Multiscale determinants of parasite abundance: A quantitative hierarchical approach for coral reef fishes
Graphical abstract
Introduction
The importance of being able to successfully model relationships between parasite species abundance and host/environmental variables has long been recognized and remains a fundamental problem in parasitology. Numerous theoretical models have been proposed to explain observed species abundance distributions and epidemiological theories point to several environmental factors and host traits that may affect abundances of macroparasite populations (Anderson and May, 1978). During the last few decades, there have been numerous attempts to identify the key determinants of parasite communities in a variety of habitats and several key variables have been elucidated at either infra-, component or compound community scales (Bell and Burt, 1991, Sousa, 1994, Poulin, 1995, Poulin, 1997, Poulin, 2004, Rohde et al., 1995, Gregory et al., 1996, Sasal et al., 1997, Thomas, 2002, Sikkel et al., 2009). However, despite these efforts, multi-scale quantitative assessment of factors structuring species richness, abundance, community structure and species associations in parasite communities have been elusive (Holmes, 1990). Only a few studies have indeed attempted to quantify the factors influencing parasite communities (Sasal et al., 1999). Defining and quantifying key factors is equally important in determining the effect of scale on parasite communities and processes, and ensuring that predictability in parasite communities is considered (Carney and Dick, 2000). It is, therefore, difficult to assess the relative importance of different host traits and environmental characteristics for the evolution of parasite diversity in general.
Species–environment relationships can be modelled using either individual species or assemblages of species. For individual species analyses, species are independently related to the environmental variables, whereas for community analyses, species are jointly related to the environment using a single model. Thus, community analyses including infra-, component and compound communities are more constrained but much more informative. Many host/environmental variables have been identified as being correlated with parasite species abundance but the relationships generally exhibit high variance. For example, many suitable hosts do not harbour a species due to environmental constraints. Because of this variability, most of the previous analytical techniques have focused on indirect ordinal methods. Ordination methods are one approach to the problem and are designed to arrange individual hosts in a theoretical space so that nearby samples in the space have similar species composition. Associations between the ordination results and environmental factors may then be explored by correlation or regression. Popular methods used for species abundance analysis include principal components analysis (PCA), canonical correspondence analysis (CCA), generalized linear models (GLM), generalized additive models (GAM), multi-dimensional scaling (MDS) and various clustering methods. Traditional ordination methods are widely used for community analyses (Sasal et al., 1997, Sasal et al., 1999, Thomas, 2002, Šimková et al., 2008, Kennedy, 2009) and perform efficiently for well designed parasitological experiments or sampling protocols. However, in view of the possible complexity of interactions among determinants, such exploratory and predictive approaches often fail to find meaningful ecological patterns from complex data. Popular methods are indeed cumbersome to use, sub-optimal or of limited utility in investigating large field epidemiological data sets (including the one analyzed in this study) (De’ath and Fabricius, 2000; Lewis, 2000. An introduction to classification and regression tree (CART) analysis. In: Annual Meeting of the Society for Academic Emergency Medicine. San Francisco, California; De’ath, 2002). There are a number of reasons for these difficulties. First, there are often many possible “predictors” and it is difficult to choose which one to use. Second, the predictors are rarely normally distributed with obvious differing degrees of variation or variance. Third, complex interactions or patterns may exist in the data. These interactions are generally difficult to model and virtually impossible to model when the number of interactions and variables becomes substantial. Co-linearity in the predictors is also a crucial problem as two highly correlated predictors may both appear non-significant even though they explain a significant proportion of the deviance if considered individually. Fourth, the results of traditional methods may be difficult to use in a predictive manner. Environmental variables can be used either directly or indirectly to explain the variability in parasite abundance. When used directly, the species and environmental data jointly determine the variability. When used indirectly, the structure of the species data is first determined and is then related to the environmental data. In most cases, traditional ordination methods neglect direct analysis with very few attempts to investigate direct analytical methods.
Within the last 10 years, there has been increasing interest in the use of classification and regression tree (CART) analysis for complex ecological data that may include lack of balance, outliers, missing values, non-linear relationships between variables, and high-order interactions (De’ath and Fabricius, 2000). This is important as the abundance of parasites may be determined by a large number of interactive factors. Within CART, multivariate regression trees (MRT) are relatively new in ecology (De’ath, 2002) and are virtually unexplored for complex epidemiological field data with multiple response variables and multiple explanatory variables. To date, CARTs have been used rarely by parasitologists for field data (but see Vignon et al., in press).
Among vertebrate hosts, the abundance and richness of the parasite fauna of fish (both marine and freshwater) have been extensively studied (Poulin, 2004). They have contributed considerably to the development of our general understanding of parasitological determinants in aquatic ecosystems. Although parasite diversity in coral reefs has not been thoroughly evaluated (Morand et al., 2000, Muñoz et al., 2007), data generally show that parasite biodiversity in these ecosystems is very high, reaching more than two to 10 times the number of fish species (Rohde, 1976, Lester and Sewell, 1989, Cribb et al., 1994).
This study aims to both introduce and illustrate the use of MRT in order to investigate the determinants of metazoan parasites abundance in a multi-scale quantitative context. To do this, we used new field epidemiological data from 1489 coral reef fishes belonging to two non-related families (Lutjanidae and Serranidae) collected off two Polynesian Islands. Only general trends are presented for each scale analysed. MRT gives us the opportunity to analyse the abundance of the parasite communities at multiple scales and to quantify the relative importance of each factor tested, as well as the impact of major factors on each parasitic taxon. We finally discuss the potential use of MRT by parasitologists as both an explorative and predictive tool.
Section snippets
Sites, host and parasite collection
A total of 1489 coral reef fish representing eight species were collected between 2005 and 2007 during an extensive survey of macro-parasites from two islands in the South Pacific Ocean (Moorea Island, 17°30’S, 149°50’W, Society archipelago, French Polynesia and Ua Huka, 8°57’S, 139°35’W, Marquesas Islands, French Polynesia) (Table 1). Fish were collected using a spear gun from both the inner and outer reefs at depths ranging from 5 to 40 m. Immediately after collection, each fish was
Pattern in parasite abundances
The abundance of parasites sharply contrasted among host individuals. There was on average 26 ± 54 (SD) parasites per fish, belonging to 3 ± 2 parasite species. Fig. 1 shows a composite exploratory tree, allowing overall visual interpretation of both relative importance and interactions among factors at multi-scales. This composite tree provides strong evidence of the complexity of epidemiological data and the synergy (high-order interactions) among several factors. For trees with a single split,
Discussion
Studying parasite diversity and the determinants of this diversity have been one of the major subjects of meta-analyses conducted during the last 10 years in parasite ecology. However, most of the studies considered hosts from different origins, potentially inducing confounding effects because parasites are not equally distributed in the host sampling area. Here, we provided strong evidence that several factors determine parasite abundance, with a prominent role for islands, host species,
Acknowledgements
We are grateful to and thank Dr. Rod Bray for revising this manuscript. The authors thank anonymous reviewers who made valuable suggestions to improve the manuscript.
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