Parasites and Dung Beetles as Ecosystem Engineersin a Forest Ecosystem

Broox G. V. Boze & Alexander D. Hernandez &

Michael A. Huffman & Janice Moore

Revised: 16 October 2011 /Accepted: 21 October 2011 /Published online: 10 November 2011# Springer Science+Business Media, LLC 2011

Abstract Dung beetles serve as the intermediate host for Streptopharagus pigmentatus,a nematode parasite that infects an old world primate, the Japanese Macaque (Macacafuscata). This study compares the behaviors of infected and uninfected beetles in bothtransmission dynamics and the ecological role of the parasite. The results suggest thatparasitism does not alter the beetle’s use of shelter or choice of substrate onYakushima Island, Japan. However, infected beetles consume significantly less feces.Dung beetles remove the majority of fecal material in this forest ecosystem,eliminating breeding grounds for many insect pests and burying nutrients that areessential for plant health. Thus, the nematode parasite S. pigmentatus, by altering itshost’s behavior, changes the availability of fecal resources to both plant and animalcommunities and should therefore be classified as an ecosystem engineer.

Keywords Dung beetle . nematode . behavioral modification . ecosystem engineer .

Yakushima

Introduction

Examples of parasite-induced behavioral changes in intermediate hosts range acrossmost major host taxa; these changes can affect a variety of behaviors including

J Insect Behav (2012) 25:352–361DOI 10.1007/s10905-011-9305-5

B. G. V. Boze (*) : J. MooreDepartment of Biology, Colorado State University, Fort Collins, CO 80523, USAe-mail: Bboze@colostate.edu

A. D. Hernandez :M. A. HuffmanDepartment of Ecology and Social Behavior, Primate Research Institute, Kyoto University, Inuyama,Aichi 484-8506, Japan

Present Address:A. D. HernandezCenter for Infectious Disease Dynamics, The Pennsylvania State University, University Park,PA 16803, USA

phototaxis which is a response to light, geotaxis which is a response to gravity,activity level or movement, and even choice of food. Such behavioral changes canhave a variety of effects, ranging from benefits to the parasite (e.g., enhancedtransmission or survival) to benefits to the host (e.g., parasite avoidance orresistance), as well as effects with no currently known beneficiary (Moore 2002).

Despite many well-documented instances of such behavioral alterations (seeMoore 2002, and Thomas et al. 2005), coprophagous animals have not figuredprominently in this literature. This is surprising, given their increased risk ofencountering the propagules of intestinal parasites for which they might serve asintermediate hosts. Because of this, we investigate behavioral changes in dungbeetles, which act as intermediate hosts for the nematode parasite Streptopharaguspigmentatus. The definitive host for S. pigmentatus is the Japanese Macaque(Macaca fuscata).

Coprophagous beetles serve as intermediate hosts for a variety of nematodeparasites. They play an important role in natural and agricultural ecosystems byremoving feces from the upper surfaces of soil at a rate that far exceeds other naturalprocesses. In the tropics, feces remain on the surface almost three times longer in theabsence of dung beetles than when they are present (Slade et al. 2007). The majorityof dung beetle species feed exclusively on feces, and depend on it for construction ofbrood balls that are buried and inoculated with eggs. These natural feeding andbreeding behaviors associated with dung-processing aid in dispersal of seeds andhelp preserve the regenerating capacity of the forest (Estrada et al. 1999). Inaddition, these beetles directly alter their ecosystem by removing feces from the soilsurface where it would otherwise serve as breeding habitat for parasitic nematodes,flies and other invertebrates. Dung beetles also contribute to ecosystem health byincreasing the rate of nutrient cycling and fertilizing by aerating soils (Halffter andMatthews 1966). Because of these roles alone, dung beetles can be consideredecosystem engineers. That is, they are organisms, plant or animal, that directly orindirectly modulate the availability of resources to other species by causing physicalstate changes to biotic or abiotic materials (Jones et al. 1994 and Jones 1997). Giventhe importance of dung beetles in ecosystem function, the possibility that parasitescan alter their ecosystem activity becomes highly relevant when applied to landmanagement practices.

The parasite of interest in this study (S. pigmentatus) typically inhabits theintestine of a primate host and depends on coprophagous beetles such asOnthophagus lenzii, O. atripennis, O. ater, and Aphodius mizo for completing itslife cycle (Machida et al. 1978 and Gotoh 2000). Cockroaches and one othercoprophagous beetle (Geotrupus laevistriatus) are also believed to be potentialintermediate hosts (Gotoh 2000). The specific pathology of S. pigmentatus has notbeen identified although there is ongoing work to identify the role of this nematodein primate health. MacIntosh et al. (2011) show that S. pigmentatus has nodetrimental effects on foraging habits, reproductive activity, or dominance status ofthe macaque. However, when the infection becomes intense the mere presence of theworms can cause intestinal blockage and S. pigmentatus may act in concert withother pathogens to make monkeys sick. Moreover, at least one pathogenic nematodeof primates, Gongylonema pulchrum, has the potential to use dung beetles asintermediate hosts. Thus, in addition to the possible role of parasites in altering the

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ecosystem function of dung beetles, they may play a role in the health and numbersof the Japanese Macaque, especially if they alter behaviors of the beetles that arerelated to parasite transmission.

The majority of research on parasite manipulated behavior focuses ontransmission effects, but there is growing interest in other outcomes of alteredbehavior (Lefevre et al. 2009). For instance, Thomas et al. (1999) suggest thatparasites can serve as ecosystem engineers through phenotypic alterations in theirhost’s behavior, morphology and/or physiology. Parsite induced behavioral changescan alter habitat availability (Thomas et al. 1999) and food web interactions(Lafferty et al. 2006) suggesting their potential as ecosystem engineers. Because ofthe increasing recognition of the important role manipulative parasites play in theecology of natural ecosystems this study has a dual purpose. We explore the effect ofS. pigmentatus on behaviors associated with parasite transmission (e.g., use ofshelter and choice of substrate), and ask if the nematode parasite influencesbehaviors integral to the beetle host’s role as an ecosystem engineer (e.g., rate offecal consumption).

Methods

Dung beetles from the genus Onthophagus were collected from the subtropical, warm-temperate evergreen forest of Yakushima, Japan. Yakushima is a 500 km2, mountainousisland located 60 km south of Kyushu, Japan (30°N, 131°E). Much of the island isprotected as a UNESCO World Natural Heritage site and has been since 1993. Theisland serves as home to an endemic subspecies of Japanese macaque (Macaca. fuscatayakui) that exists relatively undisturbed within protected areas (Yamagiwa and Hill1998). Monkeys on Yakushima are infected by five gastrointestinal nematode parasitespecies including two that are trophically transmitted: Streptopharagus pigmentatus andGongylonema pulchrum (Gotoh 2000; Hernandez et al. 2009; MacIntosh et al. 2010).Both of these species require a coprophagous beetle intermediate host to complete theirlife cycle (Machida et al. 1978).

In July 2008, we collected coprophagous beetles inside the home range of the‘Umi’ troop of Japanese macaques whose members have been studied since 2005(Tarnaud and Yamagiwa 2008; Hernandez et al. 2009; MacIntosh et al. 2010). Thegroup ranges between altitudes of 0 and 250 m, with an estimated home range sizeof approximately 0.7 km2 (MacIntosh et al. 2010). During the summer of our study(2008), over 80% of individuals in the troop were infected with S. pigmentatus,while less than 10% were infected with G. pulchrum (MacIntosh et al. 2010).

Beetles were collected in baited pitfall traps constructed from 12 oz plastic cups buriedwith the rim level to the ground, and modified from those used by Kanda et al. (2005). Atotal of ten traps were set randomly within nine plots (10×10 m) located in the centre ofthe troop’s home range. Traps were baited with feces from troop members known not tobe shedding nematode eggs, and with water added at the base to prevent insects fromescaping. Traps were set twice during a 24 h period, morning and dusk, because someOnthophagus species are known to be noctournal and other diurnal, although this canvary with seasonal changes (Sasayama et al. 1984). Traps were cleared and reset twice aday to separate beetles into noctournal and diurnal groups.

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Once collected, beetles were placed in 28-liter aquaria (40×25×28 cm) andallowed to acclimate to tank life for a minimum of 24 h before the start of anyexperiments. Beetles collected during daylight hours were kept separate fromthose collected at night. Beetles belonging to the genus Onthophagus areclassified as paracoprid beetles, meaning they procure dung in tunnels directlybelow the fecal source. A minimum of 5 in. of soil was added to each tank toaccommodate this tunneling behavior. Dung beetles can live on feces alone andwere fed monkey feces ad libitum, which served as a source of both food andwater. Field conditions precluded the use of controlled rearing chambers; tankswere kept outside in natural conditions, which included an average temperature of30.7±3.86ºC and an average humidity of 67.08±5.64%. Conditions weremonitored throughout the experiments and did not appear to influence thebehaviors addressed here. Because these were field collected animals, whether ornot a beetle was infected was known only upon dissection (see below). Thus, theexperiments conformed to a double blind design.

After acclimation, beetles were tested for several behavior changes: substratepreference, shelter preference, and amount of dung consumed in 48 h. All preferencetests were done during daylight hours because this is when monkeys are most likely toforage for insects. Any parasite-induced change in behavior is likely to have the greatesteffect on possible transmission to monkeys if it is expressed during this time.

Preference tests were done with individual beetles. Each individual was placed ineither the substrate or shelter test apparatus with the order of tests randomized.Preliminary observations suggested that15 min were sufficient for a beetle toacclimate to the apparatus before a test began. During these 15 min, flight escapebehavior ceased, and the beetle began to crawl around the tank instead of remainingstationary with legs tucked in close to the body.

Substrate Preference Test

In order to test for predator avoidance behavior via crypsis we assessed whetherbeetles spent more time on the surface of a substrate lighter or darker than thenatural color of their body (black). In each of these cases the parasite makes itshost more conspicuous to predators which serve as the final host. An aquarium,similar to that used in rearing, was divided into equal halves with one side ofthe aquarium containing a thin layer of black aquarium gravel and the otherwhite aquarium gravel. Gravel size and texture did not differ between colorsand was rinsed with soapy water, dried and replaced after each test to ensureconsistency between trials. Altered substrate or habitat preference in thepresence of parasites is not uncommon and has been demonstrated in a varietyof arthropods including isopods, amphipods and cockroaches (see examples inMoore 2002).

The amount of time spent on each half of the tank was determined in thefollowing manner: beetle location was recorded every 30 s during a fifteen-minuteperiod for a total of 30 observations per beetle. Individuals were assigned a scorebetween zero and thirty points for each test based on the sum of their location scoresat each thirty-second interval. One point was assigned for every observation of thebeetle on white substrate.

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Shelter Preference Test

Predatory avoidance behavior was also assessed by measuring the amount of timebeetles spent out in the open versus underneath shelter. Black styrofoam with a threecm clearance provided shelter on one half of the tank. Opaque black tape was usedto cover the glass area below the styrofoam shelf. Thus one side of the tank provideda compact area devoid of light while the other half of the tank remained open andhad no type of structure for the beetle to hide under or in.

The location of each beetle was recorded every 30 s for a fifteen-minute period,giving a total of 30 observations per beetle. Individuals were assigned a score betweenzero and thirty points based on the sum of their location scores at each 30 s interval. Onepoint was assigned for every observation that found the beetle in the open.

Consumption Test

After the choice experiments were complete, beetles were isolated and deprived offood for 24 h before being placed a small 18 oz container with 0.2 g (dry-weight) ofprimate feces rehydrated with 1 ml of water. The dry weight of feces remaining after48 h was then weighed and the amount consumed by the individual beetledetermined. The amount of dung consumed by each individual was found bysubtracting the final weight from the initial weight of the dried feces

At the termination of all experiments and dung feeding trials, beetles were fixedin 70% ethanol for later dissection. Length, width, weight, and sex were recorded foreach individual. The beetles were then dissected and examined for parasites;prevalence and intensity of infection were recorded. Prevalence refers to theproportion of hosts infected by a particular parasite species whereas intensity ofinfection is defined as the number of individuals of a particular parasite species in asingle host (Bush et al. 1997).

Data Analysis

Statistical analysis was carried out using Stata 11 software. Analysis involvedANOVA confirmed by t-tests when data were heteroscedastic. Mann–Whitney Utests were applied to non-normal data and significance was established at P=.05.

Results

A total of 146 dung beetles were used in this study (diurnal N=75, nocturnal N=71).There was no difference in prevalence of infection based on collection area (F2, 291=2.15; p=0.192) so data from various plot locations were pooled for analysis.

Using length as an indicator of size, nocturnal beetles (8.296±0.918 mm) foundon Yakushima Island Japan were slightly larger than those active during daylighthours (6.74±1.58 mm) (F1, 144=52.11; p<0.0001). Despite the difference in sizebased on activity patterns, length was not associated with prevalence of infection ineither the diurnal (Mann–Whitney U=2850, P=0.1015) or nocturnal groups (Mann–Whitney U=2556, P=0.4119).

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Both mean intensity (F1, 77=12.499; p=0.00069) and prevalence (F1, 144=15.58318; p=0.00012) of infection were higher in the smaller diurnal beetles thanthey were in those collected at night (Fig. 1). Approximately 62% of diurnal beetleswere infected and had an average of 11.59±12.04 larval nematodes per infectedindividual. Forty-five percent of nocturnal beetles were infected and the intensity ofinfection was much lower with only 3.2±5.21 nematodes per individual.

Presence of nematode larvae did not affect substrate choice or use of shelter ineither the nocturnal or diurnal groups. Both infected and uninfected beetles exhibitedsimilar predator avoidance behaviors. There was no difference between uninfectedand infected beetles in the amount of time spent under the shelter. (Mann–WhitneyU=2556, P=.6100 nocturnal; Mann–Whitney U=2850, P=.6259 diurnal). Bothgroups spent more time underneath the shelter than out in the open. Likewise, therewas no difference in the proportion of time spent out in the open for either group.

Fig. 1 Both prevalence and intensity of infection are higher in diurnal dung beetles than nocturnal dungbeetles. a Intensity of infection shown as mean number of Streptopharagus larvae found in hemoceol ofinfected beetles b Prevalence of infection shown as proportion of infected individuals within two beetlepopulations

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Both infected and uninfected individuals spent more time on the dark coloredsubstrate (which matches their external markings) than the light colored substrate.This was true for both nocturnal (Mann–Whitney U=2556, P=.5433) and diurnalbeetles (Mann–Whitney U=2850, P=.4894).

Infected beetles consumed significantly less feces than uninfected beetles in boththe nocturnal (Fig. 2a) and diurnal groups (Fig. 2b). Infected nocturnal beetlesconsumed almost 30% less feces than uninfected nocturnal beetles (Mann–WhitneyU=1540, P=0.0472); and infected diurnal beetles consumed approximately 22%less feces than their uninfected counterparts (Mann–Whitney U=990, P=0.0093).

Discussion

This study shows that both intensity of infection within individuals and prevalenceof infection within the population are greater in diurnal beetles than in those that are

Fig. 2 a Mean consumption of nocturnal Onthophagus beetles during a 48 h period (results shown ingrams). Mann–Whitney U=1540, P=0.047 b Mean consumption of diurnal Onthophagus beetles during a48 h period (results shown in grams). Mann–Whitney U=990, P=0.009

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nocturnally active. This may be related to the differences in species diversity oractivity cycles and associated foraging habits associated with each group. Somenematode eggs are subject to desiccation and cannot survive for great lengths of timeoutside their host (Bryan 1973). The likelihood of feces containing viable parasiteeggs at night is thus decreased as feces from the diurnally active definitive hostremain on the surface of the soil and lose moisture. While more work needs to bedone in this area, we believe that dung beetles exhibiting similar activity patterns astheir final host—in this case, diurnal beetles– are more likely to encounter freshfeces of that host than those that forage at other times. Arthropods with activitycycles that are congruent with those of definitive hosts are also more likely to serveas intermediate hosts because overlapping activity times increase the likelihood ofinteraction and therefore predation.

Using substrate choice and shelter preference as indicators of predator avoidancebehavior, we found no evidence of parasite-induced behavioral alterations that mightincrease predation risk in these parasitized beetles. There may be other behaviorsthat we have yet to test that will demonstrate an effect of this parasite on behaviorsassociated with predation risk. What is more intriguing is the unanticipated effect ofthe parasite on the consumption of feces by a beetle.

The mean consumption of feces by infected individuals is significantly lower thanthe mean consumption of feces by uninfected individuals. In this case the merepresence of S. pigmentatus within Onthophagus beetles creates two distinct groupsof beetles with different ecological roles; those that are readily consuming feces andaiding breakdown of feces, and those that are not. The two groups of beetlesinevitably share the same trophic niche, thus the parasite has potential to alterinterspecific competition processes and reduce the amount of time spent feeding/burying dung.

In addition, this situation may also alter food availability and energy flow withinthe greater population of animals on the island. This would not be the first time wesee parasites affecting food web dynamics (Thompson et al. 2005; Lafferty et al.2008; Hernandez and Sukhdeo 2008). However, most of the reports of such effectshave been in the realm of parasite transmission, particularly transmission related toaltered host behavior and subsequent predation. In experiments described here, theparasite affects food webs in very different ways from those related to predation andtransmission. Most notably, the parasite is reducing the dung beetle’s role in nutrientcycling by 20 to 30%. Because dung beetles are among the most importantecosystem entities that move fecal material, such a reduction can have measurableconsequences for the rest of the ecosystem.

Dung beetles play a significant role in terrestrial ecosystems by driving a series ofecological processes including nutrient recycling, parasite suppression, soil aeration,pest control, and secondary seed dispersal (summarized in Nichols et al. 2008).These processes are all outcomes of the consumption and burying of feces below thesurface soil. The physical movement of feces from above to below the soil surfacerelocates nutrient rich organic material and instigates micro-organismal and chemicalchanges in the upper soil layers. In addition, the consumption of feces helps reducethe number of viable parasite eggs in the environment and removes larvae ofpestiferous insects. Dung beetles can move many times their weight in feces and areoften the predominant competitor when it comes to procuring fecal resources

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(Hanksi and Cambefort 1991). If behaviors associated with the use of feces arechanged by parasitism, then both the parasite and beetle have great potential to offsetnatural flow of resources through the environment. As such, they should both beconsidered ecosystem engineers.

In addition, because feces serve as the only food source for these beetles, it isreasonable to expect the decreased intake to result in less energy for infected beetlesas they carry out functional roles such as feces removal and brood ball creation foryoung. This could have measurable consequences on Yakushima Island as it haspotential to alter the diversity and abundance of dung beetle species. Future studiesshould assess the formation and use of brood balls in addition to measuring theconsumption of feces by individual groups.

In the United States alone, over a million hectares of pastureland are lost due to dungaccumulation and contamination (Fincher 1981). Dung beetles decrease the time a fecalpat spends on the surface of the soil by 19% and saves the agricultural communityalmost 380 million dollars annually (Losey and Vaughn 2006). If dung beetles infectedwith nematodes are consuming three-quarters the feces they normally would then theyare indeed acting as ecosystem engineers and the economic value of their ecosystemservice is dramatically reduced by parasitism. Because S. pigmentatus has the ability toinfect at least three genera of dung beetle (Gotoh 2000) and the introduction of foreigndung beetles is becoming more common (de Oca 1998) knowledge about howparasites alter their host behavior is becoming more and more important.

Acknowledgements Financial support for this study was provided the National Science Foundation andJapanese Society for the Promotion of Science’s East Asia and Pacific Summer Institute. The NationalScience Foundation also provided funding for Broox Boze through the Alliance for Graduate Educationand the Professoriate program.

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