TEXAS TECH UNIVERSITY

Natural Science Research Laboratory

Occasional Papers

Museum of Texas Tech University

Number 337 2 December 2015

Coccidia (Apicomplexa: Eimeritoae) from Small Mammals or the
Southwestern Sandhills in Nebraska, USA

KalebJ. Thomas and Scott L. Gardner

Abstract

Coccidian parasites of the genus Eimeria (Apicomplexa: Eimeriidae) were prepared and
studied from small mammals collected from late July through early August during 2012 and
2013 on and around the area of the University of Nebraska-Lincoln, Cedar Point Biological
Station, north of Ogallala, Nebraska. Habitats from which mammals were sampled included
riparian, great-plains grasslands, and sandhills-grasslands. Twelve species representing 11
genera of small mammals were studied to begin to understand diversity of parasites in the
area. Rodents of the following species were examined: Geomys lutescens Merriam, 1890;
Dipodomys ordii Woodhouse, 1853; Perognathus flavescens Merriam, 1889; Chaetodipus
hispidus (Baird, 1858); Peromyscus leucopus (Rafinesque, 1818); Peromyscus maniculatus
(Wagner, 1845); Reithrodontomys megalotis (Baird, 1857); Onychomys leucogaster (Wied-
Neuwid, 1841); Microtus ochrogaster (Wagner, 1842); Zapiishudsonius (Zimmerman, 1780);
and Spermophilus tridecimlineatus (Mitchill, 1821). One species of shrew, Blarina brevi-
cauda (Say, 1823), also was examined. Eimeria was found in 22 of 165 small mammals for
an overall prevalence of 13%. A multivariate statistical analysis performed on measurement
variables of the oocysts and sporocysts revealed reasonable separation of species of Eimeria.

Key words: biodiversity, canonical analysis, Coccidia , Eimeria , rodents, sandhills,
small mammals

Introduction

From July through August of 2012 and 2013,
as part of a field parasitology course conducted at the
University of Nebraska-Lincoln, Cedar Point Biologi¬
cal Station (CPBS), individuals of several species of
small mammals were collected from both the station
grounds and from the surrounding area. The area sur¬
rounding CPBS is both geographically and ecologically

diverse, providing opportunities for a wide range of bio¬
diversity to be observed and studied. Little published
information is available on the presence of parasites
from mammals in the area, and no coccidia had been
reported from mammals of this region. In the current
study, 12 species of small mammals representing 11
genera were examined for presence of coccidia.

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Materials and Methods

Mammals examined for parasites were captured
either with Sherman™ live-traps or Museum-Special™
snap-traps at or near Cedar Point Biological Station (see
below for specific localities). All mammals collected
and studied were either treated in chloroform (if they
were from snap trap specimens) or killed in chloroform
by vapor inhalation and examined for parasites within
a few minutes after collection/death. Chloroform was
used in both cases to kill ectoparasites that potentially
could transfer to researchers/students at time of death of
the small mammal. At necropsy, fecal pellets were re¬
moved from the lower bowel of each host and preserved
in vials containing 2.0% aqueous (w/v) K 9 Cr 9 0 7 . Up to
the time of study, samples collected in 2012 were kept
refrigerated at 3°C and those from 2013 were incubated
at room temperature. Fecal samples were saved from
165 specimens. All samples were examined following
the Sheather’s (sugar) flotation method of Duszynski
and Wilber (1997). Oocysts found were measured and
imaged with a Zeiss Axiophot-II microscope equipped
with both Neofluar and Nomarski-interference 63
x objective lenses; measurements were made with

Zeiss™ software. All measurements were recorded in
micrometers (pm). Measurements are provided in the
Description of each species as the range, followed by
mean, and standard deviation in parentheses. Speci¬
mens of mammals were deposited in the Division of
Zoology, University of Nebraska State Museum, and
both samples and images of parasites (cataloged as NP
numbers) have been deposited in the Parasite Collection
of the Harold W. Manter Laboratory of Parasitology,
University of Nebraska State Museum.

Canonical discriminant analysis (CANDISC) of
each species of Eimeria identified in this study was per¬
formed using the statistical package SAS 9.3. Measure¬
ments of five characters (oocyst length, oocyst width,
sporocyst length, sporocyst width, and oocyst wall
thickness) were made for each oocyst studied. Because
of slight deviation from normality of measurements
taken, all data were log 10 transformed before analysis.
Levels of statistical significance were set a-priori at p
<0.05. For all discriminant comparisons, Mahalanobis
or generalized distances were used (Manly 1986).

Results

Prevalance

Not all species of mammals examined were
infected, but a summary of data for each species is
provided in Table 1. Small mammals collected in 2012
were found to harbor oocysts of the genus Eimeria in
6 of 81 (7.2%) specimens. Oocysts of Eimeria were
found in 16 of 84 (19%) specimens examined in 2013
from the same localities. Cumulative prevalence for
both years was 13.3% (22 of 165 specimens).

Descriptions

Measurements of oocysts of five species of Ei¬
meria collected from seven species of mammals are
provided in Table 2. Prior to this study, no data were
available on coccidian parasites of small mammals
of the southwestern Sandhills of Nebraska; therefore,
we present below complete accounts of Eimeria from
each species of infected mammal that we studied.

Photographs of oocysts from each host species also
are provided.

Host: Peromyscus leucopus (Rafinesque, 1818)

Eimeria arizonensis Levine et al. 1957

Description. —Oocyst wall smooth and 1.5 (±0.2)
thick. Sporulatedoocysts 26.1-29.9 by21.7-23.8,28.2
(±1.3) by 22.7 (±0.8) and a length:width ratio of 1.2
(±0.1). Sporocysts 10.1-13.3 by 7.7-8.7, 11.9 (±1.3)
by 8.4 (±0.3) and a length:width ratio of 1.5 (±0.2).
See Figures 1 and 2.

Prevalence. — E. arizonensis was found in eight
of 39 (20.5%) animals examined.

Specimens deposited. —NP1364, NP1374,
NP1387, NP1407, NP1408, NP1411, NP1446, and
NP1474.

Thomas and Gardner—Coccidla from Mammals in Nebraska

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Table 1. Prevalence of Eimeria in small mammals collected in western Nebraska during 2012 and
2013. Data presented as: positive individuals/total individuals (% positive).

Host

2012

2013

Total

Blarina brevicauda

0/1 (0)

-

0/1 (0)

Chaetodipus hispidis

1/11 (9)

-

1/11 (9)

Dipodomys ordii

1/3 (33)

0/4 (0)

1/7 (14)

Geomys lutescens

-

0/7 (0)

0/7 (0)

Microtus ochrogaster

0/8 (0)

0/2 (0)

0/10 (0)

Onychomys leucogaster

1/8(13)

1/2 (50)

2/10 (20)

Perognathus flavescens

1/8(13)

1/6 (17)

2/14(14)

Peromyscus leucopus

0/1 (0)

8/38 (23)

8/39 (21)

Peromyscus maniculatus

1/31 (3)

3/8 (38)

4/39 (10)

Reithrodontomys megalotis

1/9(11)

3/13 (23)

4/22(18)

Spermophilus tridecemlineatus

0/1 (0)

-

0/1 (0)

Zapus hudsonius

-

0/4 (0)

0/4 (0)

Total

6/81 (7)

16/84 (19)

22/165 (13)

Location .—Gastrointestinal tract. Oocysts ob¬
tained from fecal sample.

Locality .—Infected White-footed Mice were
trapped on eight occasions at the following localities:
23 July 2013 [CPBS] (41°12'29"N, 101°38'42"W);
23 July 2013 [CPBS] (41°12'40"N, 101°39T2"W);

24 July 2013 [CPBS] (41°11'36"N, 101°50'03"W);
24 July 2013 [CPBS] (41°12'37"N, 101°39'irW);
26 July 2013 [CPBS] (41°12'37"N, 101°38'56"W);
28 July 2013 [CPBS] (41°12'37"N, 101°38'56"W);
31 July 2013 [Ackley Valley, Haythorn Ranch, Arthur
County, NE] (41°12'00”N, 101°26'06"W); 5 August
2013 [Breen’s Flyway] (41°10'53"N, 101°21'32"W).

Figures 1 and 2. Photomicrographs of sporulated oocysts of Eimeria arizonensis recovered from the feces of Peromyscus
leucopus.

Table 2. Measurements of oocyst characters of five species of Eimeria from small mammals collected in western Nebraska (2012-2013). Data provided in
the following form: mean, range, standard deviation, and coefficient of variation (%).

Oocyst Sporocyst

Eimeria length:width length:width Oocyst wall Wall

species Host species Oocyst length Oocyst width ratio Sporocyst length Sporocyst width ratio width structure

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Thomas and Gardner—Coccidia from Mammals in Nebraska

5

Host: Peromyscus maniculatus (Wagner, 1845)

Eimeria arizonensis

Description. —Oocyst wall rough and 1.5 (±0.15)
thick. Sporalated oocysts 27.3-28.7 by 21.8-24.1,27.7
(±0.4) by 22.8 (±0.5) and a length:width ratio of 1.2
(±0.02). Sporocysts 12.0-14.9 by 6.2-8.5,13.3 (±0.7)
by 7.5 (±0.5) and a length:width ratio of 1.8 (±0.15).
See Figures 3 and 4.

Prevalence — This species was found in 4 of 39
(10.2%) animals examined.

Specimens deposited. —NP1251, NP1353,
NP1407, andNP1418.

Location. —Intestine. Oocysts obtained from
fecal sample.

Locality. —Infected species of this mouse were
trapped on four separate occasions at the following lo¬
calities: 26 July 2013 [Ackley Valley, Haythom Ranch,
Arthur County, NE] (41°12'00"N, 101°26'06"W); 23
July 2012 and 30 July 2013 [2.4 km south of CPBS
in the area known locally as the grama grass locality]
(41°11'38"N, 101°38'56"W); 23 July 2013 [CPBS]
(41°12'34”N, 101°38'57”W).

Figures 3 and 4. Photomicrographs of sporulated oocysts of Eimeria arizonensis recovered from the feces of Peromyscus
maniculatus.

Host: Reithrodontomys megalotis (Baird, 1857)

Eimeria arizonensis

Description. —Oocyst wall smooth and 1.2
(±0.13) thick. Sporulated oocysts 18.9-28.8 by
15-23.1,23.3 (±2.7) by 20.3 (±1.8) and a length:width
ratio of 1.2 (±0.1). Sporocysts 8-13.4 by 5.9-9.3,11.1
(±1.5) by 7.8 (±0.7) and a length:width ratio of 1.4
(±0.1). See Figures 5 and 6.

Prevalence. —This species was found in four of
22 (18.2%) animals examined.

Specimens deposited. —NP1224, NP1475,
NP1490, andNP1510.

Location. —Intestine. Oocysts obtained from
fecal sample.

Locality. —Infected Western Harvest Mice were
trapped on four occasions at the following localities:
18 July 2012 [CPBS] (41°12'34”N, 101°38'57”W); 5
August 2013, 6 August 2013, 7 August 2013 [Breen’s
Flyway] (41°10'53”N, 101°21'32"W).

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Figures 5 and 6. Photomicrographs of sporulated oocysts of Eimeria arizonensis recovered from the feces of
Reithrodontomys megalotis.

Host .—Dipodomys ordii Wood ho use, 1853

Eimeria balphae Ernst et al., 1967

Description .—Oocyst wall smooth 1.2 (±0.15)
thick. Sporulated oocysts 14.1-17 by 12.9-15.3, 15.6
(±0.83) by 13.9 (±0.7) and a length:width ratio of 1.1
(±0.1). Sporocysts 7.4-8.6 by 4.7-5.6, 7.9 (±0.4) by
5.1 (±0.3) and a length:width ratio of 1.6 (±0.1). See
Figures 7 and 8.

Prevalence .—This species was found in one of
seven (14.3%) animals examined.

Specimen deposited. —NP1229.

Location. —Intestine. Oocysts obtained from
fecal sample.

Locality .—This infected kangaroo rat was col¬
lected on 19 July 2012 [east of CPBS] (41°12'37"N,
101°38'56"W).

7

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10 pm

10 pm

Figures 7 and 8. Photomicrographs of sporulated oocysts of Eimeria balphae recovered from the feces of Dipodomys
ordii.

Thomas and Gardner—Coccidla from Mammals in Nebraska

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Host .—Chaetodipus hispidus (Baird, 1858)

Specimens deposited. —NP1272.

Eimeria hispidensis Ford et al. 1990

Description. —Oocyst wall smooth and 1.1 (±0.1)
thick. Sporulated oocysts 19.4-22.1 by 17.2-19.7,20.8
(±0.9) by 18.1 (±0.9) and a length:width ratio of 1.1
(±0.1). Sporocysts 7.8-9.8 by 6.5-7.6, 9.3 (±0.7) by
7.1 (±0.4) and a length:width ratio of 1.1 (±0.1). See
Figures 9 and 10.

Location. —Intestine. Oocysts obtained from
fecal sample.

Locality. —The infected Hispid Pocket Mouse
was trapped on 25 July 2012 [2.4 km south of Cedar
Point Biological Station in the area known locally as
grama grass locality] (41°1F38"N, 101°38'56"W).

Prevalence. —This species was found in one of
11 (9%) animals examined.

Figures 9 and 10. Photomicrographs of sporulated oocysts of Eimeria hispidensis recovered from the feces of
Chaetodipus hispidis.

Host .—Onychomys leucogaster (Wied-Neuwid,
1841)

Eimeria onychomysis Levine et al. 1957

Description. —Oocyst wall smooth 1.1 (±0.1)
thick. Sporulated oocysts 19.2-22.0 by 17.2-19.7,
20.1 (±0.6) by 16.5 (±0.9) and a length:width ratio of
1.2 (±0.05). Sporocysts 6.8-12.1 by 5.1-7.8,9.8 (±1.4)
by 7.0 (±0.6) and a length:width ratio of 1.1 (±0.05).
See Figures 11 and 12.

Prevalence. —This species was found in two of
10 (20%) animals examined.

Specimens deposited. —NP1259 and NP1426.

Location. —Intestine. Oocysts obtained from
fecal sample.

Locality. —Infected Northern Grasshopper
Mice were trapped on two occasions: 30 July 2013
[Ackley Valley, Haythorn Ranch, Arthur County, NE]
(41°12'00"N, 101°26'06"W) and 23 July 2012 [2.4 km
south of CPBS in the area known locally as the grama
grass locality] (41°11'38"N, 101°38'56”W).

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11

12

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Figures 11 and 12. Photomicrographs of sporulated oocysts of Eimeria onychomysis recovered from the feces of
Onychomys leucogaster.

Host .—Perognathus flavescens Merriam, 1889

Eimeria sp. (unidentified species)

Description. —Oocyst wall rough and 1.2 (±0.17)
thick. Sporulated oocysts 18-24.6 by 14.1-21.4, 21.8
(±2.0) by 18.6 (±1.8) and a length:width ratio of 1.2
(±0.05). Sporocysts 7.5-10.3 by 6.3-8.7, 8.8 (±0.7)
by 7.4 (±0.7) and a length:width ratio of 1.2 (±0.06).
See Figures 13-16.

Prevalence. —This species was found in two of
14 (14.3%) animals examined.

Specimens deposited. —NP1322 and NP1466.

Location. —Intestine. Oocysts obtained from
fecal sample.

Locality. —Infected Plains Pocket Mice were
trapped on two occasions: 31 July 2012 [Arapaho
Prairie] (41°29T9"N; 101°51'30"W); 1 August 2013
[Ackley Valley, Haythorn Ranch, Arthur County, NE]
(41°12'00", 101°26'06"W).

Canonical Discriminant Analysis

Results of the canonical discriminant analysis
of mensural characters of the coccidians studied are
shown in Figure 17. For this analysis, centroids of all
species were found to be significantly different, with
88% of the variation in the data being accounted for in
the first two canonical variates. Figure 17 shows a plot
of discriminant scores showing the minimum polygons
enclosing the spread of individuals for each species of
Eimeria identified in this study.

Thomas and Gardner—Coccidia from Mammals in Nebraska

9

Figures 13-16. Photomicrographs of poorly sporulated oocysts of an unidentified species of Eimeria recovered from
the feces of Perognathus flavescens.

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Canonical Axis I

Figure 17. Ordination showing minimum polygons for each of the host species from the
first two canonical axes derived from the morphometric analysis of Eimeria from rodents
collected from western Nebraska. Polygon labels are as follows: A = Eimeria arizonensis
in Peromyscus maniculatus ; B = Eimeria balphae in Dipodomys ordii; C = Eimeria
onychomysis in Onychomys leucogaster ; D = Eimeria hispidensis in Chaetodipus hispidus ; E
= Eimeria sp. in Perognathus flavescens ; F = Eimeria arizonensis in Peromyscus leucopus;
and G = Eimeria arizonensis in Reithrodontomys megalotis. The multivariate centroid of
each group is represented by a black dot.

Thomas and Gardner—Coccidia from Mammals in Nebraska

11

Discussion

Some species of Eimeria have been shown to
exhibit varying levels of both phenotypic plasticity
and assumed host specificity (Wash et al. 1990). In
our study, E. arizonensis was found in individuals of
Peromyscus leucopus, P. maniculatus , and Reithro-
dontomys megalotis. It has been observed previously
that E. arizonensis-\ike oocysts can infect these three
species, among others (Wash et al. 1990; Upton et al.
1992). Additionally, it has been observed that these
E. arizonensis-Mko, oocysts have shown phenotypic
plasticity that now is accepted as a well-documented
case of host-induced variation that is manifested both
morphologically and biochemically [see review by
Joyner 1982 and more specific information on this topic
in Duszynski (1971) and Wash et al. (1990)]. With
the exception of E. arizonensis , all coccidians studied
here showed very similar mensural data compared to
their descriptions. One host of E. arizonensis harbored
oocysts that were on average 7x3 micrometers (length
and width, respectively) larger than the means given
in the published descriptions, but all other characters
agree with these descriptions.

The wide range of phenotypic plasticity demon¬
strated by E. arizonensis (Upton et al. 1992) appears to
indicate that this may be a cryptic species of Eimeria
that may be morphologically convergent in different
hosts with overlapping habitats. To understand this
system, we suggest that molecular genetic studies be
conducted and, in fact, a new method of generating
genetic data from fewer than five oocysts has just been
published (Gerhold et al. 2015). Coinfections are also
difficult to detect when dealing with field-captured
wildlife. Gardner and Duszynski (1990) list some of the
difficulties associated with the phenotypic plasticity of
eimerian oocysts in subterranean rodents (Ctenomyidae
in Bolivia) and these authors show that care must be
taken in determination of species in these cases.

The multivariate statistical analysis (plot shown
in Fig. 17) shows moderate separation of the species
considered herein. Eimeria balphae from Dipodomys
ordii and E. arizonensis from Peromyscus leucopus
show strong separation, mostly due to overall size of
the oocyst and thickness of oocyst wall. The other
eimerians appear to have a significant amount of over¬
lap in multivariate space, indicating that these oocysts
have very similar morphological characteristics. This

further illustrates the difficulty of identifying species
of Eimeria using only morphology of oocysts. Again,
genetic work should be done to enhance this study (see
Zhao and Duszynski 2001; Gerhold et al. 2015).

A common problematic host/parasite association
has appeared in the case of the eimerian parasites from
Perognathus flavescens. Individual oocysts from this
host were not well-sporulated and therefore we were
unable to obtain much useful information from study of
these specimens. Further investigation of these speci¬
mens could lead to a description of a new species of
Eimeria because, to our knowledge, no previous papers
relative to species of Eimeria from P. flavescens have
been published. Presently, we do not have sufficient
data to properly identify and describe these oocysts.

One potential explanation for the annual differ¬
ence in prevalence observed in this study is the amount
of rainfall that occurred in the area. Rainfall data were
obtained from a meteorological station at CPBS run by
the High Plains Regional Climate Center (Anonymous
2015). June and July 2012 was markedly dry, with
rainfall amounts only 19% of average for that period.
The summer of 2013, though still abnormally dry at
49% of the mean precipitation, received more than
twice as much rainfall. During this same time period,
prevalence of Eimeria tripled. Data from the Sevilleta
LTER site in New Mexico (Gardner, unpublished) sug¬
gests that precipitation and prevalences of parasites are
directly linked. These data show that parasites that are
transmitted directly from host to host (without an inter¬
mediate host), such as Eimeria , have prevalences that
wax and wane in correlation with fluctuating rainfall
measures with little to no notable lag, whereas parasites
that utilize intermediate host(s) appear to follow the
same pattern set by precipitation, but with a delay of
about one year. These findings support the prevalence
differences observed in this study. In addition, high pre¬
cipitation levels in 2015 would indicate that an increase
in coccidian prevalences can be expected in 2015 with
a concomitant increase in helminth prevalence in 2016.
Further study over many years would be beneficial to
the understanding of prevalence shifts. The summer of
2014 is of particular interest, as there was a recorded
rainfall amount (at the CPBS station) of 217% of the
average in the area (Anonymous 2015).

12

Occasional Papers, Museum of Texas Tech University

Acknowledgments

We would like to thank all of the students and fac¬
ulty who helped collect and analyze host and parasitic
samples used in this study including Patricia Freeman,
Lindsey Howell, Katelyn Jelden, Erin Jones, Francisco
Tiago Melo, Rae Novich, Lauren Paasch, Gabor Racz,
S. Elizabeth Racz, Altangerel Tsogtsaikhan Dursahin-
han, and Francisco Zaragoza-Tapia. Thanks also to the
2012 and 2013 Field Parasitology classes at Cedar Point

Biological Station, University of Nebraska - Lincoln.
This work was partially funded by National Science
Foundation Grant Nos. BSR-9024816, DBI-06466356,
and DBI-1458139 to S.L. Gardner and the Cedar Point
Biological Station Room and Board Scholarship to
K. J. Thomas. Special thanks to Breen’s Flyway and
to the Haythorn family for access to important field¬
collecting sites.

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Thomas and Gardner—Coccidia from Mammals in Nebraska

13

Addresses of authors:

Scott L. Gardner

Harold W. Manter Laboratory of Parasitology

University ofNebraska-Lincoln

W529 Nebraska Hall

Lincoln, NE 68588-0514, U.S.A.

slg@unl.edu

Kaleb J. Thomas

Harold W. Manter Laboratory of Parasitology

University of Nebraska-Lincoln

W529 Nebraska Hall

Lincoln, NE 68588-0514, U.S.A.

kaleb. thomas@huskers. uni. edu

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