Great Basin Naturalist

Volume 55 Number 1 Article 8

1-16-1995

Whipworm (Trichuris dipodomys) infection in kangaroo rats (Dipodomys spp.): effects on digestive efficiency

James C. Munger Boise State University, Boise, idaho

Todd A. Slichter Boise State University, Boise, Idaho

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Recommended Citation Munger, James C. and Slichter, Todd A. (1995) "Whipworm (Trichuris dipodomys) infection in kangaroo rats (Dipodomys spp.): effects on digestive efficiency," Great Basin Naturalist: Vol. 55 : No. 1 , Article 8. Available at: https://scholarsarchive.byu.edu/gbn/vol55/iss1/8

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Great Basin Naturalist 55(1), © 1995, pp. 74-77

WHIPWORM (TRICHURIS DIPODOMYS) INFECTION IN KANGAROO RATS (DIPODOMYS SPP): EFFECTS ON DIGESTIVE EFFICIENCY

James C. Mungerl and Todd A. Slichterl

ABSTRACT.-To dcterminc whether infections by whipworms (Trichuris dipodumys [Nematoda: Trichurata: Trichuridae]) might affect digestive eHlciency and therefore enel"/,,'Y budgets of two species ofkangaroo rats (Dipodomys microps and Dipodumys urdU [Rodentia: Heteromyidae]), we compared the apparent dry matter digestibility of three groups of hosts: those naturally infected with whipworms, those naturally uninfected with whipworms, and those origi~ nally naturally infected but later deinfected by treatment with the anthelminthic Ivermectin. Prevalence of T. dipodomys was higher in D. rnicrops (.53%) than in D. ordU (14%). Apparent dry matter digestibility was reduced by whipworm infection in D. microps but not in D. ordii. Although a statistically significant effect was shown, its small mag­ nitude indicates that whipworm infection is unlikely to have a biologically significant impact on the energy budgets of host kangaroo rats.

Key words: parasite, digestive efficiency, whipworm, kangaroo rat, Trichuris, Dipodomys, energy budget.

Parasites inhabiting the gastrointestinal species were captured at the site, Ammospernw­ tract ofa host may reduce the efficiency of the philus leucurus, Neotorna lepida, Perognathus organs they inhabit cither through direct com­ jlavus, Peromyscus maniculatus, and two petition for nutrients or through damage to species of kangaroo rats, Dipodomys ordii and absorptive surfaces. Because decreased diges­ Dipodomys microps. Dipodomys ordU ranges tive efficiency may reduce the rate of energy from 42 to 72 g and consumes a diet consisting input into a host, gastrointestinal parasites have primarily of seeds (Zeveloff 1988). DipoMmys the potential to cause a change in host energy microps is larger, 72-91 g, and is unique among allocation (e.g., reduced activity or reduced kangaroo rats in that it relies heavily on leaves reproduction), and thereby impact the ecology of Atriplex confertifolia for forage (Kenagy ofthe host (Munger and Karasov 1989). 1972, Zcveloff 1988). Both species are liable to Tapeworm infections have a measurable infection by the whipworm Trichuris dipodo­ effect on digestive efHciency, but a biologically mys, a nematode that inhabits the cecum of unimportant effect on the cnergy budget of infected hosts (Grundmann 1957, Whitaker et host white-footed mice (Peromyscus leucopus; al. 1993). Munger and Karasov 1989). The present study On the study site we established a 13 X 13 was designed to determine if infection by a grid of 169 Sherman live traps baited with nematode, thc whipworm Trichuris dipodomys, millet and placed at 15 m intervals. During has a substantial effect on one aspect of the two trapping sessions, 14-22 June and 15-18 energy budget, digestive efficiency, of host August 1990, kangaroo rats (30 individuals of kangaroo rats (Dipodomys microps and D. ordii). D. microps and 85 of D. ordii) were captured and brought into the laboratory. Fecal speci­ MATERIALS AND METHODS mens from each animal were analyzed for the presence ofparasite eggs by standard centrifu­ Our study site, locatcd 2 km N of Murphy, gal flotation techniques using saturated sucrose Owyhee County, ID, is in desertscrub habitat solution (Pritchard and Kruse 1982). Six in­ with sandy loam substrate. Primary shrub fected but untreated animals from the June species of the study area are Artemisia experiment were included in the pool of ani­ spinescens, Artemisia tridentata, Atriplex mals used in the August experiment. The few canescens, Atriplex confertifolia, Atriplex spin­ animals that failed to thrive in the lab were osa, and Chrysothamnus nauseosus. Six rodent removed from the experiment; data from a

IDepartment of FIiology. Bobe State U'liversity. 1910 Univenity Drive. Boise. ID 83725.

74 1995] WHIPWORMS IN KANGAROO RATS 75 total of 29 D. microps individuals and 56 D. ordii were analyzed. Each month's set of captures was subjected to the following protocol: (1) Kangaroo rats were acclimated to a diet ofmillet seed for 3-11 d. (2) A pretreatment feeding trial was per­ , formed: Animals were placed in wire-bottomed cages with a measured amount ofwhole millet seed. At the end of5 d, fecal pellets were sep­ arated from spilled food and dried > 24 h at , 50 0 C. Initial digestive efficiency of each ani­ mal was measured as apparent dry matter digestibility (i.e., the proportion of mass con­ D. ordll sumed but not lost as waste), which was calcu­ Fig, 1. Effects of variation in parasite load on propor­ lated as (M FG -MFE)/ MFG, where MFO and MFE are the mass of food consumed and feces tional change in dry matter digestibility. Means + SE. Numbers represent sample sizes. produced, respectively. (3) Half of the infected animals were then injected subcutaneously with a solution of some minor morphological differences from Ivermectin (a systemic anthelminthic; Ivomec the original species description (Read 1956) brand, from MSD AGVET, Rahway, NJ). do exist, perhaps as a result of geographical Figure 1 gives sample sizes oftreatment groups. variation, the specimens most closely match June captures received, on each of two con­ Read's description of T dipodornys (A. Shostak secutive days, a 0.2-cc injection of lvermectin personal communication). Measurements of in 40% glycerol formal and 60% propylene several key morphological characters are as glycol; each injection delivered ca 350 p,g follows (X + SO): total length: <0 25.6 ± 0.8 Ivermectin I kg body mass. Controls received mm, ~ 41.3 ± 2.9 mm; hindbody length: <0 equal-volume injections of the glycerol for­ 12.7 + 0.4 mm, ~ 23.7 + 1.9 mm; spicule mal-propylene glycol carrier. This dosage had length: 850 + 85.1p,m; egg length: 64.8 + 5.0 little effect on the presence ofwhipworm eggs p,m; egg width: 33.5 ± 1.0 p,m. Voucher speci­ in feces of injected animals. Therefore animals mens were deposited with the University of received 8 d later a second set of two injec­ Alberta Parasite Collection (#'s UAPC11464 tions, each of 0.15 cc and delivering ca 2 mg and UAPC11465). Although we did not identi­ Ivermectin I kg body mass; control animals fy whipworms from D. ordii, we are confident received the carrier. August captures received, they are T dipodomys; the type host for T. on each of two consecutive days, an injection dipodornys is D. ordii, and T. dipodornys is of 0.15 cc volume delivering ca 2 mg known only from D. ordii and D. microps Ivermectin I kg body mass. Control animals (Whitaker et al. 1993). received the carrier. To control for possible Prevalence in Host Species. side effects of Ivermectin, halfofthe uninfect­ ed animals captured in August were also Trichuris dipodomys occurred at substan­ injected with a solution of Ivermectin. tially higher prevalence in D. microps than in (4) Two days afier each set of injections a D. ordii (Table 1), a result similar to that of posttreatment feeding trial was conducted Grundmann (1957). We can speculate as to using techniques in (2) above. Only results of three possible explanations for this pattern. the pretreatment feeding trials and feeding The first is that eggs produced by adult worms trials following the 2-mg Ivermectin / kg body in D. microps may become embryonated more mass injection will be presented below. easily than those in D. ordii. Freshly produced fecal pellets of D. microps appear moister than RESULTS AND DISCUSSION those of D. ordii (Munger personal observa­ tion), probably because of the higher amount Adult worms (seven of each gender) taken of green or leafy vegetation in the diet of D. from a Dipodomys micrors at our site were microps. Ifmoisture is necessary for emhryona­ identified as Trichuris dipodomys. Although tion of the eggs (as is implied by Parry 1968), 76 GREAT BASI 'ATURALIST [Volume 55

TABLE 1. Infection oftwo species orkangarou rdl with the TABLE 2. Effects of whipworm infection on apparent nematode Trl<:huris dipodomys. dry matter digestibility (ADM D). Standard errors are in parenth~ses. Figures on change between initial and final D. microps D. ordii feeding trials, as well as sample sizes, are in Figure 1. See Infected Uninfected Infected Uninf~ded text for a description oftreatments. June trapping 10 5 5 39 Treatment Deinfected (nfected Uninfected August trapping 6 9 7 34 Dipodomys microps Initial ADMD .956 .965 .955 (.0051) (.0029) (.0103) moister feces may lead to higher embryonation FinalADMD .961 .950 .953 rates and therefore higher prevalence among D. (.0039) (.0026) (.0052) microps. The second explanation is that social Dipodomys ordii Injli~1 ADMD .967 .957 .961 and burrow use behavior may di.ffer between (.0107) (.0076) (.0022) these species. For example, perhaps D. m.icrops Final ADMD .955 .958 .957 individuals visit one another's burrows (and (.0034) (.0037) (.0014) thereby become exposed to parasite eggs) at a substantially higher frequency tban do D. ordii. Also, D. mit-Tops inhabits a mound up to 2 m species. Experimental period Ouly vs. August) in diameter wh~e D. ordii inhabits less sub­ was included as a blocking factor. The depen­ stantial individual holes. Studies of another dent variable in the analysis was proportional system of two species of kangaroo rats has change between pretreatment and posttreat­ shown that the larger, mound-inhabiting D. meot ADMD ([post-preJjpre); this measure spectabilis uses its burrow system for pro­ should be more sensitive than posltreabnent longed periods, while the smaller D. metTiami ADMD in expressing treatment effects because rotates among several bl1l'rows (Jones 1989). it takes account ofinitial differences in ADMD This latter behavior would tend to reduce among hosts. reinfection ofindividuals; it would be interest­ Although there were no statistically signifi­ ing to see if behaviors differ similarly between cant main effects of treatment Or species on D. microps and D. ordii. The third explanation ADMD, there was a significant interaction is that resistance to infection may differ between these factors (Table 3), indicating that between these two host species. the two host species differ in their response to treatment. This difference between species was Effects on Digestive Efficiency explored using a separate ANOVA for each Apparent dry matter digestibility (ADMD) species, which revealed that treabnent with of millet seed was quite high, >95% on aver­ Ivermectin had a significant effect on change age (Table 2), a figure comparable to that in ADMD in D. microps, but not in D. ordii found by Schrieber (1979) for granivorous (Table 4, Fig. i). A Tukey's a posteriori multiple rodents. Injection of Ivermectin did not sample test revealed that, within D. microps, appear to affect ADMD of animals uninfected the cbange in ADMD of the deinfected group by whipworms, an effect that might occur differed significantly from the change in through the removal of other symbioots, or ADMD of both the infected group and the through some direct effect (proportional uninfected gronp. These results can be inter­ change in AD ID, X ± SE; untreated: preted as showing that the deinfected gronp -D.0043 ± 0.0035, treated: -D.OO58 + 0.(037). had 1.9% higher ADMD than the other two Therefore, in the following analyses all natn­ groups. rally uninfected animaJs are combined iolo one Of interest is the lack of effect Trichuris class. canses in D. ordii. This mal' be due to what The effect ofwhipworm removal on ADMD appears to be a higher intensity of infection was analyzed with a two·way analysis of vari­ (more parasites per infected host) in D. microps: ance (ANOVA). One factor analyzed was the fecal fioats of D. microps in general contained treatment: deinfected (natnrally infected but more eg,gs than did floats of D. ordiiJD. treated with Ivermectin) vs. infected (naturally mioTops X = 254, SE = 115.2; D. ordii X = infected but not treated with ivermectin) vs. 63.5, SE = 21.0; Mann-Whitney U·test, U = naturally uninfected. The other factor was 79, P = .1). Iffewer worms were present in D. 1995] WHIPWORMS IN KANCARoo RATS 77

TABLE 3. F values and probability values (P) from three.way analyses of variance on effects of species, month, and treatment (deinfected, infected, or uninfected) on apparent dry matter digestibility (ADMD). Dependent variable Proportion change Initial ADMD Rnal ADMD inADMD Source df F P F P F P Treatment 2 .15 .86 .72 .49 .47 .63 Species 1 .46 .50 .82 .37 .33 .57 Treatment * Species 2 1.33 .27 1.78 .18 4.74 .012 Block (= Mooth) 1 .51 .48 9.!! .003 .00 .95 Error 77

in the lab. Sara Murray and Aaron Munger helped in the field. Discussion with Mary Price TABLE 4. Results from one·way analyses of variance on the effect oftreatment (deinfected, infected, and uninfect- was helpful, as were comments from anony­ ed) on % change in dry matter digestibility in D. microps mous reviewers. This research was supported and D. ordii. by an Intramural Faculty Research Grant from Species Source df MS FP Boise State University.

D. microps LITERATURE CITED Treatment 2 .00106 4.64 .019 Error 27 .000229 GRUNDMANN, A. W. 1957. Nematode parasites of mam­ mals of the Great Salt Lake Desert of Utah. Journal D. ordii ofParasitology 43: 105-112. Treatment 2 .00034 1.21 .31 JONES, w. T. 1989. Dispersal distance and the range of Error 52 .01442 nightly movements in Merriam's kangaroo rats. Journal ofMammalogy 70: 27-34. KENAGY, G. J. 1972. Saltbush leaves: excision ofhypersaline tissue by a kangaroo rat. Science 178: 1094--1096. ordii, the effect of eradicating those worms MEITRICK, D. F. 1980. The intestine as an environment would have been less apparent. for Hymenolepis diminuta. Pages 281-356 in H. P. One might question the biological impor­ Ani, ed., Biology of the tapeworm Hymenolepis tance ofthe slight, albeit statistically significant, diminuta. Academic Press, New York, NY. MUNGER, J. C., AND W. H. KARASOv. 1989. Sublethal para­ decrease in ADMD caused by Trichuris infec­ sites and host energy budgets: tapewonn infection in tion. Munger and Karasov (1989) showed an white-footed mice. Ecology 70: 904-921. effect of similar magnitude resulting from tape­ PARRY, J. E. 1968. Transmission studies ofnematodes with worm infection (Hymenolepis citelli) in white­ direct life histories in selected Utah mammals. Unpublished doctoral dissertation, University of footed mice (Peromyscus leucopus). They Utah, Salt Lake City. argued that hosts can easily compensate for PRITCHARD, M., AND C. KRUSE. 1982. The coUection and such small effects by slight increases in food preservation of animal parasites. University of consumption or decreases in expenditures, or Nebraska Press, Lincoln. 141 pp. READ, C. P. 1956. Trichuris dipodomys, n. sp., from Ord's by changes in gut morphology (Mettrick 1980). kangaroo rat. Proceedings of the Helminthological and concluded that such effects on ADMD are Society of Washington 23:119. unlikely to affect host energy budgets or to SCHRIEBER, R. K. 1979. Coefficients of digestibility and translate through to population-level effects. caloric diet of rodents in the northern Creat Basin The same conclusion is likely to apply to the desert. Journal of Mammalogy 60:416-420. WHlT.... KER, J. 0., JR., W. J. WRENN, AND R. E. LEWIS. kangaroo rat-whipworm system. 1993. Parasites. In: H. H. Genoways and J. H. Brown, eds., BioJogy ofthe Heteromyidae. American ACKNOWLEDGME1\'TS Society ofMammalogists Special Publication 10. ZEVELOFF, S. I. 1988. Mammals of the Intermountain We thank Allen Shostak ofthe University of West University of Utah Press, Salt Lake City. 365 pp. Alberta's Parasitology Museum for measuring specimens ofthe parasite and for its identifica­ ReGeWed 27]ub; 1993 tion. Kay Kesling helped both in the field and Accepted 20]u"" 1994