This week in Helminthology we discussed the seminal studies by Andrew Dobson and his colleagues which were some of the first to document complex long-term host-parasite dynamics between a host and it’s parasite. The study focused on the Red Grouse populations of northern England and Scotland and their ubiquitous parasitic Nematode Trichostrongylus tenius. Nematodes (or roundworms as they’re commonly called) have parasitized nearly all known vertebrate species, along with most every other group of animals, plants, and fungi in the tree of life. Although these parasitic nematodes complete their life cycles within a host, they also have free living stages and rely on low probability events to pass to the next stage of their life cycle. These complex life history strategies have evolved in unison with their particular host, such that nearly all vertebrates on the planet have a specific nematode species that infects them. This includes humans!
In the case of red grouse and T. tenuis studied by Dobson et al., this worm does not simply infect the grouse, but also has a substantial effect on the individual, and population ecology of the bird. So much so that the grouse population cycles observed over decades on the estates where these birds live, have been shown to primarily be caused by infection of the grouse populations with tenuis. Dobson’s papers on this relationship were some of the first to show parasitic infection as the primary driver of population dynamics of a host species in the context of an entire ecosystem. In this blog I document the highlights of the individual, population, and community level studies of this system, and summarize our class discussion of what these studies show, and their implications in the fields of parasitology, ecology and conservation biology across the world.
The overall study of this host-parasite system was divided into three areas of emphasis and was published in three separate studies. These areas of emphasis were: 1) The monitoring of individual grouse and the undertaking of parasite reduction experiments within them, 2) Population dynamic modeling, and estimation of population parameters w.r.t. grouse population dynamics in the context of their infection with tenuis, and 3) a community ecology study focussing on how tenuis infection affects vulnerability of grouse to predation and how these associations can affect grouse populations dynamics.
In the individual study the authors start by emphasizing the long term nature of the study. They then go on to describe the life cycle of the tenuis and its distribution within the grouse. These turn out to be very key features in how the parasite influence the grouse population dynamics. Notably, the tenuis life cycle enters a stage of arrested development over winter months. This characteristic evolved due to the harsh larvel stage environment associated with reproducing during the winter. Since tenuis larvae cannot survive cold temperatures the parasite evolved an arrested developmental stage such that production of eggs within the host does not begin till the following spring. As I’ll outline later, this life history characteristic turns out to have a large influence on the population dynamics of the grouse. Further, Dobson et al. show that the distribution of tenuis among the grouse individuals within a population, although being prolific, tends to be aggregated (or concentrated) in a small number of individuals. In other words, although almost all individuals in the population are infected with tenuis, a small number of individuals carry most of the worm burden. This aggregated distribution of infection also turns out to affect the long term dynamics of the grouse populations affected.
The paper also outlined the effects of infection with tenius on the relative success of the grouse individuals. They found that tenius infection was positively correlated with increased overwinter mortality for the host, increased egg mortality, and increased chick loss. Importantly, since correlations are not always proof of an effect, controlled parasite reduction experiments via the use of anti-parasitic drugs were also conducted on a random selection of grouse to observe the effect of reduced worm burden. The results of these experiments provided proof of the causal negative effect of tenuis infection on grouse survival and fecundity.
After the establishment of these individual based dynamics in this host-parasite system, the authors then went on to tackle an understanding of how these characteristics actually influence the dramatic population level dynamics observed in grouse populations. Modelling the dynamics of any host-parasite system is no simple process, as managing the birth, death, growth, and transmission rates of two interdependent species over time dramatically increases the number of parameters that need to be taken into account. The figure below models the grouse-tenuis system.
In the above figure we see four population counts: Three being counts of different tenuis life stages (W, A, and P), and H denoting the number of grouse in a population. The rest of the parameters in this figure are simply rates at which we see numbers in these population classes either increase or decrease. Each of these lower case parameters represents a rate of loss or gain to one of these populations through some biological process, be it growth/entry to the next stage of a life cycle (eg. β,λ) or birth (eg. a), or death in a specific environment (ϒ). Once a complex life cycle model such as this is built, if done properly, it can then be used to estimate the effects of certain conditions/changes on the model system. That being said, the obvious challenge associated with population dynamic predictions is the accurate estimation of the parameters outlined in the model!
Dobson et al ambitiously attained parameter estimates from a range of different studies. In doing so they were then in a position to assess the effects changing certain parameters of interest in an attempt to elucidate the true nature of the grouse-tenuis population dynamics. In particular, they found that when the model accounts for a strong negative effect on fecundity due to tenuis infection (δ), grouse population numbers (H), as well as tenuis population numbers (P), tend to cycle dramatically. Further, when the arrested developmental stage (A) is taken into account, the length of these cycles is increased substantially. Indeed the cycles predicted by the large effect on fecundity with arrested development model setting, are similar to actual population fluctuations observed by the researchers. Thus, it was concluded that the time-delayed impact of tenuis on fecundity of grouse was the root cause of sustained population cycles observed in grouse. The scientific impact of this conclusion should not be understated. This was a pioneering and paradigm shifting result in a scientific community infamous for ignoring the often inconspicuous role that parasites play in the population dynamics of their hosts.
From here, Dobson et al. then extended their study to the community level of the grouse-tenuis system. Building on the individual life history characteristics of tenuis, and the pathology of tenuis infection in grouse, in addition to the dynamics characterized in the population level study, the researchers then asked the question if tenuis increased the grouse’s vulnerability to predation. Further they also addressed the consequences of these results on grouse population dynamics.
The authors found that grouse killed by predators had significantly greater worm burdens than grouse shot by hunters. Further they found that populations of grouse in areas of intense predator control showed higher levels of tenuis infection. As a result if was concluded that predators selectively prey on heavily infected grouse. This conclusion was then tested experimentally by observing the rate at which hunting dogs could locate treated vs untreated grouse. It was found that, due to the excessive scent of heavily infected grouse, dogs could much more readily locate infected grouse. The figure below shows the different distributions of parasites depending on the cause of death of the grouse. Shot grouse yielded substantially fewer worms than those killed by predators.
The ramifications of these finding were then modelled into the grouse-tenuis population dynamics already characterized, and it was revealed that predators can have some counter-intuitive effects on the system. Most interestingly the model predicts that in situations of selective predation on heavily infected grouse (which experimental results show), a moderate amount of predation can actually increase the size of host populations! Intuitively this can be explained through the increased survival and fecundity of grouse resulting from lower worm burdens achieved through the presence of predation.
As a whole, much can be taken away from the findings of grouse-tenuis host-parasite system. Their publication in the early 90s were some of the first to shed light on the extent to which parasites influence the structure and dynamics of ecosystems. The findings of this particular study can no doubt be extrapolated to countless other ecosystems around the world. In the discussions that followed in the class dedicated to these studies, it was agreed among students that it is often difficult to realize the extent to which parasites may be influencing ecosystems. Subtle effects on host fecundity, among other inconspicuous effects, are likely to blame for this difficulty. Students were also in agreement that the somewhat provocative policy implications for wildlife management and conservation are extremely important, but yet are often overlooked by managers. Notably, these models suggest predators play a key role in regulating the effects parasites have on the population dynamics of their host, and as a result predators can help sustain and stabilize a healthy host population. From a conservation perspective, it’s clear that in an ecosystem there is much more going on than meets the eye.
Contributed by Andrew Rezansoff