Context dependency of maintenance communities of invasive parasites under climate change: a case study of mussels and intestinal copepods in the Wadden Sea

Abstract

Climate change can impact the persistence of native and invasive parasites and their effects on hosts. Given the complexity of interactions in natural systems, models based on parasite-host systems can be helpful to explore long-term impacts. We investigate how two intestinal parasitic copepods impact host populations, and how the predicted temperature increase by year [Formula: see text] may affect the persistence and impacts of the parasites. We study Mytilicola intestinalis (a specialist established in blue mussels, Mytilus edulis) and Mytilicola orientalis (a recent invader infecting mussels and Pacific oysters, Magallana gigas) in the Wadden Sea. The parasites are non-lethal but can influence host maturation and fecundity. Using a mathematical model parametrized with empirical, field and literature data, we explore how temperature increase affects parasite basic reproduction numbers and the long-term population trends of parasites and mussels. Temperature increase reduces mussel populations below the critical community size for M. intestinalis persistence, while allowing M. orientalis to persist without oysters. M. orientalis does not have a negative effect on the host population in additional to that of M. intestinalis when both are present. We show that environmental change can have qualitatively different effects on related parasites by changing the role of the shared host as a maintenance population.

Keywords: Mytilicola; Mytilus edulis; climate change; ecological modelling; parasite dynamics; population dynamics.

Figure 1.

Structure of the models of the life cycles of (a) mussels, (b) M. intestinalis and (c) M. orientalis. Solid lines indicate maturation of hosts and input of free-living stages, dashed lines indicate reproduction of mussels and parasite stage transitions, dotted lines indicate loss of mussels or parasites.

Figure 2.

Model-derived steady states of the parasite populations at ${10}^{\circ }\text{C}$ as functions of $\mathrm{\Lambda }$, the rate of immigration of M. orientalis. Magenta $(P_U)$ and red $(P_W)$: mean numbers of M. orientalis in immature and mature mussels, respectively; cyan $(P_Q)$ and blue $(P_S)$: mean numbers of M. intestinalis in immature and mature mussels, respectively. Broken lines show M. orientalis values in the absence of M. intestinalis. Filled circles on the vertical axis show M. intestinalis values in the absence of M. orientalis. Parameter values as in tables 1–3 with (a) $\xi =0.0025{\text{d}}^{-1}$, (b) $\xi =0.0030{\text{d}}^{-1}$.

Figure 3.

As in figure 2, but here the values of the steady states of the parasite populations are calculated when $\xi =0.0014{\text{d}}^{-1}$ again as functions of $\mathrm{\Lambda }$, the rate of immigration of M. orientalis. Magenta $(P_U)$ and red $(P_W)$: mean numbers of M. orientalis in immature and mature mussels, respectively. Parameter values as in tables 1–3 with (a) temperature ${10}^{\circ }\text{C}$, (b) ${15}^{\circ }\text{C}$.

Figure 4.

On the vertical axis are the values for the mussel steady states ($I+M$, total immature and mature) at indicated water temperatures and maturity rates $\xi$, relative to the baseline value of an uninfected population at ${10}^{\circ }\text{C}$ and $\xi =0.003{\text{d}}^{-1}$. Values are `$0$' (green): infection free; `$in$' (blue): with M. intestinalis only present in the population; `$or0$' (orange): with M. orientalis only and $\mathrm{\Lambda }=0$; `$or$' (red): with M. orientalis only and $\mathrm{\Lambda }=0.25\ell .{\text{d}}^{-1}$; `$io$' (purple): with both parasites present in the population and $\mathrm{\Lambda }=0.25\ell .{\text{d}}^{-1}$. A striped entry indicates ${\mathcal{R}}_{in}<1$, ${\mathcal{R}}_{or}<1$, or both as appropriate, meaning that the parasite is not present in the steady state and thus does not affect the mussel population.

Figure 5.

Graphic summary of our results on the maintenance of M. intestinalis and M. orientalis at the two temperature scenarios. The terminology for maintenance is based on Haydon et al. [8], see also [1]. We depict the situation in which M. orientalis larval immigration from oysters is always present and fixed at a low rate ($\mathrm{\Lambda }=0.03{\text{d}}^{-1}$), and the mussel maturation rate is moderate to high ($0.0025{\text{d}}^{-1}<\xi <0.003{\text{d}}^{-1}$). We focus on the following situations: whether one or both parasite species are present and maintained and how this differs by temperature (10 and ${15}^{\circ }\text{C}$). Mussels are a maintenance host for M. intestinalis at ${10}^{\circ }\text{C}$, but not at ${15}^{\circ }\text{C}$, either alone or in the presence of M. orientalis (first and third columns). The maintenance community of M. orientalis depends on temperature and whether M. intestinalis is present. Mussels and oysters are a maintenance community for M. orientalis at both temperatures when M. intestinalis is absent (second column). When M. intestinalis is present (fourth column), at ${10}^{\circ }\text{C}$ larval immigration from oysters (arrow) is needed to sustain M. orientalis in mussels (hence without oysters, M. orientalis is not maintained in the system). At ${15}^{\circ }\text{C}$, mussels and oysters are a maintenance community for M. orientalis. In addition, the model results suggest that as a single species, mussels are a maintenance host for M. orientalis at ${15}^{\circ }\text{C}$ (i.e. without the influx of larvae from an oyster population).