Past, present and future of host-parasite co-extinctions

Abstract

Human induced ecosystem alterations and climate change are expected to drive several species to extinction. In this context, the attention of public opinion, and hence conservationists' efforts, are often targeted towards species having emotional, recreational and/or economical value. This tendency may result in a high number of extinctions happening unnoticed. Among these, many could involve parasites. Several studies have highlighted various reasons why we should care about this, that go far beyond the fact that parasites are amazingly diverse. A growing corpus of evidence suggests that parasites contribute much to ecosystems both in terms of biomass and services, and the seemingly paradoxical idea that a healthy ecosystem is one rich in parasites is becoming key to the whole concept of parasite conservation. Although various articles have covered different aspects of host-parasite co-extinctions, I feel that some important conceptual issues still need to be formally addressed. In this review, I will attempt at clarifying some of them, with the aim of providing researchers with a unifying conceptual framework that could help them designing future studies. In doing this, I will try to draw a more clear distinction between the (co-)evolutionary and the ecological dimensions of co-extinction studies, since the ongoing processes that are putting parasites at risk now operate at a scale that is extremely different from the one that has shaped host-parasite networks throughout million years of co-evolution. Moreover, I will emphasize how the complexity of direct and indirect effects of parasites on ecosystems makes it much challenging to identify the mechanisms possibly leading to co-extinction events, and to predict how such events will affect ecosystems in the long run.

Keywords: Biological invasions; Climate change; Ecological networks; Enemy release; Host range; Host-specificity; IUCN; Indirect competition.

Graphical abstract

Fig. 1

Cumulative number of documented species extinctions according to IUCN (2014).

Fig. 2

Comparison between helminth parasite diversity (for Acantocephala, Cestoda, Monogenea, Nematoda and Trematoda) in vertebrates (amphibians, birds, fish, mammals and reptiles) estimated using, respectively, the approach by Poulin and Morand (2004) (dark grey) and the more recent approach proposed by Strona and Fattorini (2014a) (light grey). Data were obtained from Table 1 in Strona and Fattorini, 2014a, Strona and Fattorini, 2014b, Strona and Fattorini, 2014c).

Fig. 3

Distribution of parasite specificity expressed as the logarithm of host range size in fish (A) and terrestrial vertebrates (B). Data for fish parasites (Acantocephala, Cestoda, Monogenea, Nematoda and Trematoda) were collected from FishPest (Strona and Lafferty, 2012). Data for parasites of terrestrial vertebrates (Acantocephala, Cestoda, Nematoda and Trematoda for amphibians, birds, mammals and reptiles) were collected from the Natural Museum History database (http://www.nhm.ac.uk). Since (as to June 11th 2015) all amphibians in the database are erroneously classified as reptiles, information was corrected using Catalogue of Life (http://www.catalogueoflife.org/). Y-axes indicate parasite species numbers.

Fig. 4

Schematic representation of how parasite specificity and host vulnerability may contribute to the structure of fish-parasite networks according to Strona et al. (2013). Specialist parasites tend to use hosts that are easy to encounter, i.e. hosts (i) persisting over long evolutionary time, (ii) broadly distributed, and/or (iii) locally abundant. These properties are inversely related with host vulnerability to extinction. The presence of a gradient in parasite host specificity could promote the emergence of a nested structure.

Fig. 5

Graph showing the relationship between fish parasite specificity and the corresponding average vulnerability of the hosts used by those parasites. Data were obtained using the same data and procedure as in Strona et al. (2013), computing mean host vulnerability values for different parasite host range classes. Differently from Strona et al. (2013), however, classes were defined using a logarithmic progression instead of a geometric one, resulting in an even tighter relationship between log(host range) and mean host vulnerability (r_s = 0.93; p < 0.05).

Fig. 6

Example of asymmetry of interactions as observed in all host parasite records available from FishPest dataset (Strona and Lafferty, 2012). The graph shows the relationship between the maximum specificity of the parasites using a certain host species, and the parasite richness on that host species. Boxplots correspond to different classes of hosts identified on the basis of the maximum specificity of their parasites. Thus, the first boxplot provides information on parasite species richness of all fish species whose most specific parasite uses just one host. It is apparent that specific parasites tend to use hosts harboring many parasites, while species-poor parasitofaunas are often composed by generalist parasites. Boxes indicate first and third quartiles, whiskers indicate range values, and horizontal lines indicate median values.

Fig. 7

Schematic representation of the possible different parasitological consequences of a biological invasion. A: The invader loses its parasite and does not get local parasites; B: The invader loses its parasites and gets new ones from native hosts; C: The invader retains its parasites and these establish new symbioses with local species; D: The invader retains its parasites and acquire new parasites from local hosts; its parasites establish new symbioses with local host species; E: The invader does not lose its parasites, does not get new ones from native hosts, and its parasites do not expand their host range.