Figure 1). Characteristically, the age of male squid followed the level of parasite recruitment into the host population better than did mantle length or body weight. In female squid, however, the distribution fit MLe was better than e or e. Parasites first recruited into their squid hosts at a squid ML of 9 mm, and infestation was 1% by a squid ML of 151 mm (ages from 224 d in males, 97 d in females). Mean I peaked in male squid 12e14 months old (age 38e424 d; ML 241e27 mm; I Z 14) and in female squid 7e8 months old (age 262e291 d; ML 211e24 mm; I Z 95). The increase in parasite recruitment with age was also influenced by squid maturity. In males, an enhanced level of accumulation of parasites with increased age was evident for all maturity classes (immature, maturing, mature), but it was more evident in mature squid of ML O 24 mm (p!.5). In females, parasites continued to recruit throughout the immature period of squid growth, but not into maturing or mature squid (p!.1). Parasite recruitment into seasonal hatchling groups Parasite recruitment trajectories can be described by following the linear equations that fit the data best for each seasonal hatchling group (Figure 2). Regression lines e were significantly different (p!.1), indicating a differential age-dependent recruitment of parasites into each group of squid hatchlings. In males, the most notable accumulation efficiency of parasites with increments of squid age was in winter-hatched squid (r 2 Z.6935; p!.1). From an age of 2 d, parasite recruitment was progressively less for later hatchling seasons. In females, the distribution fit e is best described for autumnhatched squid (r 2 Z.4362; p!.1). For both males and females, all squid hatched in winter were infested. Moreover, larger overdispersed parasite infrapopulations (i.e. those having variance to mean ratio, b, O1.) were always observed in the squid hatchling groups exhibiting greater parasite accumulation efficiency with age. Parasite recruitment as a categorical predictor of size-at-age data There were no significant differences between the slopes or the intercepts (p O.5) of the linear regressions eml among infested and uninfested males and females, but the regression lines e in the different parasite groups were not parallel (Figure 3). The slopes of the relationships were greater in uninfested squid than in infested squid (males and females; p!.1). From an age of 2 d, uninfested squid had a greater body weight than moderately or heavily infested squid of the same age. Discussion Recruitment of Pennella sp. into post-recruit squid caught on the continental slope and shelf off Galicia is clearly sizeand age-dependent. Older, heavier squid with larger gills have longer to become colonized by heavier parasite infrapopulations, supporting the infestation recruitment characteristics of most macroparasites in wild marine populations (Rohde, 1993). Nevertheless, parasite recruitment dynamics were markedly different between male and female squid. The number of age increments (days) and mantle length were the best descriptors of parasite recruitment in male and female squid populations, respectively. A possible explanation for this sexual parasiterelated dimorphism may lie in the marked differences in parasite recruitment into squid maturity groups. Parasite accumulation was heavier in mature males and immature females, respectively, so it seems that parasite recruitment is greatest with age increments into mature males and with ML increments into immature females. The differences in recruitment success of the parasite into male and female squid may be related to size at first maturity (González and Guerra, 1996; González et al., 1996), which is greater in females (184 mm ML) than in males (128 mm). Further, from an age of 2 d, infestation peaked in male and female squid of similar mantle length but different age (almost twice the number of increments in males than in Downloaded from at Pennsylvania State University on March 5, 214

3 Gill-infesting copepods and squid size-at-age ML a) b) ML Figure 1. Scatterplots showing the linear regressions between mantle length (ML, mm), total body weight (, g), and estimated age (, d), and the number of copepods (parasite counts, ) in (a) male and (b) female squid. Bubbles of varying size represent the relative frequencies of the number of points represented by a single plot position. The ellipses in the bottom panels show the prediction intervals with 95% confidence. Downloaded from at Pennsylvania State University on March 5, 214 females). This difference may be due to the existence at the time of sampling of squid belonging to different microcohorts (i.e. seasonal hatchling squid groups), which represent a different mixture of squid age classes with different parasite recruitment trajectories. Although recruitment of parasites is a continuum, maximum output of infective stages (the copepodids) and subsequent recruitment into the squid populations was in winter-hatched male and autumn-hatched female squid, perhaps influenced by an evolutionary mating strategy in the parasite life cycle (Pascual et al., 21). Further, it is possible that the observed differences in parasite recruitment (PR) among hatchling groups (5 mm! PR! 8 mm) may be linked to the seasonal upwelling cycles in the sampling area, which are known to influence blooms of zooplankton (Varela, 1992). Overall, the recruitment dynamics of Pennella sp. into squid populations (which play the role of intermediate host

4 632 S. Pascual et al. 2 a) b) W 2 A Su winter spring summer autumn in the parasite s life cycle) are influenced by squid size, age, and seasonal hatchling group. This conclusion could help determine, through monitoring and tracking the infestation prevalence and intensity of Pennella sp. in the final host (mostly large teleost fish of commercial interest, such as swordfish or tuna; Kabata, 1979), their feeding and migration cycles. However, considering the high individual variability in growth rates of squid even among age groups, and the great overlap of cohort groups between age groups year-round (González et al., 1996), the use of such information to bring Pennella sp. in the wild under biological control is a long way off. The ANCOVA results testing parasite recruitment as a categorical predictor of size-at-age data revealed that uninfested squid weighed more than infested squid of the same age. On that basis, it could be that, from an age of 2 d, the recruitment trajectory of gill parasites into the squid population may be influencing individual squid s robustness or condition. This effect of gill parasites contributing to the strength or importance of ageeweight Sp Su A winter spring summer autumn Figure 2. Linear regressions of estimated age (, d) against parasite count (), showing the best fit for each seasonal hatchling group of (a) male and (b) female squid (W, winter; Sp, spring; Su, summer; A, autumn) group group 1 group 2 group 3 relationships seemingly agrees with the earlier finding of Pascual et al. (1997), who noted no significant differences in the growth of a squid population when comparing lengtheweight regression patterns of infested and uninfested squid groups, but a negative effect of gill parasites on the condition (K, Fulton index) of heavily infested individual hosts. The gills of cephalopods are the major sites for respiratory exchange. Therefore, a heavy gill infestation could in some way impair an animal s ability to absorb oxygen and ultimately influence its metabolic rate. However, description of the effect and its quantification is not simple in wild populations. Consequently, physiological experiments on captive cephalopods, measuring oxygen uptake and the functional morphology of their gills, are now being carried out to ascertain more accurately the effect of parasites in cephalopod species of commercial interest, namely Sepia spp., Loligo spp., Eledone spp., Alloteuthis subulata, Todaropsis eblanae, Todarodes sagittatus, and Octopus vulgaris (see review by Pascual et al., 1996). Figure 3. Linear regressions for the relationships between estimated age (, d) against total body weight (, g) in (a) male and (b) female squid groups with different levels of infestation (, uninfested group; 1, lightly infested group; 2, moderately infested group; 3, heavily infested group). Coefficients (r 2 ) for male and female squid groups are: male (group,.8934; group 1,.8845; group 2,.9216; group 3,.867); female (group,.8915; group 1,.2519; group 2,.8387; group 3,.3659). 12 a) 11 b) W Sp group group 1 group 2 group 3 Downloaded from at Pennsylvania State University on March 5, 214

5 Gill-infesting copepods and squid size-at-age 633 Acknowledgements Thanks are due to Dirección Xeral de Investigación e Desenvolvemento (Xunta de Galicia) for providing financial support under Resolution DOGA-April 13, 24, and to Marek Lipiński and an anonymous reviewer for their valuable comments on an early draft. References Bush, A. O., Lafferty, K. D., Lotz, J. M., and Shostak, A. W Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology, 83: 575e583. FAO. 24. Yearbook of Fishery Statistics: 22 Volume 94/1. FAO, Rome. González, A. F., Castro, G., and Guerra, A Age and growth of the short-finned squid Illex coindetii in Galician waters (NW Spain) based on statolith analysis. ICES Journal of Marine Science, 53: 82e81. González, A. F., and Guerra, A Reproductive biology of the short-finned squid Illex coindetii (Cephalopoda, Ommastrephidae) of the northeastern Atlantic. Sarsia, 81: 17e118. Kabata Parasitic Copepods from British Waters. Ray Society, 152. London. 468 pp. Pascual, S., Gestal, C., and Abollo, E Effect of Pennella sp. (Copepoda, Pennellidae) on the condition of Illex coindetii and Todaropsis eblanae (Cephalopoda, Ommastrephidae). Bulletin of the European Association of Fish Pathologists, 17: 91e95. Pascual, S., Gestal, C., Estevez, J., Rodríguez, H., Soto, M., Abollo, E., and Arias, C Parasites in commerciallyexploited cephalopods (Mollusca, Cephalopoda) in Spain: an updated perspective. Aquaculture, 142: 1e1. Pascual, S., González, A., Gestal, C., Abollo, E., and Guerra, A. 21. Epidemiology of Pennella sp. (Crustacea: Copepoda) in exploited Illex coindetii stock in the NE Atlantic. Scientia Marina, 65: 37e312. Pascual, S., González, A., and Guerra, A Effect of parasitism on the productivity of the ommastrephid stocks in Galician waters (NW Spain): economic loss. Iberus, 16: 95e98. Pascual, S., and Guerra, A. 21. Vexing question on fisheries research: the study of cephalopods and their parasites. Iberus, 19: 87e95. Rohde, K Ecology of Marine Parasites. CAB International, Wallingford, UK. 298 pp. Varela, M Upwelling and phytoplankton ecology in Galician (NW Spain) rias and shelf waters. Boletín del Instituto Español de Oceanografía, 8: 57e74. Zar, J. H Biostatistical Analysis, 4th edn. Prentice-Hall, New York. 663 pp. Downloaded from at Pennsylvania State University on March 5, 214