Journal of Mammalogy, 89(4):909–915, 2008
REPRODUCTION AND GROWTH OF A RARE, ISLAND-ENDEMIC CAVY (CAVIA INTERMEDIA) FROM SOUTHERN BRAZIL CARLOS H. SALVADOR*
FERNANDO A. S. FERNANDEZ
Laboratory of Ecology and Conservation of Populations, Department of Ecology, Federal University of Rio de Janeiro, Box 68020, Rio de Janeiro, 21941-590, Brazil
Cavia intermedia is a rare cavy, endemic to the 10-ha Moleques do Sul Island, southern Brazil. We conducted the 1st study of reproductive and growth patterns for this species in its natural environment. Based on 17 months of monthly population monitoring using capture–mark–recapture methods, females were reproductively active throughout the year. Litter size was small (1 or 2 young per litter), with well-developed offspring that weighed approximately 19% of the mass of an adult female. Sexual maturity was reached later than in other species of this genus, at around 59 days of age or 70% of adult body size. There was no evidence that longevity was longer than for congeneric species. Other than longevity, these characteristics are consistent with the island syndrome, which may contribute to the persistence of this species. Key words: body development, endemism, Hystricomorpha, island syndrome, life history, life span, litter size, precocity, sexual maturity, wild guinea pig
Cavia intermedia is a hystricomorph rodent endemic to a 10-ha island in the Moleques do Sul Archipelago, southern Brazil. Other islands with endemic mammals are at least 20 times larger than this (Alcover et al. 1998a, 1998b), thus C. intermedia has one of the smallest geographic distributions among extant mammals, and also has one of the smallest population sizes (Salvador and Fernandez 2008). Previous knowledge of the biology of this species is limited to data collected on 2 short visits to the island by Olimpio (1991), summarized in the article that described the species (Cherem et al. 1999). Karyotypes obtained from individuals captured on those visits allowed Gava et al. (1998) to show that the chromosome number for C. intermedia differed from that of all other species of Cavia. Cavia intermedia has been regarded as phylogenetically closest to C. magna, from which it supposedly derived after the island was isolated by rising sea levels about 8,000 years ago (Cherem et al. 1999; Gava et al. 1998). They share many similar morphologic, morphometric (Cherem et al. 1999), and genetic traits. Hence, one would expect these species to share similar reproductive traits as well. In wild C. magna, only 1 or 2 offspring are born, weighing 18% of the body mass of the
mother, after a 64-day gestation period. Thus, the newborn offspring of C. magna are among the most extreme examples of precocial reproduction in small mammals (Kraus et al. 2005a, 2005b). Insular rodent populations display a suite of characteristics distinct from continental populations, known as the island syndrome, including lower reproduction and greater longevity (Adler and Levins 1994; Gliwicz 1980). Lower reproduction can be expressed through a shorter breeding season, delayed maturation of females, a limited number of females participating in reproduction, or smaller litters (Gliwicz 1980). Although the 8,000 years of isolation of C. intermedia on Moleques do Sul Island may not seem a long span of evolutionary time by mammalian standards, it has presumably been sufficient for speciation, and we also expect C. intermedia to present some of the traits of the island syndrome, which have been found in populations of rodents with shorter isolation times (Adler 1996; Adler and Levins 1994; Crowell 1983; Gliwicz 1980). Longer life span also would be expected for C. intermedia compared to its congeneric species because the tiny island it inhabits lacks any significant predators. We tested the hypothesis that life-history characteristics of C. intermedia have already been strongly influenced by the island syndrome despite the relatively short time of isolation of this species on Moleques do Sul Island. We examined growth rates, sexual dimorphism, litter size, age at maturity, breeding season, and longevity of C. intermedia, and compared these to those of other species of cavy, especially C. magna. Thus, our
* Correspondent: [email protected]
Ó 2008 American Society of Mammalogists www.mammalogy.org 909
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FIG. 1.—The location of Moleques do Sul Archipelago, southern Brazil.
study provided an opportunity to evaluate how strongly and rapidly the effects of the island syndrome can be manifested after a very short isolation time in an unusually small population, even by island standards.
MATERIALS AND METHODS Study site.— The Moleques do Sul Archipelago (278519S, 488269W) comprises 3 islands located 8.25 km southeast of the nearest point at Santa Catarina Island and 14 km from the adjacent continent (Fig. 1). The archipelago was formed about 8,000 years ago, estimated using the maximum depth between the archipelago and the continent (32 m) and records of past sea level changes in the region (Correˆa 1996). The archipelago is part of Serra do Tabuleiro State Park. The largest island in the archipelago is 9.86 ha in total area, 710 m long, and 200 m wide. It is the only site where C. intermedia occurs. In addition to C. intermedia, the vertebrate fauna of the island consists of 31 species of birds plus an undescribed species of a worm lizard (Amphisbaena). The only possible predators of the cavy that have been observed on the island are raptors. The climate in the region is humid mesothermal with warmer months in summer and rains distributed over the entire year, albeit winter months are less rainy. During the study, summer and winter rainfall were around 585 mm and 185 mm, respectively. Additional details about the climate and biota of the island were reported by Salvador and Fernandez (2008). Data sampling.— The population of C. intermedia was monitored during 17 months, from February 2004 to June 2005, through capture–mark–recapture methods. We marked all captured individuals by ear-tagging, determined their sex, then weighed them and classified them according to their reproductive condition (males: scrotal and nonscrotal testes; females: developed and undeveloped nipples, lactating, and
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pregnant) before releasing them at the point of capture. Developed (but not lactating) nipples had a prominent size and pigmentation in the distal part. Undeveloped nipples were smaller and had no pigmentation. Animals were captured in single-door, locally built wire mesh live traps (15 15 50 cm) baited with slices of corn. To reduce stress on captured animals, traps were kept shut during the day, opened by late afternoon, and examined and shut the next morning (Kraus et al. 2003). Total trapping effort was 5,542 trap-nights, supplemented by occasional manual captures. Methods met guidelines approved by the American Society of Mammalogists (Gannon et al. 2007). Data analysis.— Growth was analyzed in the field by monitoring changes in body mass and reproductive condition of individuals captured for the 1st time as immatures, that is, males with nonscrotal testes and females with undeveloped nipples. Individuals were regarded as sexually mature after males 1st presented scrotal testes and females were either nursing or pregnant or had developed nipples. We used museum specimens to compare body mass with age, determined according to the chronological sequence of ossification of cranial sutures adapted by Ximenez (1980) for C. magna and used by Cherem et al. (1999) for C. intermedia. Acording to Ximenez (1980), Cavia has a predictable order of suture ossification: condyle–basiocciptal followed by exocciptial– supraocciptial and basiocciptal–basisphenoids. This sequence allowed us to distinguish 4 classes: age I (young—without ossified sutures), II (with ossified condyle–basiocciptal suture only), III (with ossified condyle–basiocciptal and exocciptial– supraocciptial sutures), and IV (adult—with all 3 ossified sutures). Class II individuals were regarded as subadults, and classes III and IV as adults. We located 20 museum specimens with enough information (age class, mass, and reproductive condition) for this analysis: 18 at the Federal University of Santa Catarina (UFSC) in Floriano´polis, 1 at the National Museum (MNRJ) in Rio de Janeiro, and 1 at the Natural History National Museum in Montevideo (MNHN). Using the relationship between suture ossification and body mass from these specimens, we established an age classification based on body mass for the live animals in our field study. The hypotheses that individuals of both sexes required the same time to reach sexual maturity, and that masses of individuals classified as adults did not differ between sexes, were tested by means of t-tests. In the 2nd analysis, only the body mass at the 1st capture of each individual was used to assure statistical independence of the data. Body masses of reproductive females (lactating or pregnant) were not included in this analysis. Reproductive (pregnant or lactating) females were grouped by season: spring (23 September–10 December), summer (21 December–20 March), autumn (21 March–20 June), and winter (21 June–22 September). We used a chi-square test to test the hypothesis that the proportion of reproductively active females did not differ among seasons (Zar 1999). We excluded data from the 1st (summer 2004) and last (autumn 2005) seasons of our study because these 2 seasons were not completely sampled.
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Litter size of pregnant females was determined by abdominal palpation. Estimates of longevity were based on the number of days between the 1st and the last capture of each individual.
RESULTS During the 17 months of livetrapping, 144 C. intermedia (218 captures of 80 males and 134 captures of 64 females) were monitored. Sixteen individuals of each sex were 1st captured as immatures (Table 1). One female (COR) was born in a trap during the night, because the entire umbilical cord with part of the placenta hung from its abdomen, but it was found dead and was used for analysis of ossification of cranial sutures. This newborn was classified as age I and weighed 150 g (Tables 1 and 2). Females 806 and 824 and male 811 were captured with a partial or prominent scar of the umbilical cord, and were lighter than female COR, suggesting they were also recently born, perhaps even in the trap; all were released alive but were never recaptured (Table 1). Ten individuals were captured at least twice as immatures. Average time (6 SD) in this age class was 59 6 45 days, with no difference between the sexes for this interval (t ¼ 1.63, d.f. ¼ 8, P ¼ 0.17) or body mass (t ¼ 1.43, d.f. ¼ 8, P ¼ 0.19). Average mass (6 SD) of these 10 individuals at their last capture as immature was 383 6 111 g (Table 1). Female 976 was the only immature captured with a body mass . 500 g. Among the museum specimens, the greatest mass recorded for individuals with incomplete ossification of cranial fissures (age I) was 200 g and the lowest mass for those considered adult (ages III and IV) was 495 g (Table 2). Animals . 500 g (excluding female 976) in our field study were thus considered adults for comparison of differences in body mass between the sexes. We compared masses for 59 males with developed testes and 36 females with developed nipples. Average masses (6 SD) were 649 6 72 g for males and 671 6 69 g for females; differences between the sexes were not significant (t ¼ 1.17, d.f. ¼ 57.4, P ¼ 0.25). A total of 23 pregnant or lactating females was captured. The proportion of reproductively active females did not differ among seasons (v2 ¼ 7.45, d.f. ¼ 3, P . 0.05; Table 3). Of 9 pregnant females, 7 (78%) had 1 offspring each and 2 (22%) had 2 offspring. Females 814, 775, 913, and 497 were captured pregnant or lactating more than once. The time intervals between those captures were 21, 60, 146, and 364 days, respectively (Table 3). Maximum longevities recorded were 484 and 415 days for 2 males, followed by 405 days for a female. These were the only individuals that surpassed 400 days between the 1st and the last capture.
DISCUSSION Offspring of C. intermedia are born well developed, with body masses . 100 g, as expected for species of this genus (Kleiman et al. 1979; Kraus et al. 2005a, 2005b; Ku¨nkele and Trillmich 1997; Laurien-Kehnen and Trillmich 2003; Raffel et al. 1996; Rood 1972; Trillmich et al. 2006; Weir 1974). Although the exact time of birth is unknown, the 3 individuals
captured with recent marks of the umbilical cord must have been just a few days old, because their body masses (100, 125, and 150 g) were just slightly higher than mass of an offspring born in captivity (99 g) reported by Cherem et al. (1999). Newborns of C. intermedia weighed about 19% of the average mass of adult females (including the value from Cherem et al.  quoted above). This value is higher than recorded for C. aperea (10%) and C. porcellus (11%) and similar to that of C. magna (18%—Kraus et al. 2005b; Weir 1974). Offspring of C. intermedia can reach up to 24% of the mass of their mothers, because this is the ratio of the mass of female COR and its presumed mother (female 963, Table 3). Thus, the newborn : mother body mass ratio for C. intermedia can be even more extreme than that for C. magna, which has been regarded as one of the most extreme ratios among small mammals (Kraus et al. 2005b). Age at maturity varies widely in cavies, making comparisons among species difficult, especially considering variation in how measurements are recorded and conditions (field or laboratory) of the populations studied (e.g., Rood and Weir 1970; Trillmich et al. 2006). For C. intermedia, the average of 59 days trapped as an immature can be regarded as a minimum time span for maturation. Neither the true age of these individuals nor how long they remained immatures were known, thus C. intermedia could take longer than 59 days to reach maturity if other indicators such as the age at 1st estrus (for females) and the occurrence mobile sperm (for males) could be used, as done by Trillmich et al. (2006). Nevertheless, Trillmich et al. (2006) showed that C. aperea reached maturity more rapidly than did C. intermedia, especially in their experiments closer to natural conditions. According to Trillmich et al. (2006), male C. aperea just a few days old can show reproductive conditions (developed testis) that only appeared in adult C. intermedia in our study. In wild C. magna in Uruguay (Kraus et al. 2005b), time to maturation was one-half that recorded for C. intermedia in our study. Therefore, even if time to maturation was underestimated by the methods we used, C. intermedia still took much longer than its congenerics to reach maturity. Growth rates of C. intermedia provided additional evidence of slow maturation. Individuals in our study attained morphologic traits of adults at around 400–500 g, or approximately 70% of the average body mass of adults. This was higher than the level of 50% of average mass of adults recorded for wild C. magna by Kraus et al. (2005b). Individuals in age class I weighed about 200 g, yet still showed no evidence of fused cranial fissures, and did not show reproductive traits that indicated sexual maturity. Individuals . 495 g could be considered adults in terms of their reproductive condition and ossification of cranial fissures, with the exceptions of 1 immature individual that weighed 600 g and 3 mature individuals , 400 g. The lack of sexual dimorphism in adult body mass in C. intermedia in our study differs from findings reported for other species of Cavia, where males are heavier (C. magna—Kraus et al. 2005b; Trillmich et al. 2004; Ximenez 1980; C. aperea—Asher et al. 2004; Bonaventura et al. 2003; Sachser et al. 1999; Trillmich et al. 2004).
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TABLE 1.—Changes in body mass of cavies (Cavia intermedia) 1st captured as immature (females: nipples not developed; males: nonscrotal) on Moleques do Sul Island, southern Brazil, from February 2004 to June 2005. ID ¼ individual identification number. Abbreviations for reproductive condition: nn ¼ undeveloped nipples, dn ¼ developed nipples, prg ¼ pregnant, lac ¼ lactating, nt ¼ nonscrotal testes, st ¼ scrotal testes. See text for additional details. Sex
Date of capture
3 March 2004 8 April 2004 1 July 2004 9 January 2005 4 April 2004 30 April 2004 5 June 2004 6 June 2004 4 November 2004 7 May 2005 6 June 2004 29 June 2004 4 November 2004 10 December 2004 8 January 2005 31 January 2005 6 March 2005 28 March 2005 4 May 2005 1 June 2005 8 August 2004 3 September 2004 2 October 2004 3 November 2004 30 January 2005 7 September 2004 9 January 2005 30 January 2005 9 March 2005 28 March 2005 4 May 2005 2 February 2005 4 May 2005 7 March 2005 7 March 2005 9 March 2005 10 March 2005 1 June 2005 29 March 2005 8 May 2005 1 October 2004 4 May 2005 5 April 2004 3 September 2004 29 September 2004 7 December 2004 30 June 2004 1 October 2004 1 November 2004 6 December 2004 6 December 2004 7 January 2005 5 May 2005 6 January 2005 6 January 2005 6 January 2005 31 January 2005 10 March 2005 6 May 2005
nn nn nn dn nn nn nn nn dn dn nn nn dn dn dn dn lac dn prg dn nn nn nn nn nn nn dn lac dn dn dn nn prg nn nn nn nn nn nn nn nn dn nt st st st nt nt nt nt nt nt st nt nt nt nt st st
175 425 450 600 250 300 350 400 575 475 450 450 625 675 600 675 675 600 725 575 150 450 550 525 600 425 500 550 450 450 450 450 525 475 400 100 275 350 125 250 175 575 300 600 500 600 225 400 125 250 200 275 500 125 475 275 275 425 475
449 457 472
731 300 301 824b 816 806b 804 302 Male
954 303 927 771
765 767 948
No. days since 1st capture 0 37 122a 288 0 26a 0 0 152 337 0 23a 151 188 218 241 275 297 334 363 0 0 30 62 151a 0 126 147 185 204 241 0 123 0 0 0 0 82a 0 0 0 216 0 152 178 247 0 0 0 36a 0 33a 152 0 0 0 25a 63 120
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TABLE 1.—Continued. Sex
Date of capture
No. days since 1st capture
3 November 2004 9 December 2004 8 January 2005 31 January 2005 31 January 2005 7 January 2005 7 March 2005 28 March 2005 4 May 2005 1 June 2005 7 March 2005 7 March 2005 5 May 2005 1 June 2005 7 March 2005 28 March 2005 5 May 2005
nt nt st st nt nt nt st st st nt nt st st nt nt nt
350 450 550 550 275 275 425 450 500 500 450 500 500 500 150 150 325
0 37a 68 91 0 0 60a 81 118 146 0 0 60 95 0 0 0
930 811b 304 a b
Minimum time (days) individual was classified as immature. Individuals captured with a partial or prominent scar of the umbilical cord.
Reproduction by C. intermedia was not seasonal. Yearround reproduction has been reported for other species of Cavia, but spring and summer were considered reproductive peaks for C. aperea (Bonaventura et al. 2003) and C. magna (Kraus et al. 2003), or spring only for C. aperea (Rood 1972). With continuous breeding, C. intermedia can have more than 1 litter per year, as we observed for females 497, 913, and 775. Female 497 was captured lactating twice within a 364-day interval, and female 913 had a 146-day interval between a capture as pregnant and a capture as lactating. Female 775 was captured lactating and pregnant in a 60-day interval. Weaning in C. intermedia should not take more than about 30 days, as observed for domestic guinea pigs and wild C. magna (Kraus et al. 2005a; Raffel et al. 1996). C. intermedia can likely conceive postpartum, with a gestation time of about 60 days, as known for other cavies (Kraus et al. 2005a, 2005b; Rood 1972; Rood and Weir 1970; Trillmich 2000). The litter size of 1 or 2 corroborates Cherem et al. (1999), who reported 2 female C. intermedia pregnant with only 1 offspring each. Within the subfamily Caviinae, C. magna also has only 1 or 2 offspring per litter (Kraus et al. 2005b; Ximenez 1980). In contrast, C. aperea can have from 1 to 6 offspring per litter (Asher 2004; Rood 1972; Rood and Weir 1970; Trillmich 2000), and C. porcellus can have 3–5 offspring per litter (Raffel et al. 1996). The maximum longevity that we observed for C. intermedia was lower than expected for an insular population because recorded life expectancy was as short as for other species of Cavia on the continent. According to Kraus et al. (2005a), life expectancy of C. magna was between 2.4 and 16 months in the wild or 8 years in captivity; the difference between wild and captive individuals was mostly related to predation by mammals in wild populations (Kraus and Ro¨del 2004). On Moleques do Sul Island, mammalian predators are absent and raptors are the only potential predators of C. intermedia; however, raptors are represented by a few species that do not
seem to be effective predators of wild cavies (Kraus and Ro¨del 2004). The length of our study (17 months) surely constrained the maximum longevity that we could record for C. intermedia. Thus, comparisons to laboratory studies or to longer-term field studies should be made with caution. In conclusion, C. intermedia exhibited reproductive traits more similar to those of C. magna than to those of other cavies, TABLE 2.—Sex, body mass, and age estimated according to the chronological order of the ossification of cranial sutures of Cavia intermedia from Moleques do Sul Island, southern Brazil. Age I ¼ young, II ¼ subadults, III and IV ¼ adults. ID no.a
Body mass (g)
UFSC 3363c UFSC 3371 UFSC 583 UFSC 581 UFSC 3374 UFSC 579d UFSC 3378 UFSC 584d UFSC 3376 UFSC 3539 UFSC 3372 UFSC 3377 UFSC 3540 MNRJ 29811d MNHN 3272d UFSC 3489 UFSC 3490 UFSC 580 UFSC 3373 UFSC 585
F F F F F F F F M M M M M M M M M M M M
150 200 495 505 500 610 625 641 550 550 600 600 650 550 550 575 575 600 600 680
I I III III IV IV IV IV III III III III III IV IV IV IV IV IV IV
a Identification number of specimens housed at collections of the Federal University of Santa Catarina (UFSC) in Floriano´polis, National Museum (MNRJ) in Rio de Janeiro, and National History Museum in Montevideo (MNHN). b According to methods in Ximenez (1980) and Cherem et al. (1999). c Female COR (see Table 1). d From Cherem et al. (1999) with corrections for the sexes.
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TABLE 3.—Reproductive condition of female Cavia intermedia from Moleques do Sul Island, southern Brazil, according to season from February 2004 to June 2005. ID
Body mass (g)
497 401 421 458 438 963b 489 988 428 913 932 934 763 952 774 967 PER 759 730 497 728 775 814 913 814 775 731
2 March 2004 5 April 2004 8 April 2004 5 June 2004 1 July 2004 8 August 2004 5 September 2004 6 September 2004 2 October 2004 3 November 2004 7 December 2004 7 December 2004 6 January 2005 7 January 2005 8 January 2005 10 January 2005 30 January 2005 31 January 2005 31 January 2005 1 February 2005 6 March 2005 6 March 2005 10 March 2005 28 March 2005 31 March 2005 4 May 2005 4 May 2005
Summer Autumn Autumn Autumn Winter Winter Winter Winter Spring Spring Spring Spring Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer Autumn Autumn Autumn Autumn
Lactating Lactating Lactating Lactating Lactating Lactating Pregnant Lactating Lactating Pregnant Pregnant Lactating Pregnant Pregnant Lactating Lactating Lactating Lactating Pregnant Lactating Lactating Lactating Pregnant Lactating Lactating Pregnant Pregnant
— — — — — — 2 — — 2 1 — 1 1 — — — — 1 — — — 1 — — 1 1
700 500 700 525 500 625 750 675 650 575 725 575 950 750 650 650 550 650 950 600 550 675 625 625 450 725 525
Spring ¼ 23 September–20 December, Summer ¼ 21 December–20 March, Autumn ¼ 21 February–20 June, Winter ¼21 June–22 September. Captured with female offspring COR (see Table 1).
as reported for morphometric, morphologic (Cherem et al. 1999), and genetic traits. Nevertheless, some traits could be manifestations of the island syndrome, as suggested for homerange and population parameters (Salvador and Fernandez 2008). Delayed sexual maturation and small litter size are considered characteristics of the island syndrome (Adler and Levins 1994). Therefore, both phylogenetic relationships and the island syndrome may contribute to the life-history characteristics of C. intermedia. Reproductive features of C. intermedia may have remained similar to those of C. magna not because of phylogenetic inertia, but because they were features already suitable to the confined island conditions.
RESUMO Cavia intermedia e´ uma espe´cie rara de prea´, endeˆmica de uma ilha de 10 ha. Este foi o primeiro trabalho realizado no seu ambiente natural com objetivo de descrever aspectos reprodutivos e de desenvolvimento corpo´reo, a partir de 17 meses de monitoramento mensal atrave´s de captura–marcac¸a˜o–recaptura. C. intermedia se reproduziu o ano inteiro, pore´m com proles pequenas (um ou dois), filhotes bem desenvolvidos (cerca de 19% do peso das feˆmeas adultas) e maturidade mais tardia do que as outras espe´cies do geˆnero, em torno de 59 dias no mı´nimo, com 70% do tamanho dos adultos. Na˜o foi possı´vel detectar se a longevidade foi mais alta que espe´cies congene´ricas. Com excec¸a˜o da u´ltima, essas caracterı´sticas
sa˜o consistentes com manifestac¸~oes da sı´ndrome insular. Tanto suas afinidades filogene´ticas—que ate´ certo ponto pre´adaptaram C. intermedia a` vida insular—e a sı´ndrome insular ajudam a explicar a persisteˆncia da espe´cie.
ACKNOWLEDGMENTS We thank Brazilian Coordiantion for Higher Level Graduates Improvement, the State of Rio de Janeiro Research Foundation (FAPERJ), and Fundac¸a˜o O Botica´rio de Protec¸a˜o a` Natureza for their financial support, as well as acknowledge support provided by the Department of Behavior Biology (University of Mu¨nster, Germany) to N. Sachser and M. Asher, the Laboratory of Aquatic Mammals (Federal University of Santa Catarina) to P. Sim~ oes-Lopes and M. Graipel, the Tigrinus Co. to M. Tortato, and the Caipora Cooperativa for Nature Conservation to L. Pimenta and M. Gomes. D. Perez donated material used in our study, and J. Cherem kindly assisted with cranial analysis. We thank S. Bonatto and R. Kanitz for access to their unpublished data on genetics of C. intermedia. We thank all the colleagues that helped with field efforts. Finally, we thank E. Heske and 2 referees for their suggestions and criticisms, which were very useful to improve the paper.
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Submitted 15 February 2007. Accepted 8 December 2007. Associate Editor was Gerardo Ceballos.