The sicker the better: nematode-infected passalus beetles provide enhanced ecosystem services

Abstract

There is growing appreciation for the role that parasites have in ecosystems and food webs, though the possibility that they could improve an ecosystem service has never been considered. In forest ecosystems, fallen trees naturally decay over time and slowly return their nutrients to the soil. Beetles in the family Passalidae play a key role by excavating tunnels and consuming wood from these logs, thereby breaking down the wood into smaller debris. In the eastern United States, the horned passalus (Odontotaenius disjunctus) is host to a naturally occurring nematode, Chondronema passali, which appears to cause little harm to the beetles. We suspected this was due to compensatory food consumption by parasitized individuals, which we tested here. We collected and housed 113 adult beetles in individual containers with wood for three months, then determined the amount of wood each beetle had processed into fine debris and frass. We then assessed beetles for C. passali and compared wood processing rates between parasitized and non-parasitized groups. Results showed the average daily processing rate of parasitized beetles ($\overline{x}$ = 0.77 g d⁻¹) was 15% greater than that of unparasitized ones ($\overline{x}$ = 0.67 g d⁻¹). Parasitized beetles were 6% larger, and this may explain some of this pattern, though the effect of parasitism was still significant in our analysis. By extrapolating the daily rates, we estimate that 10 adult beetles without nematodes would break down approximately 2.4 kg of wood in a single year, while a group of 10 parasitized beetles would break down 2.8 kg. While our data are consistent with the idea of compensatory feeding, because these results are based on natural infections, we cannot rule out the possibility that beetles with heightened wood consumption are simply more likely to acquire the parasite. At an ecosystem level, it may not matter which is the case; parasitized beetles provide a more effective ecosystem service.

1. Introduction

For the animals in any given ecosystem, their physical performance must depend to some degree on their individual health, since parasites and diseases (usually) reduce mobility and/or motor function [1,2], which would limit their hosts' day-to-day activities. Imagine, for example, if the activities of dung beetles, which have a key ecosystem role in turning animal wastes into organic material [3], were hampered by illness. In fact, this very scenario is playing out now in another insect with a key ecosystem role; parasitic mites and viruses in honeybees are hindering the vital pollination service their hosts provide [4]. However, some cases of parasitism may cause the opposite pattern, by causing their hosts to compensate with increased foraging activity [5], which in theory could translate into heightened productivity within the ecosystem, especially if a large component of their ecosystem role involved their eating habits.

Insects that consume decaying wood provide an important, yet often overlooked, ecosystem service via the mechanical breakdown of fallen logs in forests, which enhances their decomposition rate [6]. Beetles in the family Passalidae exemplify this service [7]; they live their entire lives in decaying hardwood logs, eating the wood and excavating cavities where they raise their young (figure 1). These activities result in the physical breakdown of the logs (either from being consumed or building tunnels) over many years, depending on the number of individuals. Wood processing rates of passalids range from 0.01 g to 0.9 g per beetle, per day [8,9], or as much as five times their own weight per week.

Figure 1.

Horned passalus beetles (Odontotaenius disjunctus) in their natural habitat, a decaying hardwood log in a forest. The beetles excavate cavities to raise young, and they also consume the wood, thus breaking down the log and enhancing decomposition. Note the pile of chewed wood in the burrow (dotted circle). A nematode parasite, Chondronema passali (inset) inhabits the abdomen of this beetle species and can number in the thousands in a single beetle. (Online version in colour.)

In the eastern United States, the horned passalus, or bess beetle, Odontotaenius disjunctus is host to a naturally occurring nematode parasite, Chondronema passali (figure 1), that inhabits their abdominal cavity (but not the gastrointestinal tract) and can number in the thousands within individuals [10]. It is not yet clear how beetles can exist without apparent harm with such extreme parasite burdens. In fact, not only is there little outward harm, but in some field collections, parasitized individuals are actually larger than those without this nematode [11]. Other studies have indicated that beetles with C. passali do not lose as much weight when stressed [12]. Such observations led us to suspect this parasite causes compensatory food consumption by the host. This phenomenon occurs in a wide variety of other host–parasite cases, including caterpillars infected with viruses [13], beetles infected with tapeworms [14] and damselflies infected with bacteria [15]. We tested this idea here with a simple yet convincing laboratory experiment where we assessed wood breakdown rates of horned passalus beetles with and without C. passali nematodes, and then relate this information back to the ecosystem service provided by these beetles.

2. Material and methods

(a). Beetle housing and wood processing

In January 2018, we collected a total of 113 adult O. disjunctus from a wooded location near the University of Georgia campus (Athens, GA, USA). Collection involved locating moist, decaying hardwood logs (figure 1) and extracting beetles with hand tools. Importantly, we also collected large sections of wood from the same log. In the laboratory, beetles were placed individually into plastic pint containers with an intact piece of (moist) wood from its log as a food source (electronic supplementary material, file S1). The containers were not disturbed thereafter, except for occasionally misting the contents to maintain high humidity. After three months, we determined the amount of wood each beetle had broken down into fine material (electronic supplementary material, file S1). We used a plastic sieve (with 3 mm diameter holes) to sort the contents of the container, separating the small wood bits, frass and debris from the remaining, larger, wood pieces. We then weighed the filtered portion with an electronic balance. This allowed us to gauge how much cumulative wood had been broken down, or ‘processed’ by each beetle over the three months and then to calculate its processing rate per day (weight of wood debris/number of days).

(b). Parasite assessment

At the end of the experiment, each beetle was weighed, killed with alcohol and dissected under low-power magnification to determine gender (by the presence of the male aedeagus) and the presence of Chondronema passali nematode parasites. This parasite inhabits the abdominal cavity and is easily observed, especially in freshly killed specimens (figure 1). While the intensity of infection varies across individuals, for our purposes, we were only concerned with whether or not the parasite was present. Note that results of our analyses were qualitatively similar whether we used intensity of infection or presence–absence of nematodes (electronic supplementary material, file S2).

(c). Data analyses

The variable of interest in our study was the individual wood processing rate (g d⁻¹), which was normally distributed (electronic supplementary material, file S2). We examined predictors of this rate using a general linear model, with main effects being beetle sex, parasite status (infected or uninfected) and beetle mass (as a proxy for body size). All two-way interactions were initially included but were removed if non-significant. Analyses were conducted using the Statistica 12.3 software package (Tibco Software, Inc.).

3. Results

Of the 113 beetles in this experiment, 79 (69.9%) were parasitized with C. passali nematodes, which is typical in terms of prevalence [11,12]. Parasitized beetles weighed 1.7 g (0.24 s.d.) on average compared to 1.6 g (0.18 s.d.) for those without the nematode, a significant difference (t-test, d.f. = 111, t = −2.09, p = 0.039). In the model examining wood processing rate, there was no effect of sex (F_1,109 = 0.107, p = 0.744), so it was removed (see electronic supplementary material, file S2). Nor were any of the two-way interactions significant. A second, simplified, model showed a significant positive effect of beetle mass (F_1,110 = 4.78, p = 0.031) on wood processing rate (see electronic supplementary material, figure S2.3). Importantly, the wood processing rate was also predicted by parasite status (F_1,110 = 4.04, p = 0.047); the average processing rate of parasitized beetles ($\overline{x}$= 0.77 g d⁻¹) was 15% greater than that of unparasitized ones ($\overline{x}$ = 0.67 g d⁻¹; figure 2a,b).

Figure 2.

(a) Average wood breakdown rates of horned passalus beetles with no C. passali nematodes and those with nematode infections. Level of significance shown is from a GLM that included effects of beetle mass and parasitism. (b) The amount of fragmented wood left by an average unparasitized beetle (60 g, left) and an average parasitized beetle (70 g, right) after three months. (Online version in colour.)

4. Discussion

It may be counterintuitive to think of a parasite having a positive influence on an ecosystem, but this evidence strongly points to that conclusion. Here, the average daily rate of wood breakdown by nematode-parasitized beetles was 15% higher than for beetles without nematodes (figure 2). From a physiological standpoint, this is consistent with the idea that the nematode compels hosts to compensate for the presumed energy drain by increasing food consumption [5]. Recall that this nematode does not inhabit the intestinal tract, so it likely does not influence digestion nor consume host gut contents. Thus, its primary effect would be to draw essential nutrients from the host haemolymph, thereby draining energy reserves. However, because these results are based on field-collected beetles with natural parasite infections, we cannot rule out an alternative explanation: that beetles with inherently high foraging (wood consumption) rates are simply more likely to acquire the nematode. This is possible whenever hosts acquire parasites through foraging [16], which is the case in this system. To verify that the parasite causes compensatory feeding by the host, further investigations are needed, possibly looking at metabolic differences between infected and uninfected hosts.

Another complicating factor here was the confounding effect of beetle mass; parasitized beetles were slightly larger (by about 6%), and this would also increase food consumption rates. Though in the statistical model examining wood breakdown rates (electronic supplementary material, table S2.3), both mass and parasitism were significant predictors, so both are clearly important. In terms of the role these beetles play in the ecosystem, the actual explanation for the pattern observed here is less important. To put the difference in daily breakdown rates into perspective, we estimate that over a 1 year span, 10 adult beetles without nematodes would break down approximately 2.4 kg of wood within a fallen log, while a group of 10 parasitized beetles would break down 2.8 kg of wood.

Our conclusions are naturally based on estimates obtained through laboratory observations (of beetles in containers), which may or may not be reflective of what happens in a natural log. However, we do note that our estimate of wood breakdown is consistent with prior estimates for this species that were also obtained through laboratory observation: our average processing rates (0.67–0.77 g per beetle per day) are comparable to 0.9 g per beetle per day from an early study [8]. Moreover, the latter study allowed beetles to inhabit and break down a semi-natural log in the laboratory, which is closer to a natural setting than our set-up was.

While we are confident in our conclusions concerning wood breakdown and the effects of C. passali, this project now leads to related questions concerning the host feeding behaviour and how it is affected by parasitism. For example, the wood fragmentation is only one aspect of the overall feeding strategy of passalus beetles, which is a multistep process; wood is consumed and soon excreted and is then colonized by beneficial bacteria and fungi, and the beetles re-ingest the wood [17]. It is unclear which step in this process the nematodes are affecting, and as such, we hope to pursue this line of inquiry in the future.

Finally, in recent years, there has been a growing appreciation for the role of parasites in nature [18–20], because of their influence in shaping communities, and because they are innately intertwined within all food webs, and are therefore a crucial part of the natural world. Countering long-standing unpopular views of parasites is certainly challenging, but perhaps evidence like that presented here will be of use in this effort.

Ethics

All insect collecting was conducted on land owned by the University of Georgia, and no ethical approval or permission was required.

Data accessibility

All data for the experiments conducted in this project are available in the electronic supplementary material files associated with this manuscript.

Authors' contributions

A.K.D. contributed to the conception and design of the experiments, data collection, data analysis and writing the manuscript. C.P. contributed to data collection and logistics of the experiments and reviewed the final manuscript. All authors agree to be held accountable for the content therein and approve the final version of the manuscript.

Competing interests

We declare we have no competing interests.

Funding

We received no funding for this study.