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Kidney structure and allometry of Argentine desert rodents
Journal of Arid Environments (1999) 41: 453–461 Article No. jare.1998.0472 Available online at http://www.idealibrary.com on
Kidney structure and allometry of Argentine desert rodents
Gabriela B. Diaz* & Ricardo A. Ojeda Grupo de Investigaciones de Biodiversidad, Instituto Argentino de Investigaciones de las Zonas Aridas, CONICET, CC 507, 5500 Mendoza, Argentina (Received 13 January 1998, accepted 10 November 1998) Two large groups of rodents inhabit South America: the hystricognaths and the murids. It has been postulated that while the former show a high degree of specialization to desert habitats, the murids are not well adapted to xeric conditions. We studied the renal structure and function of selected desertdwelling murid and octodontid (hystricognath) rodents from Argentina to evaluate levels of adaptation to aridity. Our results show that the murids Salinomys, Andalgalomys, Calomys and Eligmodontia have the highest renal indices and urine concentration among Argentine desert rodents. The octodontid Tympanoctomys barrerae shows higher renal indices and urine osmolarity than those of its close relatives Octomys mimax and Octodontomys gliroides. We compare the renal traits of the Argentine desert murids with those of other world-desert rodents such as North American heteromyid rodents. The results show that these Argentine murid rodents posses renal adaptations to conditions which are as impressive as those of both octodontids and the classic desert-adapted heteromyids. 1999 Academic Press Keywords: renal morphology; arid habitats; murids; octodontids; body size
Introduction Mammalian kidneys control the concentration of the body fluids. Some arid-adapted small mammals are efficient at concentrating urine in order to reduce water loss. Their unilobular kidneys have elongated renal papillae, i.e. thicker medulla (Sperber, 1944; McMillen & Lee, 1969; Geluso, 1978; Brooker & Withers, 1994). According to the countercurrent multiplier model, the ability to concentrate urine depends on the length of the loops of Henle and collecting ducts that traverse the renal medulla (Schmidt-Nielsen et al., 1961). The maximum length of the loop of Henle is directly proportional to medullary thickness (Beuchat, 1990). Medullary thickness has been used to propose several indices of renal performance (Sperber, 1944; Brownfield & Wunder, 1976; Geluso, 1978). Higher indices are typical of desert small rodents. However, other morphological characteristics besides maximum nephron length affect the urinary concentrating ability (Bankir & Rouffignac, 1985). *(E-mail: [email protected]). 0140}1963/99/040453#09 $30.00/0
1999 Academic Press
454
G. B. DIAZ & R. A. OJEDA
Most variations in gross renal structure in mammals can be explained by variations in body mass, but it is also influenced by habitat and food habits (Beuchat, 1996). The ability to concentrate urine is inversely related to body mass (Calder, 1984). Absolute medullary thickness increases with increasing body mass, and conversely medullary thickness (RMT) decreases with increasing body mass (Greegor, 1975; Beuchat, 1990), suggesting that, in general, small species have more powerfully-concentrating kidneys than do large species. The RMT’s of mammals living in arid areas are greater than those of similar-sized mammals from more mesic areas (Sperber, 1944). Blake (1977) found this relation to also be true at the intraspecific level. Renal morphology and allometry have been studied in different taxa of small desert mammals, including Australian marsupials, and North American heteromyid and sciurid rodents (Blake, 1977; Lawler & Geluso, 1986; Brooker & Withers, 1994). There are few studies of small to medium-sized mammals from xeric habitats of South America (Cortes et al., 1990; Greegor, 1975). The South American desert rodent fauna is composed of two major lineages: the hystricognaths and the murids. Current wisdom regarding desert rodent adaptations has it that murids are not highly specialized for life in xeric habitats due to their relatively recent colonization of these habitats (Mares, 1975, 1976), assuming colonization of the continent after the completion of the Panama land bridge (c. 3·5 million years ago; Marshall et al., 1979). Data on octodontid (hystricognath) rodents, on the other hand, indicate a high degree of desert specialization (Mares et al., 1997; Ojeda et al., 1996). Octodontids have been associated with desert habitats since the Oligocene (Patterson & Pascual, 1972), and therefore probably far longer periods than have South American murids. In the present study, variations in the renal structure of 13 species of desert murids and octodontid (hystricognath) rodents from Argentina are analysed. In particular, we analyse the allometry of renal structure and compare it to other groups of mammals, especially rodents from other deserts. Materials and methods Thirteen rodent species (four octodontids and nine murids) were captured using Sherman live traps and Museum Special snap traps in several arid and semi-arid sites of Argentina in the lowland Monte Desert, the highland desert or Puna, and the semi-arid thornscrub or Chaco (Table 1). All specimens were preserved as skins, skulls and skeletons and housed in the Instituto Argentino de Investigaciones de las Zonas Aridas (IADIZA) Mammal Collection, Mendoza, Argentina. Most species are herbivorous, with the exception of the grass mouse Akodon molinae that incorporates approximately 30% of arthropods in its diet (Campos, 1997). Anatomical procedures Both kidneys from adult animals were removed within 24 h of death and fixed in 10% formaldehyde. Length, width and thickness of the kidneys were measured with a dial caliper to the nearest 0·5 mm. Sections along the frontal axis through the longest part of the renal papilla were obtained from the left kidney, but if a complete saggital section could not be made, the right kidney was used. Thickness of the cortex (CT), outer zone of the medulla and inner zone of the medulla were distinguishable when viewed through a stereoscopic microscope (6;); medulla thickness (MT) is the sum of the values of outer and inner medulla. The outline of the entire kidney, including the corticomedullary junction, and the outer and inner boundaries of the medulla were traced on paper using a camera lucida attached to a stereoscopic microscope (Geluso, 1978). The
Ctenomys eremophilus Octomys mimax Octodontomys gliroides Tympanoctomys barrerae
Octodontidae
Muridae Akodon molinae Andalgalomys olrogi Andalgalomys roigi Calomys musculinus Eligmodontia moreni Eligmodontia typus Graomys griseoflavus Phyllotis xanthopygus Salinomys delicatus
Species
N acun an, Mendoza Ischigualasto, San Juan Saladillo, Jujuy Nihuil, Mendoza
N acun an, Mendoza Amanao, Catamarca La Antigua, La Rioja N acun an, Mendoza Talampaya, La Rioja N acun an, Mendoza N acun an, Mendoza Talampaya, La Rioja La Antigua, La Rioja
Collecting localities
34302 29347 23343 35302
S, S, S, S,
34302 S, 27333 S, 30302 S, 34302 S, 29347 S, 34302 S, 34302 S, 29347 S, 30302 S, 67358 67354 65306 68340
W W W W
67358 W 66331 W 66304 W 67358 W 67354 W 67358 W 67358 W 67354 W 66304 W
Coordinates
Monte Monte Puna Monte
Monte Monte Chaco Monte Monte Monte Monte Monte Chaco
Biomes
300}400 mm 100}200 mm 200}300 mm 200}300 mm
300}400 mm 200}300 mm 300}400 mm 300}400 mm 100}200 mm 300}400 mm 300}400 mm 100}200 mm 300}400 mm
Rainfall range (mm)
Table 1. Species of Argentina desert rodents examined: collecting localities, coordinates, biomes and precipitation
KIDNEY STRUCTURE OF ARGENTINE DESERT RODENTS 455
456
G. B. DIAZ & R. A. OJEDA
thickness of each zone was measured with a ruler (0·5 mm). The area of each zone was measured with a LI-COR 3000A portable area meter. The following indices were calculated: relative medullary thickness (RMT"medullary thickness;10/cube root of the product of kidney length, width and thickness); ratio of inner medulla to cortex (MI/C); and relative medullary area (RMA"medullary area/cortical area) (Sperber, 1944; Brownfield & Wunder, 1976; Geluso, 1978). Urine concentration Urine samples of Tympanoctomys barrerae (N"9, 51 samples), Octomys mimax (N"7, 18 samples), Eligmodontia typus (N"16, 33 samples), Calomys musculinus (N"5, 18 samples) and Salinomys delicatus (N"1, 2 samples) were collected in Petri dishes placed under the wire-grid floor of the animals’ cages and covered with a layer of mineral oil to prevent evaporation. After 24 h the urine was pipetted into capped plastic vials, avoiding samples contaminated by faeces. The osmolarity of the urine (mosm/l) was determined on a vapour pressure osmometer (Wescor) using dilutions in distilled water. Maximum values were obtained from the field in the case of octodontids and from the laboratory in the case of murids (maintained on a diet of sunflower seeds). Statistical analysis Relationships between log-transformed data of body mass (M) and renal characteristics (CT, MT, RMT, MI/C and RMA) were assessed by Pearson’s correlation analysis. Least-squares regression analysis was performed for all the Argentine desert rodents. The allometric equations are of the form log y"log a#b log M (M"body mass in g). Comparisons among slopes and intercepts were made with the t test (Zar, 1984). Statistical analyses were performed using STATISTICA program version 5.0. Results Renal morphology Kidneys of the Argentine desert rodents studied show a single renal papilla and a medulla divided in two zones (Fig. 1). The delicate mouse, Salinomys delicatus, has the most elongated papillae and the highest renal indices (MI/C, RMT and RMA) among the murids in this sample. The same is true for the red vizcacha rat, Tympanoctomys barrerae, among the octodontids (Table 2). On the other hand, shorter papillae are associated with lower renal indices, as in Akodon molinae (murid) and Octomys mimax (octodontid; Fig. 1). Allometry Pearson’s correlation coefficients between mean cortex thickness, renal indices (RMT, MI/C and RMA) and mean body mass of Argentine desert rodents (murids and octodontids) were consistently significant (Table 3). Thus, smaller species have a thinner cortex and greater indices, but not more developed medullary thickness compared to larger rodents (Table 3). No significant correlation was found between renal morphological characteristics of octodontids and body mass. Renal indices of Argentine murids correlates significantly with body mass (MI/C: R"0·86, N"9, p"0·029; RMA: R"0·708, N"9,
KIDNEY STRUCTURE OF ARGENTINE DESERT RODENTS
457
Figure 1. Renal morphology of four selected murid (Salinomys delicatus, Akodon molinae) and octodontid rodent species (Tympanoctomys barrerae, Octomys mimax). C"cortex; M"outer medulla; Mi"inner medulla.
p"0·033; RMT: R"0·656, N"9, p"0·055). The RMT vs. M regression line for Argentine murid (log RMT"1·289!0·167 log M; R"0·656, N"9, p"0·055) is used to compare with North American heteromyids (log RMT"1·195!0·1695 log M; R"0·976, N"6, p"0·0015) (Lawler & Geluso, 1986). Slopes did not differ significantly (b "!0·17, p'0·05) but intercepts did (t"1·99, df."76, p(0·05). A This indicates that the lines of Argentine murids and heteromyids are parallel but not coincident. Therefore, Argentine desert murids show higher RMT than do desert heteromyids. Urine concentration Maximum values of urine osmolarity are shown in Table 4. Discussion The high renal indices and maximum urine osmolarity of Calomys musculinus and Eligmodontia typus (Tables 2 and 4) correspond with the physiological ability of Calomys musculinus to survive on a diet of seeds and the ability of Eligmodontia typus to tolerate highly concentrated (2)00 M) solutions of salt (Mares, 1977a,b). The high renal indices of Salinomys delicatus, Andalgalomys roigi and Andalgalomys olrogi show that the kidneys of these desert murids are also highly specialized for desert existence. Moreover, their renal indices and maximum urine osmolarity are among the highest values reported for other desert rodents (Table 4; Fig. 2). Among octodontids, the red vizcacha rat, Tympanoctomys barrerae possesses a kidney with a long broad renal papilla and produces highly concentrated urine. These renal attributes are similar to those of the fat sand rat Psammomys obesus (Table 4; Fig. 2) that excretes a large amount of fluid with a high concentration of salt (Schmidt-Nielsen, 1961). Both species have a specialized diet of halophytic chenopods and live in salt dunes habitats (Ojeda et al., 1996; Mares et al., 1997). Close relatives of Tympanoctomys barrerae, such as Octomys mimax and Octodontomys gliroides, have less-developed renal
16 (12) 11 (6) 14 (11) 1
1 11(6) 14(10) 12 (10) 1 1 14 (7) 3 28 (25)
N
86·79$1·00 98·32$1·57 121·18$2·26 153·00
12·50 12·73$0·27 14·50$0·13 18·58$0·25 23·00 28·00 31·11$0·35 44·00$4·67 54·50$0·37
M (g)
1·72$0·01 1·74$0·02 1·97$0·04 1·83
0·83 0·82$0·02 0·99$0·01 0·80$0·01 1·17 1·33 1·17$0·03 1·63$0·02 1·44$0·01
CT (mm)
12·38$0·07 6·38$0·08 9·61$0·07 6·83
7·83 6·94$0·04 6·72$0·12 6·97$0·05 8·66 8·66 7·01$0·05 8·44$0·36 8·72$0·03
MT (mm)
9·41$0·07 6·09$0·06 8·98$0·08 5·35
13·98 12·29$0·10 10·66$0·21 11·42$0·11 13·48 12·60 10·09$0·08 10·10$0·47 9·64$0·04
RMT
5·00$0·06 2·58$0·03 3·91$0·07 3·19
7·02 6·58$0·38 5·32$0·12 6·36$0·08 5·84 4·01 4·27$0·22 3·68$0·19 4·24$0·04
MI/C
1·73$0·03 0·83$0·01 0·75$0·02 1·03
1·69 1·47$0·04 1·63$0·06 1·63$0·04 1·18 1·06 1·44$0·04 0·96$0·07 1·27$0·01
RMA
M"body mass; CT"cortex thickness; MT"medullary thickness; RMT"relative medullary thickness; MI/C"ration of inner medulla cortex; RMA"relative medullary area.
Tympanoctomys barrerae Octomys mimax Ctenomys eremophilus Octodontomys gliroides
Octodontidae
Salinomys delicatus Calomys musculinus Eligmodontia moreni Eligmodontia typus Andalgalomys olrogi Andalgalomys roigi Akodon molinae Phyllotis xanthopygus Graomys griseoflavus
Muridae
Species
Table 2. Renal indices (s$SE) for the desert rodents of Argentina. Number of individuals are indicated in parentheses when the numbers for MI/C or RMA were different
458 G. B. DIAZ & R. A. OJEDA
KIDNEY STRUCTURE OF ARGENTINE DESERT RODENTS
459
Table 3. Allometry of renal morphology of the 13 species of desert rodents from Argentina
CT MT RMT MI/C RMA
a
b
R
F
p
!0)44$0)061 0)80$0)098 1)425$0)087 1)093$0)099 0)420$0)119
0)347$0)038 0)063$0)061 !0)269$0)054 !0)273$0)061 !0)207$0)073
0)94 0)30 0)83 0)80 0)65
84)036 1)0884 25)138 20)172 7)946
(0)0001 0)319 0)0004 0)0009 0)0167
CT"cortex thickness; MT"medullary thickness; RMT"relative medullary thickness; MI/C"ratio inner medulla/cortex; RMA"relative medullary area.
papilla (Fig. 2), low renal indices and low urine concentration (Table 4). This may reflect a water-rich diet of cacti, as found in the wood rat Neotoma lepida (Stallone, 1979; Ojeda et al., 1999). The pattern of decreasing renal indexes and an increase in cortex thickness with increasing body mass in Argentine desert rodents agrees with previous studies for different taxa of mammals (Greegor, 1975; Lawler & Geluso, 1986; Brooker & Withers, 1994). However, Argentine desert rodents show higher slopes than mammals of xeric habitats (Beuchat, 1996). They also do not show a relatively more developed medullary thickness compared to larger rodents, as has been reported for mammals (Beuchat, 1990). The smaller range of body mass considered in our study may account for these differences. Compared with heteromyids, Argentine murids exhibit higher RMT and metabolic rate (Bozinovic & Rosenmann, 1988; Bozinovic, 1992). This may explain the different intercept values for murids and heteromyids in the regression line. Granivorous heteromyids have low metabolic rate and low evaporative water loss, thereby facilitating water conservation (Hinds & MacMillen, 1985). Higher metabolic rates in Argentine desert rodents result in greater respiratory exchange and concomitant increases in water loss. More efficient kidneys (i.e. higher RMT) may compensate for high evaporative water loss. Table 4. Maximum urine osmolarity (mosm/l) of desert rodents
Species
Maximum urine osmolarity (mosm/1)
Source
Muridae Calomys musculinus Eligmodontia typus Salinomys delicatus Notomys alexis Psammomys obesus
8773 8612 7440 9370 6340
This study This study This study MacMillen & Lee, 1967 Schmidt-Nielsen, 1964
7080 2071
This study This study
7500 5540
Altschuler et al., 1979 Schmidt-Nielsen, 1964
Octodontidae Tympanoctomys barrerae Octomys mimax Heteromyidae Perognathus penicillatus Dipodomys merriami
460
G. B. DIAZ & R. A. OJEDA
Figure 2. Relationship between mean relative medullary thickness, and mean body mass for Argentine desert rodents (this study, solid line) and similar sized non-Argentine desert rodents. (䊉)"Argentine Muridae: Sd"Salinomys delicatus; Cm"Calomys musculinus; Em"Eligmodontia moreni; Et"Eligmodontia typus; Ao"Andalgalomys olrogi; Ar"Andalgalomys roigi; Am"Akodon molinae; Px"Phyllotis xanthopygus; Gg"Graomys griseoflavus; (䊊)"Octodontidae: Tb"Tympanoctomys barrerae; Om"Octomys mimax; Ce"Ctenomys eremophilus; Og"Octodontomys gliroides; (䊏)"Non-Argentina Muridae: Na"Notomys alexis; Nc"Notomys cervinus (MacMillen & Lee, 1969); Ps"Psammomys obesus (Sperber, 1944); (䉱)"Heteromyidae, Dm"Dipodomys merriami; Mp"Microdipodops pallidus; Pi"Perognathus longimembris (Lawler & Geluso, 1986).
In conclusion, the renal morphology and function of Argentine desert rodents, either murids or octodontids, evidence the capacity for reducing water loss. Moreover, it is suggested that these renal specializations to arid habitats are independent of the time of South American rodent colonization. The authors thank our fellow colleagues of the Biodiversity Research Group, C. Campos and C. Borghi, for their critical comments, suggestions and statistical advice on earlier drafts of the manuscript. We also thank Drs P. Hanford and M. Willig. Ana M. Scollo kindly helped with the extraction of kidneys, and M. Gallardo kindly provided some animals. We thank Dra P. Valles, Dept. Physiopathology, University of Cuyo, for the loan of the vapour pressure osmometer Wescor 5500, and Ing. Cavagnaro, Plant Physiology Dept., University of Cuyo, for the loan of the area meter. We thank D. Duen as and R. Marti (Magraf) for helping with figures. This project was partially funded by the National Council of Scientific and Technical Investigations (CONICET, Argentina) grants PID 3363800 and PIP 4684.
References Altschuler, E.M., Nagle, R.B., Braun, E.J., Lindstedt, S.L. & Krutzsch, P.H. (1979). Morphological study of desert heteromyid kidney with emphasis on the genus Perognathus. Anatomical Record, 194: 461}468. Bankir, L. & Rouffignac, C. (1985). Urinary concentrating ability: insights from comparative anatomy. American Journal of Physiology, 249: R643}R666. Beuchat, C.A. (1990). Body size, medullary thickness, and urine concentrating ability in mammals. American Journal of Physiology, 258: R298}R308. Beuchat, C.A. (1996). Structure and concentrating ability of the mammalian kidney: correlations with habitat. Americal Journal of Physiology, 271: R157}R179.
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Blake, B.H. (1977). The effects of kidney structure and annual cycle on water requirements in golden-mantled ground squirrels and chipmunks. Comparative Biochemistry and Physiology, 58A: 413}419. Bozinovic, F. (1992). Rate of metabolism of grazing rodents from different habitats. Journal of Mammalogy, 73: 379}384. Bozinovic, F. & Rosenmann, M. (1988). Comparative bioenergetics of South American cricetid rodents. Comparative Biochemistry and Physiology, 91A: 195}202. Brooker, B. & Withers, P. (1994). Kidney structure and renal indices of dasyurid marsupials. Australian Journal of Zoology, 42: 163}176. Brownfield, M.S. & Wunder, B.A. (1976). Relative medullary area: a new structural index for estimating urinary concentrating capacity of mammals. Comparative Biochemistry and Physiology, 55: 69}75. Calder, W.A.III. (1984). Size, Function, and Life History. Cambridge: Harvard University Press. 431 pp. Campos, C. (1997). UtilizacioH n de recursos alimetarios por mammH feros medianos y pequen os del desierto del Monte. Doctoral thesis, Universidad Nacional de CoH rdoba. 183 pp. CorteH s, A., Rosenmann, M. & Baez, C. (1990). FuncioH n del rin oH n y del pasaje nasal en la conservacioH n de agua corporal en roedores simpaH tridos de Chile central. Revista Chilena de Historia Natural, 63: 279}291. Geluso, K.N. (1978). Urine concentrating ability and renal structure of insectivorous bats. Journal of Mammalogy, 59: 312}323. Greegor, D.H. (1975). Renal capabilities of an Argentine desert armadillo. Journal of Mammalogy, 56: 626}632. Hinds, D.S. & MacMillen, R.E. (1985). Scaling of energy metabolism and evaporative water loss in heteromyid rodents. Physiological Zoology, 58: 282}298. Lawler, R.M. & Geluso, K.N. (1986). Renal structure and body size in heteromyid rodents. Journal of Mammalogy, 67: 367}372. MacMillen, R.E. & Lee, A.K. (1967). Australian desert mice: independence of exogenous water. Science, 158: 383}385. MacMillen, R.E. & Lee, A.K. (1969). Water metabolism of Australian hopping mice. Comparative Biochemistry and Physiology, 28: 493}514. Mares, M.A. (1975). South American mammal zoogeography: evidence from convergent evolution in desert rodents. Proceedings National Academy of Sciences, 72: 1702}1706. Mares, M.A. (1976). Convergent evolution of desert rodents: multivariate analysis and zoogeographic implications. Paleobiology, 2: 39}63. Mares, M.A. (1977a). Water economy and salt balance in a South American desert rodent, Eligmodontia typus. Comparative Biochemistry and Physiology, 56A: 325}332. Mares, M.A. (1977b). Water independence in a South American non-desert rodent. Journal of Mammalogy, 58: 653}656. Mares, M.A., Ojeda, R.A., Borghi, C.E., Giannoni, S., Diaz, G.B. & Braun, J.K. (1997). A desert rodent uses hair as a tool to overcome halophytic plant defenses. BioScience, 47: 699}704. Marshall, L.G., Butler, R.F., Drake, R.E., Curtis, G.G. & Tedford, R.H. (1979). Calibration of the Great American Interchange. Science, 204: 272}279. Ojeda, R.A., Gonnet, J., Borghi, C.E., Giannoni, S.M., Campos, C. & Diaz, G.B. (1996). Ecological observations of the red vizcacha rat Tympanoctomys barrerae in two desert habitats of Argentina. Mastozoologn& a Neotropical, 3: 183}191. Ojeda, R.A., Borghi, C.E., Diaz, G.B., Giannoni, S.M., Mares, M.A. & Braun, J.K. (1999). Evolutionary convergence of the highly adapted desert rodent Tympanoctomys barrerae (Octodontidae). Journal of Arid Environments, 41: 443}452. Patterson, B. & Pascual, R. (1972). The fossil mammal fauna of South America. In: Keast, A., Erk, E. & Glass, B. (Eds), Evolution, mammals and Southern continents, pp. 247}309. Albany Publications, State University New York Press. Schmidt-Nielsen, B., O’Dell, R. & Osaki, H. (1961). Structure and concentrating mechanism in the mammalian kidney. American Journal of Physiology, 200: 1119}1124. Schmidt-Nielsen, K. (1964). Desert animals: physiological problems of heat and water. London: Oxford University Press. 277 pp. Sperber, I. (1944). Studies on the mammalian kidney. Zoologiska Bidrag fran Uppsala, 22: 249}431. Stallone, J.N. (1979). Seasonal changes in water metabolism of woodrats. Oecologia, 38: 203}216. Zar, J.H. (1984). Biostatistical analysis. Second edition. Prentice-Hall International, Inc. 718 pp.
Kidney structure and allometry of Argentine desert rodents
Gabriela B. Diaz* & Ricardo A. Ojeda Grupo de Investigaciones de Biodiversidad, Instituto Argentino de Investigaciones de las Zonas Aridas, CONICET, CC 507, 5500 Mendoza, Argentina (Received 13 January 1998, accepted 10 November 1998) Two large groups of rodents inhabit South America: the hystricognaths and the murids. It has been postulated that while the former show a high degree of specialization to desert habitats, the murids are not well adapted to xeric conditions. We studied the renal structure and function of selected desertdwelling murid and octodontid (hystricognath) rodents from Argentina to evaluate levels of adaptation to aridity. Our results show that the murids Salinomys, Andalgalomys, Calomys and Eligmodontia have the highest renal indices and urine concentration among Argentine desert rodents. The octodontid Tympanoctomys barrerae shows higher renal indices and urine osmolarity than those of its close relatives Octomys mimax and Octodontomys gliroides. We compare the renal traits of the Argentine desert murids with those of other world-desert rodents such as North American heteromyid rodents. The results show that these Argentine murid rodents posses renal adaptations to conditions which are as impressive as those of both octodontids and the classic desert-adapted heteromyids. 1999 Academic Press Keywords: renal morphology; arid habitats; murids; octodontids; body size
Introduction Mammalian kidneys control the concentration of the body fluids. Some arid-adapted small mammals are efficient at concentrating urine in order to reduce water loss. Their unilobular kidneys have elongated renal papillae, i.e. thicker medulla (Sperber, 1944; McMillen & Lee, 1969; Geluso, 1978; Brooker & Withers, 1994). According to the countercurrent multiplier model, the ability to concentrate urine depends on the length of the loops of Henle and collecting ducts that traverse the renal medulla (Schmidt-Nielsen et al., 1961). The maximum length of the loop of Henle is directly proportional to medullary thickness (Beuchat, 1990). Medullary thickness has been used to propose several indices of renal performance (Sperber, 1944; Brownfield & Wunder, 1976; Geluso, 1978). Higher indices are typical of desert small rodents. However, other morphological characteristics besides maximum nephron length affect the urinary concentrating ability (Bankir & Rouffignac, 1985). *(E-mail: [email protected]). 0140}1963/99/040453#09 $30.00/0
1999 Academic Press
454
G. B. DIAZ & R. A. OJEDA
Most variations in gross renal structure in mammals can be explained by variations in body mass, but it is also influenced by habitat and food habits (Beuchat, 1996). The ability to concentrate urine is inversely related to body mass (Calder, 1984). Absolute medullary thickness increases with increasing body mass, and conversely medullary thickness (RMT) decreases with increasing body mass (Greegor, 1975; Beuchat, 1990), suggesting that, in general, small species have more powerfully-concentrating kidneys than do large species. The RMT’s of mammals living in arid areas are greater than those of similar-sized mammals from more mesic areas (Sperber, 1944). Blake (1977) found this relation to also be true at the intraspecific level. Renal morphology and allometry have been studied in different taxa of small desert mammals, including Australian marsupials, and North American heteromyid and sciurid rodents (Blake, 1977; Lawler & Geluso, 1986; Brooker & Withers, 1994). There are few studies of small to medium-sized mammals from xeric habitats of South America (Cortes et al., 1990; Greegor, 1975). The South American desert rodent fauna is composed of two major lineages: the hystricognaths and the murids. Current wisdom regarding desert rodent adaptations has it that murids are not highly specialized for life in xeric habitats due to their relatively recent colonization of these habitats (Mares, 1975, 1976), assuming colonization of the continent after the completion of the Panama land bridge (c. 3·5 million years ago; Marshall et al., 1979). Data on octodontid (hystricognath) rodents, on the other hand, indicate a high degree of desert specialization (Mares et al., 1997; Ojeda et al., 1996). Octodontids have been associated with desert habitats since the Oligocene (Patterson & Pascual, 1972), and therefore probably far longer periods than have South American murids. In the present study, variations in the renal structure of 13 species of desert murids and octodontid (hystricognath) rodents from Argentina are analysed. In particular, we analyse the allometry of renal structure and compare it to other groups of mammals, especially rodents from other deserts. Materials and methods Thirteen rodent species (four octodontids and nine murids) were captured using Sherman live traps and Museum Special snap traps in several arid and semi-arid sites of Argentina in the lowland Monte Desert, the highland desert or Puna, and the semi-arid thornscrub or Chaco (Table 1). All specimens were preserved as skins, skulls and skeletons and housed in the Instituto Argentino de Investigaciones de las Zonas Aridas (IADIZA) Mammal Collection, Mendoza, Argentina. Most species are herbivorous, with the exception of the grass mouse Akodon molinae that incorporates approximately 30% of arthropods in its diet (Campos, 1997). Anatomical procedures Both kidneys from adult animals were removed within 24 h of death and fixed in 10% formaldehyde. Length, width and thickness of the kidneys were measured with a dial caliper to the nearest 0·5 mm. Sections along the frontal axis through the longest part of the renal papilla were obtained from the left kidney, but if a complete saggital section could not be made, the right kidney was used. Thickness of the cortex (CT), outer zone of the medulla and inner zone of the medulla were distinguishable when viewed through a stereoscopic microscope (6;); medulla thickness (MT) is the sum of the values of outer and inner medulla. The outline of the entire kidney, including the corticomedullary junction, and the outer and inner boundaries of the medulla were traced on paper using a camera lucida attached to a stereoscopic microscope (Geluso, 1978). The
Ctenomys eremophilus Octomys mimax Octodontomys gliroides Tympanoctomys barrerae
Octodontidae
Muridae Akodon molinae Andalgalomys olrogi Andalgalomys roigi Calomys musculinus Eligmodontia moreni Eligmodontia typus Graomys griseoflavus Phyllotis xanthopygus Salinomys delicatus
Species
N acun an, Mendoza Ischigualasto, San Juan Saladillo, Jujuy Nihuil, Mendoza
N acun an, Mendoza Amanao, Catamarca La Antigua, La Rioja N acun an, Mendoza Talampaya, La Rioja N acun an, Mendoza N acun an, Mendoza Talampaya, La Rioja La Antigua, La Rioja
Collecting localities
34302 29347 23343 35302
S, S, S, S,
34302 S, 27333 S, 30302 S, 34302 S, 29347 S, 34302 S, 34302 S, 29347 S, 30302 S, 67358 67354 65306 68340
W W W W
67358 W 66331 W 66304 W 67358 W 67354 W 67358 W 67358 W 67354 W 66304 W
Coordinates
Monte Monte Puna Monte
Monte Monte Chaco Monte Monte Monte Monte Monte Chaco
Biomes
300}400 mm 100}200 mm 200}300 mm 200}300 mm
300}400 mm 200}300 mm 300}400 mm 300}400 mm 100}200 mm 300}400 mm 300}400 mm 100}200 mm 300}400 mm
Rainfall range (mm)
Table 1. Species of Argentina desert rodents examined: collecting localities, coordinates, biomes and precipitation
KIDNEY STRUCTURE OF ARGENTINE DESERT RODENTS 455
456
G. B. DIAZ & R. A. OJEDA
thickness of each zone was measured with a ruler (0·5 mm). The area of each zone was measured with a LI-COR 3000A portable area meter. The following indices were calculated: relative medullary thickness (RMT"medullary thickness;10/cube root of the product of kidney length, width and thickness); ratio of inner medulla to cortex (MI/C); and relative medullary area (RMA"medullary area/cortical area) (Sperber, 1944; Brownfield & Wunder, 1976; Geluso, 1978). Urine concentration Urine samples of Tympanoctomys barrerae (N"9, 51 samples), Octomys mimax (N"7, 18 samples), Eligmodontia typus (N"16, 33 samples), Calomys musculinus (N"5, 18 samples) and Salinomys delicatus (N"1, 2 samples) were collected in Petri dishes placed under the wire-grid floor of the animals’ cages and covered with a layer of mineral oil to prevent evaporation. After 24 h the urine was pipetted into capped plastic vials, avoiding samples contaminated by faeces. The osmolarity of the urine (mosm/l) was determined on a vapour pressure osmometer (Wescor) using dilutions in distilled water. Maximum values were obtained from the field in the case of octodontids and from the laboratory in the case of murids (maintained on a diet of sunflower seeds). Statistical analysis Relationships between log-transformed data of body mass (M) and renal characteristics (CT, MT, RMT, MI/C and RMA) were assessed by Pearson’s correlation analysis. Least-squares regression analysis was performed for all the Argentine desert rodents. The allometric equations are of the form log y"log a#b log M (M"body mass in g). Comparisons among slopes and intercepts were made with the t test (Zar, 1984). Statistical analyses were performed using STATISTICA program version 5.0. Results Renal morphology Kidneys of the Argentine desert rodents studied show a single renal papilla and a medulla divided in two zones (Fig. 1). The delicate mouse, Salinomys delicatus, has the most elongated papillae and the highest renal indices (MI/C, RMT and RMA) among the murids in this sample. The same is true for the red vizcacha rat, Tympanoctomys barrerae, among the octodontids (Table 2). On the other hand, shorter papillae are associated with lower renal indices, as in Akodon molinae (murid) and Octomys mimax (octodontid; Fig. 1). Allometry Pearson’s correlation coefficients between mean cortex thickness, renal indices (RMT, MI/C and RMA) and mean body mass of Argentine desert rodents (murids and octodontids) were consistently significant (Table 3). Thus, smaller species have a thinner cortex and greater indices, but not more developed medullary thickness compared to larger rodents (Table 3). No significant correlation was found between renal morphological characteristics of octodontids and body mass. Renal indices of Argentine murids correlates significantly with body mass (MI/C: R"0·86, N"9, p"0·029; RMA: R"0·708, N"9,
KIDNEY STRUCTURE OF ARGENTINE DESERT RODENTS
457
Figure 1. Renal morphology of four selected murid (Salinomys delicatus, Akodon molinae) and octodontid rodent species (Tympanoctomys barrerae, Octomys mimax). C"cortex; M"outer medulla; Mi"inner medulla.
p"0·033; RMT: R"0·656, N"9, p"0·055). The RMT vs. M regression line for Argentine murid (log RMT"1·289!0·167 log M; R"0·656, N"9, p"0·055) is used to compare with North American heteromyids (log RMT"1·195!0·1695 log M; R"0·976, N"6, p"0·0015) (Lawler & Geluso, 1986). Slopes did not differ significantly (b "!0·17, p'0·05) but intercepts did (t"1·99, df."76, p(0·05). A This indicates that the lines of Argentine murids and heteromyids are parallel but not coincident. Therefore, Argentine desert murids show higher RMT than do desert heteromyids. Urine concentration Maximum values of urine osmolarity are shown in Table 4. Discussion The high renal indices and maximum urine osmolarity of Calomys musculinus and Eligmodontia typus (Tables 2 and 4) correspond with the physiological ability of Calomys musculinus to survive on a diet of seeds and the ability of Eligmodontia typus to tolerate highly concentrated (2)00 M) solutions of salt (Mares, 1977a,b). The high renal indices of Salinomys delicatus, Andalgalomys roigi and Andalgalomys olrogi show that the kidneys of these desert murids are also highly specialized for desert existence. Moreover, their renal indices and maximum urine osmolarity are among the highest values reported for other desert rodents (Table 4; Fig. 2). Among octodontids, the red vizcacha rat, Tympanoctomys barrerae possesses a kidney with a long broad renal papilla and produces highly concentrated urine. These renal attributes are similar to those of the fat sand rat Psammomys obesus (Table 4; Fig. 2) that excretes a large amount of fluid with a high concentration of salt (Schmidt-Nielsen, 1961). Both species have a specialized diet of halophytic chenopods and live in salt dunes habitats (Ojeda et al., 1996; Mares et al., 1997). Close relatives of Tympanoctomys barrerae, such as Octomys mimax and Octodontomys gliroides, have less-developed renal
16 (12) 11 (6) 14 (11) 1
1 11(6) 14(10) 12 (10) 1 1 14 (7) 3 28 (25)
N
86·79$1·00 98·32$1·57 121·18$2·26 153·00
12·50 12·73$0·27 14·50$0·13 18·58$0·25 23·00 28·00 31·11$0·35 44·00$4·67 54·50$0·37
M (g)
1·72$0·01 1·74$0·02 1·97$0·04 1·83
0·83 0·82$0·02 0·99$0·01 0·80$0·01 1·17 1·33 1·17$0·03 1·63$0·02 1·44$0·01
CT (mm)
12·38$0·07 6·38$0·08 9·61$0·07 6·83
7·83 6·94$0·04 6·72$0·12 6·97$0·05 8·66 8·66 7·01$0·05 8·44$0·36 8·72$0·03
MT (mm)
9·41$0·07 6·09$0·06 8·98$0·08 5·35
13·98 12·29$0·10 10·66$0·21 11·42$0·11 13·48 12·60 10·09$0·08 10·10$0·47 9·64$0·04
RMT
5·00$0·06 2·58$0·03 3·91$0·07 3·19
7·02 6·58$0·38 5·32$0·12 6·36$0·08 5·84 4·01 4·27$0·22 3·68$0·19 4·24$0·04
MI/C
1·73$0·03 0·83$0·01 0·75$0·02 1·03
1·69 1·47$0·04 1·63$0·06 1·63$0·04 1·18 1·06 1·44$0·04 0·96$0·07 1·27$0·01
RMA
M"body mass; CT"cortex thickness; MT"medullary thickness; RMT"relative medullary thickness; MI/C"ration of inner medulla cortex; RMA"relative medullary area.
Tympanoctomys barrerae Octomys mimax Ctenomys eremophilus Octodontomys gliroides
Octodontidae
Salinomys delicatus Calomys musculinus Eligmodontia moreni Eligmodontia typus Andalgalomys olrogi Andalgalomys roigi Akodon molinae Phyllotis xanthopygus Graomys griseoflavus
Muridae
Species
Table 2. Renal indices (s$SE) for the desert rodents of Argentina. Number of individuals are indicated in parentheses when the numbers for MI/C or RMA were different
458 G. B. DIAZ & R. A. OJEDA
KIDNEY STRUCTURE OF ARGENTINE DESERT RODENTS
459
Table 3. Allometry of renal morphology of the 13 species of desert rodents from Argentina
CT MT RMT MI/C RMA
a
b
R
F
p
!0)44$0)061 0)80$0)098 1)425$0)087 1)093$0)099 0)420$0)119
0)347$0)038 0)063$0)061 !0)269$0)054 !0)273$0)061 !0)207$0)073
0)94 0)30 0)83 0)80 0)65
84)036 1)0884 25)138 20)172 7)946
(0)0001 0)319 0)0004 0)0009 0)0167
CT"cortex thickness; MT"medullary thickness; RMT"relative medullary thickness; MI/C"ratio inner medulla/cortex; RMA"relative medullary area.
papilla (Fig. 2), low renal indices and low urine concentration (Table 4). This may reflect a water-rich diet of cacti, as found in the wood rat Neotoma lepida (Stallone, 1979; Ojeda et al., 1999). The pattern of decreasing renal indexes and an increase in cortex thickness with increasing body mass in Argentine desert rodents agrees with previous studies for different taxa of mammals (Greegor, 1975; Lawler & Geluso, 1986; Brooker & Withers, 1994). However, Argentine desert rodents show higher slopes than mammals of xeric habitats (Beuchat, 1996). They also do not show a relatively more developed medullary thickness compared to larger rodents, as has been reported for mammals (Beuchat, 1990). The smaller range of body mass considered in our study may account for these differences. Compared with heteromyids, Argentine murids exhibit higher RMT and metabolic rate (Bozinovic & Rosenmann, 1988; Bozinovic, 1992). This may explain the different intercept values for murids and heteromyids in the regression line. Granivorous heteromyids have low metabolic rate and low evaporative water loss, thereby facilitating water conservation (Hinds & MacMillen, 1985). Higher metabolic rates in Argentine desert rodents result in greater respiratory exchange and concomitant increases in water loss. More efficient kidneys (i.e. higher RMT) may compensate for high evaporative water loss. Table 4. Maximum urine osmolarity (mosm/l) of desert rodents
Species
Maximum urine osmolarity (mosm/1)
Source
Muridae Calomys musculinus Eligmodontia typus Salinomys delicatus Notomys alexis Psammomys obesus
8773 8612 7440 9370 6340
This study This study This study MacMillen & Lee, 1967 Schmidt-Nielsen, 1964
7080 2071
This study This study
7500 5540
Altschuler et al., 1979 Schmidt-Nielsen, 1964
Octodontidae Tympanoctomys barrerae Octomys mimax Heteromyidae Perognathus penicillatus Dipodomys merriami
460
G. B. DIAZ & R. A. OJEDA
Figure 2. Relationship between mean relative medullary thickness, and mean body mass for Argentine desert rodents (this study, solid line) and similar sized non-Argentine desert rodents. (䊉)"Argentine Muridae: Sd"Salinomys delicatus; Cm"Calomys musculinus; Em"Eligmodontia moreni; Et"Eligmodontia typus; Ao"Andalgalomys olrogi; Ar"Andalgalomys roigi; Am"Akodon molinae; Px"Phyllotis xanthopygus; Gg"Graomys griseoflavus; (䊊)"Octodontidae: Tb"Tympanoctomys barrerae; Om"Octomys mimax; Ce"Ctenomys eremophilus; Og"Octodontomys gliroides; (䊏)"Non-Argentina Muridae: Na"Notomys alexis; Nc"Notomys cervinus (MacMillen & Lee, 1969); Ps"Psammomys obesus (Sperber, 1944); (䉱)"Heteromyidae, Dm"Dipodomys merriami; Mp"Microdipodops pallidus; Pi"Perognathus longimembris (Lawler & Geluso, 1986).
In conclusion, the renal morphology and function of Argentine desert rodents, either murids or octodontids, evidence the capacity for reducing water loss. Moreover, it is suggested that these renal specializations to arid habitats are independent of the time of South American rodent colonization. The authors thank our fellow colleagues of the Biodiversity Research Group, C. Campos and C. Borghi, for their critical comments, suggestions and statistical advice on earlier drafts of the manuscript. We also thank Drs P. Hanford and M. Willig. Ana M. Scollo kindly helped with the extraction of kidneys, and M. Gallardo kindly provided some animals. We thank Dra P. Valles, Dept. Physiopathology, University of Cuyo, for the loan of the vapour pressure osmometer Wescor 5500, and Ing. Cavagnaro, Plant Physiology Dept., University of Cuyo, for the loan of the area meter. We thank D. Duen as and R. Marti (Magraf) for helping with figures. This project was partially funded by the National Council of Scientific and Technical Investigations (CONICET, Argentina) grants PID 3363800 and PIP 4684.
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