Southwestern Association of Naturalists
Renal Structural Adaptations among Three Species of Peccary
Author(s): Stam M. Zervanos
Source: The Southwestern Naturalist, Vol. 47, No. 4 (Dec., 2002), pp. 527-531
Published by: Southwestern Association of Naturalists
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Accessed: 13-07-2015 05:48 UTC
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THE SOUTHWESTERN
NATURALIST
47(4):527-531

DECEMBER2002

RENAL STRUCTURAL ADAPTATIONS AMONG
THREE SPECIES OF PECCARY
STAM M. ZERVANOS*
PennsylvaniaStateUniversity,
Department
ofBiology,
Reading,PA 19610
*
smzl@psu.edu
Correspondent:
ABSTRACT-Severalmorphological characteristicsof the kidneywere studied to determine the
degree of interspecificand intraspecificadaptation that mightoccur within3 species of peccary
fromarid, semi-arid,and moist habitats.Paired kidneysamples were collected fromcollared (Tayassu tajacu), Chacoan (Catagonus wagneri),and white-lipped (T pecari) peccaries from habitats
varyingin water availability.Two indexes for renal concentratingability,the relative medullary
thicknessand relativemedullaryarea, exhibited highervalues for animals fromarid and semi-arid
habitats than for those from moist habitats. Relative kidney mass also was higher for collared
peccaries from dry environments.It was concluded that renal structuresare flexible in response
to environmentvariation,and the differencesobserved were related to the adaptabilityof renal
concentratingstructures.
RESUMEN-Se estudiaron algunas caracteristicasmorfol6gicasdel rifi6npara determinarel grado
de adaptaci6n interespecificae intraespecificaque pueden ocurrir en 3 especies de pecari de
habitats aridos, semiaridos,y hfimedos. Se reunieron muestraspares de rifi6nde los pecaries de
collar (Tayassu tajacu), del Chaco (Catagonus wagneri),y de quijada blanca (T pecari) de habitats
que variaban en la disponibidad de agua. Dos indices que miden la habilidad renal para concentrar,el grosor relativomedular y el irea medular relativa,mostraroncifrasmaisaltas en los animales
de haibitatsiridos y semiiridos que los de hibitats
Tambi6n la masa renal relativafue
hrimedos.
mis alta para los pecaries de collar en ambientes secos. Se concluy6 que las estructurasrenales
son flexiblescon respecto a las variaciones del medio ambiente, y que las diferenciasobservadas
se relacionaron con la adaptabilidad de las estructurasrenales que sirven para la concentraci6n.

The familyof peccaries, Tayassuidae, is composed of 3 livingspecies, the collared (Tayassu
tajacu), the white-lipped (T pecari), and the
Chacoan (Catagonuswagneri).Of the 3, the collared peccary has the widestdistribution,ranging from southwesternUnited States through
Central America to northern Argentina and
Uruguay. It inhabits a diversityof habitats,including deserts, semi-deserts,and rainforests.
The white-lippedpeccary ranges from southern Mexico to southern Brazil and Paraguay.It
inhabits primarily moist habitats, including
most South American rainforests.The Chacoan peccary has a restrictedrange consisting
of semi-aridhabitatsin Paraguay and northern
Argentina (Sowls, 1997). In general the Chacoan peccary inhabits mesic habitats,the collared peccary xeric to moist habitats,and the
white-lipped peccary primarilymoist habitats
(Wetzel, 1977; Mayer and Brandt, 1982). Understanding the ecophysiology among the 3

species could furtherexplain theirdistribution
and environmentaladaptation.
An importantmeasure of environmentaladaptation is renal function. The relative medullary thickness (RMT) and the relative medullary area (RMA) are morphological indexes
of the kidney's capacity to concentrate urine.
The higher these indexes, the greater the kidney's capacity to produce concentrated urine
(Brownfieldand Wunder, 1976). RMT is a relative measure of the lengthof the loop of Henle, corrected for kidneyvolume, and is, therefore, a measure of the abilityto generate an
osmotic gradient within the renal medulla.
Brownfieldand Wunder (1976) found a 0.80
correlationcoefficientbetween RMT and renal
concentratingcapacity and a 0.99 correlation
for RMA. Several other studies have shown
both interspecific and intraspecific correlations between RMT/RMA and the degree of
water stress in the environment,including 3

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528

The Southwestern
Naturalist

vol. 47, no. 4

ullary regions were cut and sent to the Animal Disease Laboratory of PennsylvaniaState Universityfor
processing into hematoxylin-stained and eosinstained slides. The number of glomeruli per microscopic field was counted in 10 differentfields of vision withinthe deep cortical region of each kidney
section. All glomeruli thatwere only partiallyvisible
withina fieldwere counted as one-halfa glomerulus.
The glomerular density (number per mm2) was determined by dividing the average glomerular number per field by the area of the field of vision. In
addition, within each field of vision, the 3 largest
glomerular diameters were measured with a micrometer and recorded. This technique enhanced the
chance of measuring the mid-saggitaldiameter of
glomeruli.
All indices for both kidneys were averaged for
each animal. Thus, data fromeach kidneywere not
MATERIALSANDMETHODS-Paired kidney samples
independent observations, whereas data averaged
from adults representing the 3 species of peccary fromeach pair were independent. This reduced the
were collected from hunters at 5 differenthabitat variance and degrees of freedom for more conserlocations. Eighteen collared peccary samples were vative comparisons. A t-testshowed no difference
collected from 2 desert (arid) locations in Arizona among male and female indices, thereforedata from
(Fort Huachuca between 7 March and 16 March both sexes were combined. To factorout body mass
1986 and the 3-Bar Research Station between 4 in testing for interspecificand intraspecificdifferMarch and 27 April 1978). The annual precipitation ences in RMT and kidney mass, a 1-wayanalysis of
at these 2 locations was similarand averaged 19 cm. covariance (ANCOVA), withbody mass as the covarTen Chacoan peccary and 5 collared peccary kidney iate, was used as described by Gabor et al. (1997).
pairs were collected between 22 Julyand 4 August Because scaling equations for body mass were not
1977 fromthe semi-aridGran Chaco region of west- available for the other data comparisons, I utilized a
ern Paraguay (average annual precipitation of 65
1-wayanalysis of variance (ANOVA) and tested the
cm). Seven collared peccary and 8 white-lippedpec- differencesbetween means by post hoc Tukey tests
cary samples were collected between 18 June 1998 for unequal sample sizes. All differenceswere conand 5 May 2000 fromprimaryrainforestin the Tam- sidered significantat P < 0.05.
shiyacu-Tahuayoriver region in northeasternPeru.
Annual precipitationin this region is 261 cm.
RESULTs--Except for collared peccaries from
Upon collection, the kidney samples were the arid deserts of Arizona, no difference (P =
weighed, cut midsagittally,and preserved in 10%
0.37) in kidney mass, corrected for body mass,
bufferedformalinsolution. RMT values were deterwas found among the 3 species (Table 1). A
mined using the methods described by Sperber
difference (P < 0.05) was found be(1944). Measurements of kidneytotal length,width, significant
tween the arid-inhabiting collared peccaries
and thickness and medullary thicknesswere made
using a dial caliper. The medullary thicknessmea- and the other groups. Collared peccaries from
surement was taken at the radial extension of the arid habitats had larger kidneys in proportion
medulla fromthe tip of the renal papilla to the cor- to their body mass.
When expressed relative to body mass, RMT
ticomedullaryjunction. The original midsagittalcut
was such that the maximum area of the medulla was values of
peccaries from moist habitats (colvisible. All measurementswere made to the nearest lared and
white-lipped) were significantly low0.1 mm. RMT was calculated as 10x medullarythick- er
(P < 0.05) than those from arid or seminess/ (length X width X thickness)/3
arid habitats (Table 1). The collared and whiteRMA values were determined by the method defrom Peru's rainforest had
scribed by Brownfieldand Wunder (1976). RMA was lipped peccaries
RMT
values
of
and 1.88, respectively,while
2.14
measured by placing a 5-mmgrid over a 2X photocollared
and
Chacoan
peccaries from arid or
of
the
bisected kidney and
graphic enlargement
measuring both the medullary and cortical areas. semi-arid locations had RMT values ranging
The RMA value was obtained using the formula from 2.98 to 3.24. There was no significant difRMA = medullary area/cortical area.
ference in RMT values within this range when
Kidneysections containing both corticaland med- scaled for body mass. The same relationships
species of the genus Sylvilagus (Heisinger and
Breitenbach, 1969), ground squirrels (Spermophilus lateralis) and 3 species of the genus Tamias (Blake, 1977), 2 species of Rattus (Yabe et
al., 1985), 6 species of heteromyid rodents
(Lawler and Geluso, 1986), feral hogs (Sus scrofa) (Zervanos and Naveh, 1988), and feral
hogs and collared peccaries (Gabor et al.,
1997). Thus, comparing the RMT/RMA values
among the 3 species of peccary could reveal
the degree of xeric and non-xeric adaptability
at both the interspecific and intraspecific levels. In addition to RMT and RMA, this study
also evaluated the value of glomerular size and
density on renal adaptation.

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renalstructural
Zervanos--Peccary
adaptations

December2002

529

of3 speciesofpreccariesfrommoistto aridhabitats(mean
TABLE1-Comparisonofrenalcharacteristics
SD).
+
Collared
Arizona
n
Body mass (kg)
Kidney mass (g)
RMT
RMA
Glomerular density(number per
mm2)
Glomerular size (diameter Rm)
Habitat
Annual precipitation (cm)

18
20.1 - 1.1
37.1 ? 6.9
2.98 + 0.48
0.57
0.07
_
2.1 + 0.3
155 ? 7
Arid
19

Paraguay
21.9
29.1
3.23
0.55

5
? 1.4
? 5.7
? 0.56
? 0.05

2.7 ? 0.8
149 ? 21
Semi-Arid
65

were found using RMA values (Table 1). Using
ANOVA, RMA values were significantly
higher
for peccaries from arid and semi-aridhabitats
than for those frommoist habitats (P < 0.05).
No significantdifferencewas found in glomerular density(number) among the 3 species
(Table 1). There was no significantdifference
in glomerular size among the 3 species (Table
1) except for the collared peccaries from Peruvian rainforests,whose glomerular diameter
smaller (P < 0.05)
of 117 [Lmwas significantly
than that of the other groups.
DIscussIoN-Renal structuralindexes such
as RMT and RMA have long been used as measures of renal concentratingabilities in mammals (Brownfield and Wunder, 1976; Calder
and Braun, 1983). Blake (1977) found that
specimens of westernchipmunks ( Tamiasspp.)
from drier habitats had higher RMT values
than those from mesic habitats. By measuring
urine concentrations,she found a direct correlation between the RMT values and urineconcentratingability.However,Beuchat (1996)
challenged this relationship,arguing that because of the complexityof the mammalian kidney, renal structuralindexes (such as kidney
mass, RMT, and RMA) have limited abilityin
predicting renal function.Although I was not
able to measure renal concentratingability,relationshipsbetween renal structureand habitat
observed among the 3 species of peccary seem
to implyfunctionaladaptations.
In this study,both an interspecificand intraspecific correlation existed between environmental water availabilityand kidneystructural

Chocoan
Peru

Paraguay

7
23.8
29.9
2.14
0.37

+
+
+
?

1.2
4.7
0.38
0.03

2.4 ? 0.9
117 + 6
Moist
261

34.2
34.5
3.24
0.58

10
? 1.6
? 5.0
? 0.51
? 0.07

2.3 ? 0.4
149 ? 22
Semi-Arid
65

White-lipped
Peru
33.1
45.9
1.88
0.33

8
? 1.3
? 5.6
? 0.37
+ 0.04

1.8 ? 0.9
141 + 25
Moist
261

measures of relativemass, RMT, and RMA. Intraspecific comparisons of collared peccary
samples from the rainforestindicated lower
RMT/RMA indexes than samples from more
xeric environments. The collared peccary
RMT/RMA values from arid and semi-arid
habitats did not differsignificantlyand were
only slightlylower than the RMT value of 3.67
and RMA value of 0.62 reported by Gabor et
al. (1997) forcollared peccaries fromsemi-arid
habitats in Texas. However, comparing the 3
groups of collared peccaries, peccaries from
dry desert habitats had relativelylarger kidneys.Thus, kidneysize also seems to play a role
in renal adaptation and may be an important
adaptation to dry environments.Similar intraspecificrelationshipshave been shown in other
studies. In addition to Blake's (1977) studyon
chipmunks,Zervanos and Naveh (1988) demonstrateda direct relationshipbetween the degree of environmentalwater stressand RMT/
RMA values in feral hogs.
Blake (1977) reported a direct relationship
at the interspecificlevel between ground squirrels and chipmunks. My results also show interspecificrelationships of renal indexes and
water availability.The Chacoan peccary and
collared peccaries fromsemi-aridhabitatshad
similar RMT/RMA values. The Chacoan peccary is restrictedto the relativelysmall distribution withinSouth America's Gran Chaco. Although our specimens were froma region that
receives 65 cm of rain annually,the annual precipitationwithinthe Chacoan peccary's distribution ranges from 40 to 140 cm (Wetzel,
1977). It is possible that Chacoan peccaries

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530

The Southwestern
Naturalist

vol. 47, no. 4

from dryer or wetter habitats would demon- is unclear (Heisinger and Breitenbach, 1969).
stratesimilarintraspecificdifferencesas those Lawler and Geluso (1986) found local variafound for the collared peccary. The white- tion in renal morphology of heteromyid rolipped peccary would seem to be the least xe- dents and attributedit to sensitivityof renal
ric-adapted as measured by RMT, RMA, and function to differencesin microhabitats.This
kidney mass. Other investigatorshave found typeof phenotypicplasticityalso was observed
similar interspecificrenal adaptations to envi- by Zervanos and Neveh (1988), who found
ronmental conditions, including various spe- that the degree of environmentalwater stress
cies of Sylvilagusby Heisinger and Breitenbach during growth and development influenced
(1969), sympatricspecies of heteromyid ro- the renal morphologyin feral hogs. Gabor et
dents by Lawler and Geluso (1986), and 2 spe- al. (1997) found thatyoung collared peccaries
cies of Rattusby Yabe et al. (1985). As withthe growingunder drought conditions had higher
intraspecific relationships, interspecific rela- RMT values than those from the same area
tionships also are present between the degree growing during a rainy year. In the present
of environmentalwater stressand renal struc- study,in addition to the interspecificand inture.
traspecificdifferencesobserved, the degree of
In this study,measures of glomerular size variance in the RMT and RMA values, as meaand densitydid not appear to be usefulin eval- sured by the standard deviation (Table 1),
uating kidney function. Glomerular density seemed to be greater for animals from arid
among the 3 species did not correlatewithen- and semi-arid habitats and smaller for those
vironmentalwater availability.Glomerular size frommoist tropical habitats.This would be exvaried inverselyto the availabilityof wateronly pected, because arid and semi-aridhabitatsexin the collared peccary. Small glomeruli are
pose the peccaries to a more heterogeneous
present in human kidneyswith low functional array of both spatial and temporal microclidemands and significantly
largerglomeruliare mates (in terms of temperature and water
in
with
kidneys
high demands (Wil- availability)than do tropical rainforests.Howpresent
trakis,1972). Red kangaroos (Macropusrufus), ever, F-distribution analysis indicated that
withhigher renal concentrationdemands than there was no
significantdifference(P = 0.17)
other kangaroos,have higherglomerularfiltra- between these standard deviations,
possibly
tion rates (GFR) that correlated with the oc- due to small
sample sizes. The effectof habitat
currence of larger and more numerous gloheterogeneityon structuralvariationswarrants
meruli (Denny and Dawson, 1977). However, further
investigationwith larger samples, and
Zervanos and Naveh (1988) found that feral it
might furthersupport the contention that
hogs frommore xeric environmentshad small- the length of the loop of Henle has a high
er glomeruli than those from less xeric envisensitivityto environmental variation, which
ronments. In addition, Abdulla and Abdulla
mightdecrease the degree of heritabilityin re(1979) compared the camel (Camelusdromedar- nal concentratingabilities.
ius) withother mammals and reported thatthe
It is apparent that in many mammals, renal
number and size of glomeruli did not have a structure is flexible in
response to environdirect influence on the abilityto produce con- ment variation.
Clarifyingthe adaptive significentrated urine. In peccaries, it would appear cance of this
flexibilityin termsof genetic inthat glomerular size and number are less imfluence and links to functionwould provide a
portant to renal adaptation than is the length better
understanding of renal physiologyand
of the loop of Henle (as measured by RMT)
its ecological significance.
or relativekidneymass.
This studyfurthersupports the relationship
The authorwishesto acknowledgethe valuable
between kidneymass, RMT, RMA and the enassistanceof Dr. J.J.Mayerforthecollectionofthe
vironment. Changes in water availabilityap- Chacoan
peccarykidneysamples;J.
Dayand S. Belfit
pear to provide a selection pressure for adap- for the collectionof the collared peccarykidney
tation. However, relating renal structure to samplesfromArizona;Dr. R. Bajema and R. Flores
function needs more empirical studies. In ad- Lozano for the white-lipped
and collaredpeccary
dition, the degree of genetic versus environ- samples from Peru; and J. Brown for assistance in
mental influence on this phenotypicvariance the kidneyanalysis.Also, a special thanksis given to

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December2002

renalstructural
Zervanos-Peccary
adaptations

Drs. T. Gabor and C. Salsburyfortheirreviewof the
manuscript.
LITERATURECITED
ABDULLA,M. A., AND O. ABDULLA.1979. Morphometric observations on the kidney of the camel
Camelusdromedarius.
Journal of Anatomy129:4550.
BEUCHAT,C. A. 1996. Structure and concentrating
ability of the mammalian kidney: correlations
withhabitat.AmericanJournal of Physiology271:
157-179.
BLAKE,B. H. 1977. The effectsof kidney structure
and the annual cycle on water requirements in
golden-mantled ground squirrels and chipmunks. Comparative Biochemistryand Physiology [A] 58:413-419.
BROWNFIELD,M. S., AND B. A. WUNDER. 1976. Relative
medullary area: a new structuralindex for estimating urinary concentration capacity of mammals. Comparative Biochemistryand Physiology
[A] 55:69-75.
CALDER,W. A., III, ANDE. J. BRAUN. 1983. Scaling of
osmotic regulation in mammals and birds.American Journal of Physiology244:601-606.
DENNY,M. J. S., ANDT.J. DAWSON.1977. Kidneystructure and functionof desert kangaroos.Journal of
Applied Physiology42:636-642.
ANDN. J. SILVY.1997.
GABOR,T. M., E. C. HELLGREN,
Renal morphology of sympatricsuiforms:implications for competition.Journal of Mammalogy
78:1089-1095.
1969. Renal
HEISINGER,
J.F., ANDR. P. BREITENBACH.
structuralcharacteristicsas indexes of renal ad-

531

aptation for water conservation in the genus Sylvilagus.PhysiologicalZoology 42:160-172.
LAWLER,R. M., ANDK. N. GELUSO.1986. Renal structure and body size in heteromyidrodents.Journal of Mammalogy 67:367-372.
distriMAYER,J.J.,AND P. N. BRANDT. 1982.Identity,
bution and natural historyof the peccaries, Tayassuidae. In: Mares, M. A., and H. H. Genoways,
editors. Mammalian biology in South America.
Universityof PittsburghPress, Pittsburgh,Pennsylvania.Pp. 547-584.
SOWLs,L. K. 1997. Javelinasand other peccaries, second edition. Texas A&M UniversityPress,College
Station.
SPERBER,
I. 1944. Studies on the mammalian kidney.
Zoologiska Bidrag Fran Uppsala 22:249-432.
WETZEL,R. M. 1977. The Chacoan peccary, Catagonus wagneri(Rusconi). Bulletin Carnegie Museum
of Natural History3:1-36.
WILTRAKIS, M. G. 1972. Correspondence between
glomerular size and renal volumes in atrophic,
normal, and hypertrophichuman kidneys.Acta
Pathology,Microbiology and Immunology Scandanavia [A] 80:801-811.
YABE, T., M. CHENCHITTIKUL,AND B. PHANTHUMACHIN-

DA. 1985. Water requirementand its relationship
to habitat performance in Rattus norvegicus
and
R exulans in Chanthaburi Province, Thailand.
Japanese Journal of Sanitary Zoology 364(4):
285-288.

ZERVANOS, S. M., AND S. NAVEH. 1988. Renal struc-

tural flexibilityin response to environmentalwater stressin feral hogs. Journal of Experimental
Zoology 247:285-288.

22 May 2001. Accepted18 October2001.
Submitted
AssociateEditorwas CheriA. Jones.

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