Changes in prevalence and intensity of infection of Profilicollis altmani (Perry, 1942) cystacanth (Acanthocephala) parasitizing the mole crab Emerita analoga (Stimpson, 1857): an El Niño cascade effect?
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Prevalence and intensity changes in cystacanths of the acanthocephalan Profilicollis altmani parasitizing the mole crab Emerita analoga under El Niño (EN) and non-El Niño (non-EN) conditions are analyzed. Both, mean intensity and prevalence of infection by P. altmani differ significantly for the whole size range and for each size class of 10 mm intervals (except prevalence for size classes exceeding 18 mm carapace length) between EN (1998) and non-EN (2002) years, without observed size distribution differences in the intermediate host E. analoga under either condition. Significant difference in infestation rates of the intermediate host E. analoga is discussed as being an EN cascade effect on predators such as sea birds (i.e., Larus spp. and Calidris sp.), acting as definitive hosts of P. altmani, and which are known to decrease significantly in abundance during EN.
KeywordsENSO Crustacean Parasites Humboldt Current System
As emphasized by Arntz (2002), changes undergone by marine ecosystems during strong El Niño (EN) can be used as a proxy of how these systems may have responded to past climate variability and how they will respond to future changes. Such large-scale climatic fluctuations are known to affect a multitude of ecological processes (Arntz 2002; Fiedler 2002). Climate oscillation, and thus changes in ambient temperature, affects several ecological and physiological processes. This ranges from the performance of individual organisms to the dynamics of populations, including the distribution of species, changes in species dominance and diversity, reproductive biology, population dynamics, and behavior (Arntz 2002; Poulin 2006; Poulin and Mouritsen 2006; Arntz et al. 2006).
Parasites occur in almost every population (Lafferty and Kuris 1999) and parasitism is regarded as one of the most successful ways of life, considering that more than 50% of all living forms are parasites (Windsor 1998). However, despite the strong evidence that parasites can influence the composition and structure of natural communities (Minchella and Scott 1991; Hudson and Greenman 1998) and that parasite transmission is often strongly affected by weather conditions (Mouritsen and Poulin 2002), there are few papers dealing with parasites and changes induced by natural oceanographic phenomena such as El Niño-Southern Oscillation (ENSO).
The mole crab Emerita analoga (Anomura: Hippidae) is dominating soft-bottom intertidal and upper sub-tidal communities along the Pacific coast off South America (Osorio and Bahamonde 1967) and is of great importance in the food web (Koepcke and Koepcke 1952), i.e., being an important prey for fish (both teleost and elasmobranchs) and birds (Larus spp. and Calidris sp.). Alvitres et al. (2002) and Contreras et al. (2000) indicated that E. analoga lives up to 3.5 years in Peru and northern Chile. Parasites of E. analoga include larval forms of the acanthocephalan Profilicollis altmani, the digenean Maritrema sp., the eucestodes Nybelinia sp. and Eutetrarhynchus sp., the nematodes Proleptus sp. and Spiruroidea gen. sp. known from the Peruvian coast (Oliva et al. 1992; Alvitres et al. 1999a). Emerita analoga from northern Chile is a host for larval P. altmani and Proleptus sp. (Oliva et al. 1992), P. altmani being quantitatively the most important parasite. The life cycle of P. altmani was experimentally elucidated by Mateo et al. (1983). In brief, eggs are released from adult worms living in the intestine of gulls of the genus Larus (L. pipixcan, L. belcheri, L. modestus, L. serranus) and Calidris sp. (Oliva et al. 1992). Eggs are filtered by E. analoga and cystacanths develop and encyst in the crab coelomic cavity. The cycle is completed when an infected mole crab is ingested by a marine bird and the cystacanth develops to the adult stage. The cystacanth of P. altmani like other members of Profilicollis is long-lived and probably remains infective throughout the life of the mole crab (Thompson 1985).
In this paper we evaluate the quantitative characteristics of the infection of P. altmani in E. analoga in order to evaluate the potential impact of EN on parasite burden. Specifically, we are discussing whether changes in quantitative characteristic of parasite infection are a direct consequence of EN or a cascade effect.
Emerita analoga in northern Chile
Size class (mm)
Mean size (mm)
Mean intensity (SD in parenthesis) of Profilicollis altmani parasitizing E. analoga during EN and non-EN conditions
Size class (mm)
Profilicollis altmani in E. analoga. Prevalence of infection during EN and non-EN conditions
Size class (mm)
The coastal zone of the Humboldt Current upwelling system is significantly influenced by the ENSO. Both its warm (El Niño: EN) and cold (La Niña: LN) phase have drastic implications for the ecology, socio-economy and infrastructure. ENSO is not only involving the tropical marine realm, but also the global atmosphere. It comprises an unstable interaction between the sea surface temperature (SST) and the atmospheric pressure and results in altered winds, rainfall, thermocline depth, and circulation patterns, strongly impacting the biological productivity, feeding and reproduction of fish, birds and marine mammals (Fiedler 2002) as well as the structure of benthic communities (Rojo et al. 2002; Escribano et al. 2004).
The impact of the last EN (1997–1998) in South America has been well documented (e.g., Peña et al. 2005; Riascos 2006). Mouritsen and Poulin (2002) emphasized that, despite the evidence that parasites can influence the composition and structure of natural communities, parasite transmission is often strongly affected by weather conditions. In the last review of the NAO (Ottersen et al. 2001), the mirror phenomena of EN in the northern hemisphere, parasite–host interactions were not considered at all. A similar picture was evident in the last review of EN impacts in the upwelling zone of the Humboldt Current System (Escribano et al. 2004). Examples of EN-mediated parasite induced host dynamics do however exist: Mouritsen and Poulin (2002) gave a comprehensive list of articles that directly or indirectly showed that parasite-induced host population dynamics or distributions are governed by short-term changes in weather conditions or general climate change. Recently, Mouritsen et al. (2005) demonstrated by evaluating a theoretical model and field data that an increase in water temperature of 3.8°C will likely result in a parasite-induced collapse of an amphipod population. Almost all of the cited articles are related to temperature-dependent effects on emergence and survival of larval stages, egg and larval development, infectivity, and parasite survival in helminths (Monogenea, Digenea, Cestoda, Nematoda). In addition, indirect cascade effects are included and emphasized in relation to the impact of parasites and climate changes on host population and community structure, but the impact of population changes in intermediate and/or definitive hosts of the parasite population remains unclear.
We thank Robert Poulin (Otago University, New Zealand) for comments on the manuscript and Julie Cunningham for her correction of the English. CENSOR is financed through the INCO-DEV-FP6 programme and supported by the European Commission (contract no. 511071). Partial support came from PBCT–CONICYT (Chile) grant CENSOR-RUE02 and Cooperative Program between the Alfred Wegener Institute for Polar and Marine Research and the Instituto de Investigaciones Oceanológicas, Universidad de Antofagasta, Chile. This is CENSOR publication no. 84.