Long-term survey of key macrobenthic species in a temperature eutrophic estuary and the influence of trematode parasites

Abstract

One of the main purposes for the present work is to identify and investigate the influence of digenetic trematodes on the estuarine isopod Cyathura carinata, plus to describe temporal patterns of prevalence and intensity of these parasites in the populations of their intermediate macroinvertebrate hosts. It is also intended to assess the population dynamics of C. carinata through a period of almost 10 years, in a eutrophic estuary, the Mondego Estuary, located in the mid-Atlantic coast of Portugal, where an environmental rehabilitation programme was implemented. This work will be presented in several chapters, corresponding to different manuscripts being prepared, submitted or already published in scientific journals. Initially, there is a brief introduction to the need of developing management strategies, with the purpose of achieving a sustainable utilisation of coastal resources. In this section, some of the most important types of environmental pressures in coastal zones are mentioned, namely eutrophication processes. In this scenario, some of the problems that affect the Mondego Estuary are addressed. C. carinata is presented as one of the intertidal macrobenthic key-species and there is a first approach to the possible role of digenetic trematodes. The first chapter is dedicated to the identification of digenetic trematodes infecting C. carinata (second intermediate host of these parasites) and to the description of trematode patterns from two key sites in the estuary: a Zostera noltii bed and an inner eutrophic sand flat. Two trematode species were dominant: Maritrema subdolum and a hitherto unknown Levinseniella species, the latter being the most frequent one. Generally, the prevalence of both species peaked during winter months, when migratory water birds occurred in the estuary. Isopods from the Z. noltii bed harboured more infections per specimen than those from the sand flat. A much higher density of Hydrobia ulvae mud snails ≥ 2 mm (first intermediate host) and a low abundance of C. carinata were indicated as the most probably motives for this pattern. The second chapter refers a short-term microcosm experiment, conducted with the microphallid trematode M. subdolum and both of its intermediate hosts: H. ulvae and C. carinata. Results indicated that small-scale factors, such as differences in substratum and associated features, may have considerable impact on infections of host populations. C. carinata from a fine sand substratum, with a higher proportion of particles < 125 μm, were more surface active and hosted significantly more M. subdolum parasites than isopods from another fine sand sediment type. There were no parasite-induced effects on the hosts during this short-term experiment. M. subdolum distribution within C. carinata showed that the cercariae primarily penetrated through the isopod’s ventilation structures and afterwards located themselves in the middle- posterior region of the host’s body. The third chapter is related to a laboratory experiment performed to assess the impact of microphallid trematodes on the survival, growth and fecundity of C. carinata. For nearly 12 weeks, infected and non-infected isopods were kept at 25oC. Regardless of the mechanisms involved, microphallids showed that they may have severe consequences, through negative effects on survival, growth and fecundity of their hosts. For species with direct development, such as C. carinata, parasite induced reproduction failure may contribute to temporal fluctuations of abundance. Consequently, it was recommended to include parasites as an important factor influencing host populations from shallow-water ecosystems. The fourth chapter is dedicated to the identification of digenetic trematodes also found within H. ulvae mud snails from the Mondego Estuary. These parasites belonged to the families Haploporidae, Plagiorchiidae, Echinostomatidae and Microphallidae. Higher prevalence occurred in autumn/winter (4.3%) and again in spring (3%), decreasing until 1% in summer, which corresponded to 800 - 5 440 infected mud snails per m2. Digenetic trematodes were found in mud snails from size classes between 2.0 and 5.9 shell Abstract vi height and those > 5.9 mm were non-infected. The parasitised H. ulvae had generally thin shells, very easy to crush, with large and round whorls, fouled by epibionts. The fifth chapter regards the infection characteristics and transmission strategies of the two most common trematodes found in C. carinata: M. subdolum and Levinseniella sp.. Two short-term experiments were performed to compare their transmission success from H. ulvae to C. carinata. Both microphallids penetrated the isopod through the pleopods and encystment took place in the middle-region of the host’s body. The two parasites showed different strategies with respect to cercarial production and dispersal ability (cercarial behaviour). M. subdolum produced a high quantity of swimming cercariae, whereas Levinseniella sp. created few crawling free larval stages. These results can be interpreted as adaptations to different crustacean hosts. The strategy exhibited by Levinseniella sp. is more efficient to infect C. carinata, a relatively quiet bottom-dwelling isopod. The sixth chapter focus on the population dynamics of C. carinata at the Mondego Estuary, from 1993 to 2002, to assess the development of a restoration programme for the seagrass beds of Z. noltii endangered by eutrophication. The mitigation measures implemented since 1998 have contributed to a more stable C. carinata population density at an inner unvegetated sand flat area, where these isopods were abundant. This species was resilient to the occurrence of macroalgal blooms and floods, although both events have caused dispersion of isopod individuals to other areas of the estuary. Despite the increasing environmental quality in the estuary, C. carinata could not establish itself successfully in rooted-macrophyte beds, in contrast to other common estuarine species (e.g. H. ulvae or Scrobicularia plana) that prospered at all sites (bare sand or vegetated mud flats). Finally, there is a general discussion of the role of microphallid trematodes in explaining the irregular presence of C. carinata at the Z. noltii bed, where the mud snail H. ulvae is a dominant species and all the elements needed to complete these parasites’ life cycles are present. The infection characteristics and parasite effects in their macroinvertebrate hosts are also summarised. The possible full restoration of the intertidal areas to the original Z. noltii coverage is discussed, as well as the possible consequences for the C. carinata population. Relatively to the results obtained in this work, it is suggested that unexpected animal responses to habitat modification, such as parasite-hosts interactions, should also be thoroughly considered in environmental management.