Parasites and cephalopod fisheries uncertainty ... - Springer Link

Rev Fish Biol Fisheries (2007) 17:139–144 DOI 10.1007/s11160-006-9021-y

ORIGINAL PAPER

Parasites and cephalopod fisheries uncertainty: towards a waterfall understanding S. Pascual Æ A. Gonza´lez Æ A. Guerra

Received: 10 February 2006 / Accepted: 6 November 2006 / Published online: 6 April 2007 Springer Science+Business Media B.V. 2007

Abstract Recent work provides strong evidence of the role of parasitic diseases as contributing predictors to the variability found in cephalopod growth and condition, from the molecular to population levels. Parasites (both micro and macro) impair the wellbeing of cephalopod populations by diminishing the nutrient absorption capabilities of infected animals. Parasites produce mechanical lysing of large areas of functional tissues and they also deplete energy stores, which are directed towards tissue repair and the host’s defence mechanisms. This review focuses on the impact of parasitic infection as an environmental stressor and thus as a source of uncertainty in cephalopod populations within an ecosystem-based fishery management (EBFM) model. Keywords Cephalopod Cephalopod fishery Parasites Population dynamics Waterfall approach

Introduction A full range of approaches have recently been used to incorporate multiple uncertainty or variability into fisheries work and ecosystem management (Patterson et al. 2001). Three sources of uncertainty are thought S. Pascual (&) A. Gonza´lez A. Guerra ECOBIOMAR, Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, 36208 Vigo, Spain e-mail: [email protected]

to create risks for exploited populations: variability in population dynamics, inaccurate stock size estimates, and inaccurate implementation of harvest quotas. The issue of uncertainty from a biological perspective should take into account multiple sources of variability, which in fact, in turn, makes the world’s fisheries highly variable in terms of recruitment and production. Within the sources of environmental variability the contribution of parasitic diseases on the productivity and marketability of infected cephalopod stocks has not been previously emphasized in fisheries management literature. Herein, we provide a review of the complex effects of parasites as predictors of uncertainty or variability in cephalopod population dynamics. This complex problem can be approached by breaking it up into conceptually manageable pieces, which correspond to the different hierarchical levels of biological systems (namely from the molecular level to the population level). At this point it must be said that the scientific effort dealing with cephalopod parasites and associated pathology related to the relative nominal catch by this group of species represents less than 54% of that on parasitic diseases of other commercially important invertebrates and marine fish (Pascual and Guerra 2001). We summarize and illustrate the epizootiological status of cephalopod populations by updating new and recently published information on various cephalopod-parasite systems in order to give an overall picture of the cost of harbouring parasites.

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The cephalopod-parasite systems The occurrence of parasites in many species of cephalopods is common in all major oceans and seas, from coastal and shelf species to oceanic and deep-sea (Hochberg 1990; Pascual et al. 1996; Lo´pez-Gonza´lez et al. 2000). This fact is not surprising considering the widespread distribution of different parasite phyla worldwide (Rohde 1993), and that cephalopods are a key trophic element in marine communities (Clarke 1996). It has been Fig. 1 Illustration of the more prevalent and pathogenic etiological agents of wild cephalopod populations showing their preferred sites of infection

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Rev Fish Biol Fisheries (2007) 17:139–144

shown that all known exploited species of cephalopods harbour parasites, which might well illustrate the important role of these marine molluscs as a trophic bridge for parasite flow in marine ecosystem (Abollo et al. 1998). (Fig. 1). The natural tendency of an open system (as they are in the majority of cephalopod-parasite systems) in a given ecosystem is to seek and maintain a condition of ecological balance (i.e., equilibrium or homeostasis) by adjusting both elements of the system to their respective environments. Nevertheless, under different


environmental scenarios, changes in parasite infrapopulations within a cephalopod species can produce a destabilizing effect, which does not result in homeostasis. If homeostasis is not restored, or while the system is gradually recovering its equilibrium, the impairment of the normal state or functioning may produce diseases from acute to chronic characterized by an identifiable group of signs or symptoms, (i.e., pathological conditions) which define the epizootiological status of a given cephalopod stock.

The Epizootiology of cephalopod-parasite systems The Epizootiology of cephalopods is concerned with the origin, frequency, distribution, development and determinants of cephalopod health and disease at any place, time and hierarchical level of biological organization. It covers two important aspects, namely: etiology and pathological condition. Etiology Our understanding of the epizootiology of many parasitic species in cephalopods is severely hampered by the existence of phenotypic characters that are difficult to interpret. The existence of unstable anatomical and meristic characters (e.g., in coccidians), cryptic species (e.g., in anisakid nematodess) or morphotypes (e.g., in cestodes) present particular difficulties because of the plasticity of body structures in most of the 200 endoparasitic species reported in cephalopods (Hochberg 1990). In fact, most of these parasites (and even their hosts) have not been taxonomically identified to species level, with high rates of synonymy (close to 70%) for numerous nominal parasite species or larval stages identified by light microscopy. Molecular techniques are now being applied as useful complementary taxonomic tools for parasite diagnosis and their specific identification in cephalopods (e.g., Abollo et al. 2001; Brickle et al. 2001). This also will allow us to elucidate and re-evaluate the taxonomic status and host–parasite relationships of many previously reported cephalopodparasite systems. Pathological condition Diseases and pathology caused by microparasites on wild and cultured cephalopods have been reported in

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a few cases. Parasitic infection by the eimeriorin coccidian genus Aggregata (Protozoa:Apicomplexa) has been noted as the most important etiological agent in cephalopod populations (100% prevalence and up to 82 · 106 sporocysts/g infected tissue in endemiotopic areas) (Gestal 2000). Histopathological studies on infected tissues of cephalopods showed a high degree of invasiveness and pathogenicity (Fig. 2) (Pascual et al. in press). These intracellular parasites produce hypertrophy and degradation of infected cells with distension of the infected tissue area, rupture of the basal membrane and a breakdown of junctions among epithelial cells (Gestal et al. 2002a). Severe loss of epithelial cells and atrophy of mucosa folds occurred in the infected organs. In heavy infections large areas of cephalopod tissue were replaced by parasites, with partial or total destruction of tissue architecture. Although enteric coccidiosis is not believed to be the primary cause of death, severe infection by Aggregata spp. may weaken the cephalopods, making them more vulnerable to other biotic and abiotic stressors. Gestal et al. (2002b) noted that Octopus vulgaris cultured in an open-water culture system infected with Aggregata octopiana showed evidence of a malabsorption syndrome resulting from parasitic infection. This detrimental effect on gastrointestinal function as a result of parasitic-caused acidification of infected lumen may be the cause of a decrease or malfunction of absorption enzymes (e.g., maltase and leucineaminopeptidase), and massive increase of lysosomal activity as revealed by the variation in acid phosphatase activity. Additionally, the ratios RNA/DNA and RNA/protein from the mantle muscle tissue of infected octopods revealed significant decreases in relation to the infection level (as expressed by the number of sporocysts per gram of infected tissue and the total number of sporocysts per whole infected organ) (Gestal 2000). Furthermore, the diminution of the concentration of plasmatic protein and the number of circulating haemocytes as the infection intensity increases may explain the synchronicity of absorption between all the above changes in the infected epithelium and the observed decrease (up to values of r2 = 0.58) in the condition (K-Fulton index) in heavily-infected octopus populations. Other important pathological conditions are due to macroparasites infecting the digestive tract and gills of cephalopods (Fig. 2). Histopathological analysis

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Fig. 2 Cellular/tissular impact of different parasites (p) on cephalopod condition. (A) Gross pathological condition showing numerous oocysts of Aggregata octopiana (arrows) infecting several organs of Octopus vulgaris. (B) SEM image of emerging oocysts (arrows) from the intestine of an infected O. vulgaris. (C) Histological section of an oocyst (oc) located on the connective tissue of an infected caecum of O. vulgaris. (D) TEM image of the sporogonic (sp) development of Aggregata eberthi in Sepia officinalis. (E) Histological section of macro- (mag) and microgametes (mig) on a heavily-infected caecum of O. vulgaris. (F) Large tetraphyllidean cestodes (arrow) which are commonly found free or in the lumen of the digestive tract of squids. (G, H) Histological sections of a larval nematode infecting the intestine of Eledone cirrhosa. (I) Histological section of a larval spiruroid nematode infecting

the digestive gland of O. vulgaris. (J) Histological section of anisakid larvae infecting the stomach of Illex coindetii. (K) Gross pathological condition showing numerous anisakids (arrows) infecting several organs of Todaropsis eblanae. (L) Histological section at higher magnification of the infected stomach as in Fig.2 J. (M) Histological section of a parasitic copepod (Pennella sp.) infecting the gills of I. coindetii. (N) Histological section of Genesi vulcanoctopusi (Copepoda:Tibsidae) on the mantle musculature of the hydrothermal vent Vulcanoctopus hydrothermalis. In all cases (both intracellular and tissular parasites) a marked pathogenic effect was observed in infected cells and tissues, comprising cell atrophy, nucleus displacement and lyses, host inflammation by hemocytes (hc), fibrosis (f), mature capsules (cp), necrosis, disruption of tissue architecture and replacement of large areas of host tissue

on heavily infected individuals revealed alteration of tissue architecture, encapsulation, fibrosis and necrosis (Pascual et al. 1995; Pascual et al. 1996). Furthermore, the effect of gill parasites (i.e., postembrionic stages of siphonostome copepods of the

genus Pennella) on condition (Pascual et al. 1997) and size-at-age data (Pascual et al. 2005) of heavilyinfected (up to 700 parasites on a gill lamella) exploited squid populations suggest the existence of causal relationships between parasitic infection and

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stock productivity. Pascual et al. (1998) noted an important economic loss in the Galician fishery of the ommastrephid stocks due to the effect of this parasite, with a reduction up to 21% on the condition of the squid stock.

Concluding remarks Although parasites are not as well understood as are the many other sources of stock uncertainty, the pathological conditions described above suggest that costs of harbouring parasites and parasitic-caused diseases have obvious ecological consequences for exploited populations. One principal frustration in discussing the effects of parasite infection on cephalopod uncertainty continues to be the inability to quantify the ecological impact of such effects in wild and cultured populations. Host–parasite systems are characterized by highly complex and non-linear interactions among a large number of individual elements organized along hierarchical levels. Such complexity leads to the emergent properties and unexpected dynamics of host–parasite systems, complicating our ability to understand and predict the impact of parasitic disease on cephalopod prognosis. A waterfall approach may aid to review the consequences of parasitism through multiple levels of biological organization by providing discrete, easily understandable and explainable ‘‘phases’’ and markable ‘‘milestones’’ in the disease process. The advantage of a waterfall approach is that it allows for departmentalization and managerial control in complex systems research. As a whole, the cascading parasitic effect in a multi-level hierarchical approach reveals that the relationships between host condition and parasite infection is revealed as a tissue energy balance (trade-off) between energy intake and exposure to parasites. Those heavily-infected cephalopods will show low condition as a result of common energy being directed towards tissue repair and host defence mechanisms. Although an unconsidered source of uncertainty in cephalopod fisheries, the costs of being severely infected suggest that parasitic infection is one of the multiple categorical predictors of the variability found in cephalopod growth and condition. Therefore, further research should be continued on two fronts simultaneously: the first is to investigate the effects of the different parasite

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species on the physiological characteristics and biochemical composition of infected cephalopods under controlled experimental designs which incorporate a hierarchical thinking in biological analysis and ecological interpretation; and secondly, to formulate a waterfall understanding which requires the use of mathematical models in order to determine how parasites can affect the dynamics of exploited cephalopod populations under different environmental and fishing scenarios. Once this research is done, then it would be possible to establish mechanistic links between adjacent levels to address how relationships at cellular and organismal levels influence population, community, and ecosystem-scale processes in cephalopod-parasite systems. Results from these investigations will contribute to a more mechanistic description of how environmental biotic stressors influences cephalopod fisheries uncertainty, a primary goal in the fisheries management. Acknowledgements The ECOBIOMAR group is especially grateful to our colleagues Camino Gestal, Elvira Abollo, Carlos Azevedo, Chingis Nigmatullin, Eric Hochberg, Armand Kuris, Pablo Lo´pez, Stefano D’Amelio, Mario Rasero, Marcos ´ lvarez-Pellitero, Ju-shey Ho, Losada, Lia Paggi, Pilar A Bernardino Castro, Marıá Paez, Jorge Millos, Jesus Mendez, Carmen Serra and Pilar Martinez for their help and numerous suggestions over the last 15 years of studying cephalopod parasites.

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