University of Kansas Publications MUSEUM OF NATURAL HISTORY The University of Kansas Publications, Museum of Natural History, beginning with volume 1 in 1946, was discontinued with volume 20 in 1971. Shorter research papers formerly pub- lished in the above series are now published as Occasional Papers, Museum of Natural History. The Miscellaneous Publica- tions, Museum of Natural History, began with number 1 in 1946. Longer research papers are published in that series. Monographs of the Museum of Natural History were initiated in 1970. All manuscripts are subject to critical review by intra- and extra- mural specialists; final acceptance is at the discretion of the publications committee. Institutional libraries interested in exchanging publications may obtain the Occasional Papers and Miscellaneous Publica- tions by addressing the Exchange Librarian, University of Kan- sas Library, Lawrence, Kansas, 66045. Individuals may pur- chase separate numbers of all series. Prices may be obtained upon request addressed to Publications Secretary, Museum of Natural History, University of Kansas, Lawrence, Kansas 66045. Editor: Linda Trueb PRINTED BY UNIVERSITY OF KANSAS PRINTING SERVICE LAWRENCE, KANSAS OCCASIONAL PAPERS r» w \j of the MUSEUM OF NATURAL HISTORY The University of Kansas Lawrence, Kansas NUMBER 67, PAGES 1-22 July 11, 1977 REPRODUCTION, GROWTH AND DEVELOPMENT IN TWO SPECIES OF CLOUD FOREST PEROMYSCUS FROM SOUTHERN MEXICO By Eric A. Rickart1 Ontogeny and reproduction together represent a significant portion of a species' adaptive response to its environment, and their study is a powerful tool for interpretation of ecological patterns of mammals. The two parameters yield direct information concerning energy budgets and in addition may provide insight into other aspects of a species' biology that are less easily examined directly. Because of its widespread distribution and ease of rearing and maintenance, the genus Peromyscus has received considerable at- tention from students of growth and development. Layne (1968) assembled existing information on reproduction and ontogeny for several species and attempted to discern trends in these parameters for the genus as a whole. However, his efforts were mainly limited to temperate species due to a lack of information on tropical forms. As a group, tropical Peromyscus exhibit some interesting but poorly understood characteristics of reproduction and ontogeny. Many species have small litter sizes (less than three) compared to most temperate Peromyscus, and breeding season varies from strongly seasonal in some forms to year-round in others. Layne (1968) had limited data on growth and development in Peromyscus megalops and P. thomasi. These are both very large montane forms, 1 Division of Mammalogy, Museum of Natural History and Department of Systematics and Ecology, The University of Kansas, Lawrence, Kansas 66045 (present address: Department of Biology, University of Utah, Salt Lake City, Utah 84112). 2 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY and yet relative neonatal size (neonatal weight as a percentage of adult weight) is well below the average for the genus. Both species also have relatively slow growth rates, although rates of develop- ment are similar to those of temperate species. The combined effect of these two differing rates results in the occurrence of postnatal developmental events (e.g. weaning and sexual maturity) at smaller relative body size. For example, Layne (1968) reports sexual maturity in female thomasi at approximately 50% adult size. Pero- myscus yucatanicus, a lowland tropical species recently studied by Lackey ( 1976 ) , is similar to temperate species of similar size with regard to many parameters of growth and reproduction. What little information exists for other tropical species is generally con- fined to breeding season and litter size information obtained from trap records. The variability of these data indicates that several strategies may be involved, but more information is required before general trends become clear. The species-rich rodent assemblage within the cloud forest zone on the Gulf slope of the Sierra de Juarez in northeastern Oaxaca is striking with regard to its litter size and breeding season diversity (Robertson, 1975). The present paper deals with comparative reproduction and ontogeny in two members of this tropical rodent assemblage; Peromyscus melanocarpus and P. mexicanus totonte- pecus. I also hope to provide data that will help to clarify growth and reproduction trends in the genus Peromyscus as a whole, and to provide insight into the general ecology of cloud forest rodent communities. Acknowledgments. — Among the many individuals who offered encouragement and help throughout this study, a few deserve special recognition. To Paul B. Robertson, I am indebted for initiating my interest in tropical ecology and for his assistance in the field and throughout the entire study. The financial and in- tellectual support of my advisor, Robert S. Hoffmann, has also been considerable. James W. Koeppl offered advice and assistance in data analysis, and allowed me to use several of his own computer programs. Many other individuals provided help during various phases of this study. Discussions with Norman A. Slade, James H. Honacki, Gregory E. Glass, Lawrence R. Heaney, Richard Racine and Debra K. Bennett were especially valuable. In addition, Ms. Bennett and Drs. Hoffmann, Michael S. Gaines, James A. Lackey and James N. Layne critically read the manuscript. I also wish to thank Joseph Mendelson and the Department of Psychology at the University of Kansas for allowing me to use their animal care facilities. Field work for this study was supported, in part, by grants from the Saul Fund of the Museum of Natural History, and the Graduate School of the University of Kansas. TWO SPECIES OF CLOUD FOREST PEROMYSCUS 3 MATERIALS AND METHODS The study region consisted of a roughly north-south altitudinal transect on the Gulf slope of the Sierra de Juarez, from the north slope of Cerro Pelon (2650 m) north into the Gulf lowlands near the Oaxaca- Veracruz border ( average elevation 50 m ) . The highest point of this transect is in the pine-oak upper cloud forest. Descend- ing to the north, oaks and other hardwoods increase in number as conifers gradually diminish in size and numbers and become re- stricted to the edges of road cuts and other recently disturbed areas. Below the cloud forest, vegetation becomes seasonally deciduous in response to the greater seasonality of moisture at lower elevations. The rugged topography of the mountains has kept human disturbances to a minimum; this is especially true of the cloud forest zone where steep slopes together with excessive moisture and low temperatures discourage native crop production. Near the crest of Cerro Pelon, logging has reduced the number of pines in some areas but oaks and other hardwoods have remained unmolested. In general, rainfall is distinctly seasonal in northeastern Oaxaca, the wet season extending from June to October. The cloud forest near the village of Vista Hermosa ( 1500 m ) receives an average of 230 inches (5840 mm) of rainfall annually (Robertson, 1975). In this area, seasonality in rainfall is very much reduced. Rain falls regularly, even during the dry season, and heavy fogs occur almost daily. Very few trees in the cloud forest are seasonally deciduous and productivity probably fluctuates much less here than in the lowlands. Live specimens of both species were trapped from mid-February to early March, 1975. Peromyscus melanocarpus was collected at several localities from 2 to 28 kilometers south of Vista Hermosa (1550 to 2350 m). Specimens of P. mexicanus totontepecus were obtained from a narrow zone of sympatry with melanocarpus ( 1550 m) and at localities north to Vista Hermosa (1500 m). Animals were trapped in surface and sub-surface runways using Sherman live traps baited with rolled oats and peanut butter. Peromyscus melanocarpus was taken in close association with Cryptotis magna, Sorex saussurei, S. verapaecis, Heteromys lepturus, Oryzomys al- faroi, Peromyscus chinanteco, P. ihomasi, Reithrodontomys mexi- canus and Microtus oaxacensis. Peromyscus mexicanus was found with the above complement, except that the last four species were replaced by Oryzomys falvescens and O. palustris. For both melanocarpus and mexicanus, the particular association varies with altitude (Robertson, 1975). In the field, animals were kept singly in portable plastic and hardware cloth cages, with diet consisting of apple, whole kernel corn and Purina Laboratory Chow. Animals were maintained in 4 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY the laboratory from April, 1975 to February, 1976. Pairs were housed in metal cages provided with cotton for nesting material. The laboratory diet consisted of rat chow and apple, supplemented with raw peanuts, sunflower seeds and whole oat seeds. Water was available ad libidum. Laboratory temperature was maintained near 20° C, and lighting was adjusted to a 12L:12D cycle. Twenty-eight litters (51 individuals) of melanocarpus and nine litters ( 19 individuals ) of mexicanus were born in captivity during the course of the study. Data on all or part of the growth and development of 49 and 17 individuals, respectively, were obtained. First day data were not recorded for the first few melanocarpus litters born in the laboratory because of an unfounded concern that early handling might result in parental rejection. In cases where newborn mice died or proceeded to lose weight rapidly in the first few days after birth, only neonatal measurements were recorded. Growth data were not taken for three melanocarpus in- dividuals born in the field, but partial data on development were taken for these animals. Measurements were taken every other day from birth until six weeks of age, and then weekly until growth ceased. Head-body length and tail length were taken to the nearest millimeter (mm). Hind foot and ear length were measured to 0.5 mm, and weight was recorded to 0.1 grams (g) on an Ohaus triple beam balance. Prior to weaning, young were handled with surgical rubber gloves. All post-weaning measurements were taken under light ether anesthesia. Notes on individual development were made daily from birth to sxual maturity. In addition to these laboratory studies, information on reproduc- tion in these species was obtained from field autopsies on snap- trapped specimens and from the literature. RESULTS Reproduction Gestation Period. — The length of time between conception and birth was not measured directly, but minimal intervals between successive litters were recorded. Three categories of data are available: 1) for lactating females whose preceding litter was entirely successful, 2) lactating females in which one or more of the young in the preceding litter died prior to weaning, and 3) non-lactating females whose previous litter died prior to one week of age. For melanocarpus, the eight shortest intervals in category one were: 41, 39, 38 (three instances), 35, and 31 days (mean: 37.1 days). Intervals of 37 and 36 (two instances) were recorded for category two ( mean : 36.3 days ) , and a single record of 30 clays for category three. For mexicanus, intervals of 39 and 31 (one TWO SPECIES OF CLOUD FOREST PEROMYSCUS 5 each) were recorded in category one (mean: 35) and a single 30 day interval for category three. Although the data do not represent direct measurements of gestation, the apparent regularity of these intervals suggests that both species experience post-partum estrus and that normal gesta- tion is approximately 30 days. The mean gestation period for ten temperate species of Pewmyscus ranges from 23 to 26 days ( Layne, 1968), and Lackey (1976) found a mean of 27.8 days for the five shortest intervals between litters for non-lactating yucatanicus. It is possible that the greater length of gestation apparent for melano- carpus and mexicanus indicates slower prenatal growth in these species. Longer gestation for lactating females has been attributed to implantation delay ( as suggested by Lackey ( 1976 ) for yucatanicus, and Svihla (1932) for maniculatus and leucopus). Although the mean intervals for female melanocarpus in categories one and two are not significantly different, the larger value of the former may indicate a similar delay in that species. Breeding Season. — On the basis of field autopsies and age structure data, Robertson (1975) classified melanocarpus as a seasonal, and mexicanus as an aseasonal breeder. He found a breeding peak in melanocarpus extending from March to July, corresponding to the end of the dry season and the beginning of the wet season, but at least some evidence of reproductive activity was found in every month. No definite breeding peaks were found for mexicanus. Birth of litters in the laboratory for the ten month period of study (April, 1975 through January, 1976) were 0,0,1,3,- 3,2,4,4,7,4 for melanocarpus, and 0,0,0,1,1,1,0,1,3,2 for mexicanus. These records are incomplete, but some pattern does exist in the data. Pewmyscus melanocarpus exhibited an apparent breeding peak in December, and although sample sizes are small, mexicanus also experienced greater productivity during this month. The period of peak productivity in the laboratory corresponds to a period of relatively low productivity in the wild ( Robertson, 1975 ) . To what degree this discrepancy is caused by laboratory condi- tions is unknown. The natural breeding peak for melanocarpus and other "seasonal" breeders from the study area is thought to correspond to the period of greatest seed and fruit production (Robertson, 1975). In a number of species, including melanocarpus and mexicanus, some breeding animals are simultaneously in seasonal molt at this time. It has been suggested that molt-breeding overlap in some tropical birds indicates that they are not devoting a maximum effort toward reproduction (Foster, 1974). The simultaneous occurrence of these events in melanocarpus and mexicanus suggests that, at least during the period of peak productivity, food is not a limiting factor. 6 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY Litter Size. — Mean litter sizes in captivity as well as litter size frequencies are given in Table 1 and compared with embryo counts for snap-trapped specimens from the study area. All but two of the females which littered in the laboratory were wild-caught indi- viduals, so that age-specific fecundity could not be examined directly in either species. Among all female melanocarpits that littered more than once, there was, however, an average increase in litter size through time. The low mean litter size in captivity as compared to mean em- bryo counts from field data is probably due to increased production of early litters by young females in the laboratory. The trend of increasing litter size with age seems to support this contention. This explanation has previously been proposed to explain similar discrepancies between field and laboratory data in other species (McCabe and Blanchard, 1950). All available data indicate that three is the maximum litter size for both melanocarpus and mexi- canus ( Robertson, 1975 ) . In comparison with data on other Peromyscus species sum- marized by Layne ( 1968 ) , it is clear that the mean litter size in both melanocarpus and mexicanus is below the average for the genus. Litter size for the genus as a whole does not appear to be correlated with body size, but among temperate species it shows positive correlation with both latitude and altitude (Smith and McGinnis, 1968). Breeding season length was shown to be the critical factor in this relationship by Spencer and Steinhoff ( 1968). This relationship between litter size and latitude or altitude does not hold for tropical Peromyscus however ( Smith and Mc- Ginnis, 1968; Robertson, 1975), the reason being the lack of correla- tion between these factors and breeding season length. Among many tropical rodents breeding occurs year-round, and a variety of factors may be responsible for any seasonal patterns which may exist. Robertson (1975) found a general negative correlation between habitat stability and average litter size in Peromyscus. Stability was considered to be inversely related to climatic and vegetational seasonality. For five temperate and tropical habitat categories, stability ( habitat type ) accounted for 65% of the litter size variation Table 1. — Mean litter sizes and distributions as determined from field embryo counts and laboratory data. Number of Embryos1'2 12 3 Mean Litter Size in Lab.1 12 3 mean P. meianocarpus P. mexicanus 5 12 13 2.3 0 8 12 2.6 9 15 4 1.8 1 6 2 2.1 1 Present study. 2 Robertson ( 1975 ) . TWO SPECIES OF CLOUD FOREST PEROMYSCUS 7 between respective species groups, and the relationship was strongest among tropical groups. Tropical wet montane forest (including cloud forest) was thought to be most stable, and the associated species group (including melanocarpus and mexicanus) showed the lowest mean litter size. The major problem with such a model is the difficulty of accurately assessing relative stability, but the general correlation appears to substantiate the relationship. The trends in litter size in both temperate and tropical Pero- myscus appear to be clue to the same causal mechanism; any given reproductive effort being influenced by the probability of successful future effort ( Williams, 1966; Schaffer, 1974 ) . In temperate regions, at high altitudes and latitudes breeding seasons are usually very short and, for small mammals, the probability of surviving to the next season may be very low. As a consequence, the entire repro- ductive effort must be made during a rather abbreviated period and this results in a small number of relatively large litters. In areas where breeding season is lengthened or longevity increased to include more than one season, the probability of future reproduction increases, and an increased number of smaller litters indicates that reproductive effort is being spread over a longer breeding period. In tropical areas, the inverse correlation between litter size and habitat stability indicates that where resources are constant or fluctuate in a predictable way there is selection for repeated re- production or "breeding longevity." Although the same effect might result from resource limitation or high litter mortality, the common occurrence of molt-breeding overlap (discussed above) indicates that some species exhibit less than maximal reproductive effort at certain times. Sex Ratios. — The ratio of male to female mice born in captivity was 1.93 for melanocarpus (N=41) and 2.25 for mexicanus (N=13). A binomial test for the fit of these values to an expected 1.00 sex ratio yields two-tailed probabilities of 0.06 and 0.52 respectively. Although neither of these are statistically significant at the 0.05 level, the low probability associated with the melanocarpus ratio suggests a possible bias toward males at birth. The basic theory of sex ratio selection developed by Fisher (1930) states that parents should invest roughly equal energy into the production of both sexes. Biased ratios at birth are caused by sex related differential offspring costs, which may result from size dimorphism or differential mortality. Nevertheless, equal invest- ment results in an equilibrium ratio of 1.00 at the termination of parental care. Overproduction of male melanocarpus, if such is the case, may indicate that males suffer higher mortality7 prior to weaning. A similar bias is expressed in the sex ratios of snap-trapped specimens from the study area. A total of 246 melanocarpus con- 8 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY tained in the collections at the University of Kansas show a sex ratio of 1.54 (P less than 0.001). In contrast, 118 mexicanus show a ratio of 1.11 (P=0.646). Under Fisher's principle, the sex ratio among independent animals has no influence on the equilibrium ratio of 1.00 expected at weaning. The male biased ratio in the field is probably due to a greater susceptibility of males to capture ( Myers and Krebs, 1971 ) . Parental Care. — Females of both species showed a very high tolerance toward males throughout the rearing period, and no fight- ing was ever observed between pairs with litters. Male parental care was observed in a number of individuals of both species. This mainly involved assistance in nest building, retrieval and grooming of young, and a major role in nest defense. The significant male involvement in parental care in the laboratory indicates a high reproductive investment on the male's part, and may reflect a tendency toward monogamy in the wild (Trivers, 1972). Growth To test for sexual differences in growth, Wilcoxon's two-sample tests were performed on the five growth measurements for all ages in both species. Significant differences in size (P less than 0.05) were found in only a few cases, and these followed no pattern. As a result, growth data on the sexes were combined for both species. Statistics for the five measurements are given in Tables 2 and 3. Growth in terms of increase in percentage of adult dimensions is Table 2. — Statistics for five parameters of growth in Peromyscus melanocarpus from birth through 111 days. N=sample size, S.E.=standard error. Age Weighl Body L ength Tail Length Hind Foot Ear Length ( days ) (g) ( mm ) Mean S.E. (mm) Mean S.E. (mm) Mean S.E. ( mn Mean >) N Mean S.E. S.E. 0 41 4.5 0.1 44.8 0.2 16.2 0.2 8.6 0.1 6 41 7.9 0.2 56.1 0.5 25.0 0.4 12.0 0.2 5.6 0.1 14 38 14.1 0.4 72.4 0.8 45.0 1.0 18.6 0.3 9.7 0.2 20 35 18.5 0.6 81.9 0.8 59.4 1.2 22.8 0.3 13.0 0.2 28 33 23.2 0.5 93.9 0.6 74.2 1.7 25.6 0.2 16.6 0.2 34 27 29.3 0.6 101.4 0.7 86.1 1.2 27.0 0.2 18.2 0.2 41 25 32.3 0.7 106.8 0.6 95.5 1.1 27.8 0.1 19.0 0.2 48 23 35.5 0.9 108.9 0.7 102.2 1.1 28.1 0.2 19.4 0.2 55 21 38.5 1.1 110.4 0.7 107.5 1.5 28.3 0.2 19.7 0.1 62 21 41.2 1.2 112.7 0.6 111.0 1.5 28.5 0.2 20.1 0.1 69 21 43.8 1.4 115.2 0.6 114.2 1.5 28.8 0.2 20.4 0.1 76 18 46.9 1.6 116.0 0.7 117.9 1.3 28.9 0.2 20.6 0.1 83 18 49.0 1.6 117.3 0.8 119.8 1.4 29.2 0.2 20.7 0.1 90 16 52.3 1.9 118.5 0.9 122.1 1.2 29.2 0.2 20.9 0.1 97 13 54.7 2.5 119.5 1.1 123.5 1.4 29.3 0.2 20.9 0.1 104 13 55.8 2.9 120.9 1.2 124.2 1.3 29.4 0.2 20.9 0.1 111 11 58.8 3.3 121.9 1.3 125.0 1.6 29.7 0.2 21.1 0.1 TWO SPECIES OF CLOUD FOREST PEROMYSCUS 9 summarized in Table 4 for the first ten week period. "Average adult" measurements used for these calculations are from Robertson (1975) and are based on field data from the study region. Values for weight are plotted against age in Figure 1. Curves for four additional species are included to indicate the growth rate extremes ( as presently known ) for the genus. Growth rates are somewhat slower in melanocarpus than in mexicanus. Rate of weight increase ( in terms of gain in percentage Table 3. — Statistics for five parameters of growth in Peromyscus mexicanus from birth through 97 days. Age Weight Body Length Tail Length Hind Foot Ear Length ( days ) (g) ( mm ) (mm) (mm) Mean S.E. (mm Mean i ) N Mean S.E. Mean S.E. Mean S.E. >.E. 0 17 4.4 0.2 43.9 0.7 15.8 0.1 8.3 0.1 6 15 8.4 0.2 57.5 0.4 26.7 0.4 12.4 0.2 5.9 0.1 14 13 14.8 0.3 74.0 0.8 49.2 0.9 20.0 0.4 10.2 0.3 20 10 19.0 0.5 84.8 0.8 65.1 1.7 24.2 0.3 14.4 0.3 28 9 25.8 0.6 96.9 0.5 79.4 2.3 26.5 0.2 17.6 0.3 34 9 32.4 0.6 104.1 0.6 86.8 2.0 27.3 0.1 18.7 0.2 41 9 36.7 1.2 108.6 0.9 93.3 2.0 27.8 0.2 19.2 0.2 48 9 41.1 1.7 110.8 1.0 98.8 2.1 28.3 0.2 19.9 0.1 55 7 45.3 2.2 112.3 1.4 103.8 3.4 28.9 0.2 20.4 0.1 62 5 47.5 3.7 111.4 1.5 105.4 4.4 29.3 0.3 20.5 0.2 69 5 51.7 4.6 112.0 1.6 106.8 4.6 29.4 0.3 20.6 0.2 76 5 54.7 5.0 113.8 2.2 107.4 4.6 29.5 0.2 20.7 0.1 83 5 56.5 4.9 116.0 1.3 108.0 4.7 29.5 0.2 20.8 0.1 90 5 58.2 5.6 116.1 1.1 108.2 4.9 29.5 0.2 20.8 0.1 97 5 60.5 6.1 116.6 1.1 108.6 5.2 29.5 0.2 20.8 0.1 Table 4. — Growth expressed as a percentage of adult dimension for weight, body length and tail length. Melanocarpus Mexicanus Weight Body Tail Weight Body Tail Age (g) ( mm ) ( mm ) (g) (mm) ( mm ) 0 7.6 34.7 11.8 8.2 35.0 11.7 6 .__.. 13.4 43.4 18.3 15.7 45.9 19.7 14 ..... 23.9 56.1 32.9 27.7 59.0 36.4 20 ..... 31.4 63.4 43.4 35.6 67.7 48.1 28 39.3 72.7 54.2 48.3 77.3 58.7 34 ..._ 49.7 78.5 62.9 60.7 83.1 64.2 41 54.7 82.7 69.8 84.4 74.7 68.7 77.0 86.7 88.4 69.0 48 ..... 60.2 73.0 55 ... 65.2 85.5 78.6 84.8 89.6 76.7 62 ..... 69.8 87.3 81.1 89.0 88.9 77.9 69 _ 74.2 89.2 83.5 96.8 89.6 78.9 Mean Adult ...... 59.0 129.1 136.8 53.4 125.3 135.3 Measurement1 — (g) (mm) (mm) (g) (mm) ( mm ) 1 from Robertson (1975) 10 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY of adult weight) for rnelanocarpus is slower than that for any previously studied species, with the exception of thomasi and megalops. The weight curve for mexicanus resembles that of truei, and is similar in this respect to yucatanicus (Lackey, 1976). Given the similarity in size between rnelanocarpus and mexicanus (59 and 54.3 g, respectively), it is obvious from the striking differences in their respective growth curves that body size alone is not the only factor influencing rate of growth. Sample sizes in rnelanocarpus were large enough to allow the examination of the effects of litter size on growth rate in this species. Table 5 contains statistics for the five growth measures from birth to 48 days by litter size. Data for litters of two and three were in- cluded in the calculations, along with neonatal data for litters of one. Figure 2 is a graphic portrayal of the values for weight, and includes data for partial growth (through day 20) of three litters of one. The mean growth curve for all individuals is included for comparison. Increased litter size apparently has a negative effect on growth rates in rnelanocarpus, especially during the early phases of growth. There is some indication that post-weaning rates become altered in such a way as to counteract the early effects of litter size, and that average curves for litter size classes may converge during the final stages of growth. This suggests that during the period of maternal care, energy available for growth is strictly limited. This is to be expected, but given the relatively small litter and neonatal sizes 100r x LU 80 60 =>40 < 20 mexicanus ■ ^^ truei leucopus / 7 y \ /<-' megalops s s^s ^s*^ ^\ /^>^ ^^ ■^^ rnelanocarpus " ^^-^-' thomasi 12 3 4 5 AGE 6 7 8 9 10 (WEEKS) Figure 1. — Increase in weight expressed as a percentage of adult weight in six species of Peromyscus. Data for leucopus from Lackey (1976). Data for megalops, thomasi and truei from Layne (1968). Data for rnelanocarpus and mexicanus from present study. TWO SPECIES OF CLOUD FOREST PEROMYSCUS 11 40 30 c/) < cc 20 O \- X ID 10- 0 3 4 AGE (WEEKS) — i — 5 Figure 2. — Weight increase according to litter size for Peromyscus melano- carpus. Numbers indicate litter size categories. Dashed line shows mean weight increase for entire laboratory population. involved, the maternal energy commitment to growth of the young in melanocarpus may be lower than that made by other species with larger average litter sizes. After the period of dependency, the growth deficit in animals from larger litters is apparently offset by an increase in post-weaning commitment to growth. As discussed above, litter size in the laboratory for both species is somewhat smaller than that estimated from field embrvo counts ( Table 1 ) . Given the negative effect of litter size on growth rates, if true average litter size is greater, average growth rates for both species under natural conditions might be slower than those esti- mated in the laboratory. In a number of melanocarpus individuals, weight fluctuated ir- regularly at a time corresponding to the initiation of post-juvenile molt. Since molt began over a wide range of ages and weights, in- dividual fluctuations due to this event would be masked in an average growth curve. To isolate this problem, I standardized the weight data for melanocarpus in the following way. For each in- dividual, the age at which molt was first apparent was chosen as time zero. To indicate change in weight, values at three week intervals to either side of the zero point were scored plus or minus by subtraction of the weight at time zero. 12 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY Table 5. — Growth in relation to litter size in Peromyscus melanocarpus from birth through 48 days. Litter Weight Body Length Tail Length Hind Foot Ear Length Age Size : N Mean S.E. Mean S.E. Mean S.E. Mean S.E. Mean ! S.E. 0 1 8 5.0 0.2 46.1 0.7 16.5 0.7 8.9 0.1 2 21 4.5 0.1 45.3 0.2 16.5 0.3 8.6 0.1 3 12 4.1 0.1 43.2 0.2 15.6 0.3 8.4 0.1 6 2 27 8.2 0.2 56.8 0.6 25.6 0.4 12.4 0.2 5.8 0.1 3 11 6.7 0.3 53.7 0.7 22.6 0.7 11.1 0.3 4.9 0.2 14 2 24 14.5 0.4 73.7 0.8 47.4 0.6 19.3 0.2 10.0 0.1 3 11 12.0 0.5 68.0 1.1 38.6 1.9 16.7 0.6 8.6 0.2 20 2 21 18.6 0.5 83.0 0.8 62.7 1.2 23.5 0.2 13.4 0.2 3 11 16.0 0.5 77.4 0.7 52.0 1.6 21.2 0.6 12.0 0.3 28 2 21 24.4 0.5 95.1 0.7 78.5 1.7 26.1 0.2 16.8 0.2 3 11 20.6 0.6 91.5 1.0 65.7 2.3 24.7 0.4 16.1 0.3 34 2 21 29.5 0.7 101.4 0.8 87.2 1.4 26.9 0.2 18.1 0.2 3 5 27.7 0.9 101.8 1.7 81.4 1.2 27.4 0.3 18.6 0.2 41 2 19 32.6 0.8 106.7 0.8 96.6 1.2 27.7 0.2 18.9 0.2 3 5 30.6 1.0 107.4 1.2 90.4 1.1 28.2 0.3 19.3 0.2 48 2 17 36.0 1.0 108.5 0.8 103.8 1.2 28.0 0.2 19.2 0.2 3 5 32.9 1.4 110.2 1.6 97.4 1.9 28.4 0.2 19.9 0.2 Figure 3 shows the results of this operation, with the averaged curve for all animals (N=18) and also the curves for the two ex- treme individuals to indicate range. The decrease in growth rate associated with the initiation of molt is clearly seen. Unfortunately, sample sizes were insufficient for a similar treatment of the mexicanus data. The possibility that the observed effect of molt on growth is an artifact of laboratory conditions seems unlikely; if anything, it has probably been minimized in the laboratory, since the animals were fed ad libidum. It is possible that similar effects on growth rates result from other energetically costly developmental events. Table 6 contains geometric growth rates calculated according to Simpson et al. (1966). A reduction and subsequent reacceleration in growth is evident for melanocarpus over the interval from 20 to 34 days. This corresponds to the estimated age of weaning in this species, and it may reflect the adjustment to solid foods. The same effect has been shown for other members of the genus ( Layne, 1968 ) . Development Postnatal Morphological Development. — Statistics for five major postnatal developmental events are shown in Tables 7 and 8. Combined data for both sexes are grouped by litter size and also totaled for all animals. Wilcoxon's two-sample tests between litter size categories showed significance (P less than 0.05) in some of the parameters for the melanocarpus data, indicating that litter size has a negative influence on the rate of early development. No TWO SPECIES OF CLOUD FOREST PEROMYSCUS 13 10 - / s / s / s / s CO / / / s ^ 5 , < / / DC y / . , o Cj y > — ' LU ID 0 - n— - —~^y y£ r~" T < ^y / / X o r— r / / I I / / _^ — / / r- I — I — y / X -5 s c\ .05 All 44 4.68 0.19 2- 6 Lower 1 4 10.50 0.50 10-12 >.05 Incisor 2 24 10.88 0.29 8-14 <.05 Eruption 3 11 13.45 0.77 10-16 <.05 All 39 11.56 0.34 8-16 Upper 1 4 14.00 0.00 14 >.05 Incisor 2 23 14.43 0.25 12-14 >.05 Eruption 3 11 15.82 0.83 12-20 >.05 All 38 14.79 0.30 12-20 Opening of 1 4 17.50 0.50 16-18 >.05 Auditory 2 22 16.73 0.25 16-20 <.05 Meatus 3 11 19.27 0.41 18-22 <.01 All 37 17.57 0.27 16-22 Opening 1 4 21.00 1.00 18-22 >.05 of 2 20 21.45 0.46 18-24 >.05 Eyes 3 11 23.09 0.78 20-26 >.05 All 35 21.91 0.39 18-26 to develop in the head and neck regions, and progresses in a regular anterior-posterior manner producing what resembles a molt line. No hair is lost as in a true molt however, and the entire process is completed by the fifth week. Although mexicanus also develops longer hairs at this age, nothing resembling a molt line was observed in this species. The pattern of post-juvenile molt is the same in both species. It is initiated in the mid- ventral region, and progresses over the entire venter, then upward along the sides to the dorsum. The posterior rump and the shoulder region are the last areas to undergo molt. In melanocarpus, the average age at which molt was initiated was 72.3 days (N=18, range: 56-98), and the average age of com- pletion was 120.3 days (N=ll; range: 112-140). For five mexicanus, these values were 58.8 davs (range: 49-77) and 119.0 days (range: 91-154). The subadult pelage in both species is quite similar in appear- ance to that of old adults, and in some instances is indistinguishable. In addition, molt lines were rarely seen in conjunction with later TWO SPECIES OF CLOUD FOREST PEROMYSCUS 15 Table 8. — Age (days) at which various postnatal developmental events were completed for Peromyscus mexicanus. Grouped by litter size. Abbreviations as in Table 7. Event Litter Size N X S.E. Range P Elevation of Pinnae 2 3 All1 12 3 16 4.67 4.67 4.62 0.28 0.67 0.24 4- 6 4- 6 4- 6 >.05 Lower Incisor Eruption 2 3 All 10 3 13 10.60 10.00 10.46 0.52 0.00 0.40 8-12 10 8-12 >.05 Upper Incisor Eruption 2 3 All 10 3 13 12.20 11.33 12.00 0.81 0.67 0.64 8-14 10-12 8-14 >.05 Opening of Auditory Meatus 2 3 All 9 3 12 15.78 14.67 15.50 0.62 0.67 0.50 14-18 14-16 14-18 >.05 Opening of Eyes 2 O O All 6 o 9 19.00 20.00 19.33 0.68 0.00 0.47 18-22 20 18-22 >.05 1 including a single litter of one molts. These two factors confounded attempts to estimate the timing and patterns of adult molt. Peromyscus melanocarpus is apparently somewhat slower than mexicanus in general development. In comparison with data for other species summarized by Layne (1968), it is clear that melano- carpus and mexicanus are among the slowest with regard to de- velopmental rates. Both species resemble the large tropical forms megalops and thomasi in the timing of some events (e.g. erection of the pinnae and eye opening ) . As with growth, rates of development in Peromyscus show only a weak negative correlation with body size. Species of similar size may differ widely in the timing of specific events. A wide variety of intrinsic and environmental factors probably simultaneously regulate the specific developmental timetables, so that relatively detailed information on life histories is required for discernment of possible generic trends. As shown for growth rate, litter size has a strong negative effect on early postnatal development in melanocarpus. This suggests that the energy expenditure for each litter is relatively constant, and that increase in litter size results in a finer partitioning of this energy among litter mates. Although this relationship is to be ex- pected, the very strong effect of litter size on development in this species, where litter size is small in the first place, may indicate a rather low energy commitment on the part of the mother. 16 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY Behavioral Development. — Although detailed data on behavioral development were not taken for either species, some general obser- vations may be useful for specific comparisons. Peromyscus melano- carpus — Day 6: Animals capable of righting themselves and able to crawl slowly. Slight response to stimulation of mystacial vibrissae. Day 7-8: Strong tactile response from vibrissae and general body surface. Day 10: First grooming movements, able to crawl quickly. Day 12: Able to stand. Day 14: Running and climbing. Day 16-18: Very active and nervous with signs of auditory response. First seen chewing solid food. Day 20: Increasing oral investigation of ob- jects. Peromyscus mexicanus — Day 6-7: Righting and crawling. Day 8: Strong tactile responses. Day 10: Able to stand. Day 12- 13: Running and climbing. Day 14: Increasingly active, with attempts to bite when handled. At birth, young of both species were unable to cling to the mother's teats. By the second day however, nipple clinging ten- dencies increased and the young would remain firmly attached until about the second week. During this time, young were removed only with great difficulty and would often remain attached as the mother moved about. After the second week, nipple clinging tendencies gradually decreased. In both species, intense vocaliza- tion of isolated young was noted from birth through the first week. Older dependents were generally silent unless roughly handled. Young of both species showed increasing activity and nervousness after eye opening, and this became especially intense among the mexicanus. As adult size was reached, animals became more docile and, as subadults, both species were easily handled although melanocarpus continued to be more tractable than was mexicanus. The general sequence and timing of behavioral development in these species are similar to those reported for other large forms ( Layne, 1968 ) . However, a comparison of these data does indicate that, as in the case of morphological development, mexicanus is the more precocial of the two. Age at Weaning. — Weaning, defined as the age at which the young animals showed no weight loss after 24 hours of isolation (King et al., 1963), was estimated to occur prior to the fourth week in both species, or roughly four to five days after the eyes opened. These estimations of weaning age are similar to those reported for other species (Layne, 1968). Animals allowed to remain with the mother would intermittently nurse through the fifth week, but such individuals did not appear to grow at a faster rate than others isolated after weaning. The earliest age at which solid food was seen to be taken was 18 days. Sexual Development. — Sexual development was followed in- directly by noting changes in the external genitalia. Females were considered sexually mature when the vulva became perforate, and TWO SPECIES OF CLOUD FOREST PEROMYSCUS 17 males when observable scrotal swelling occurred. In mexicanus, four males first showed signs of scrotal swelling at 49, 63 and 77 (two instances) days (mean=66.5). The vulva of a single female became perforate at 46 days. In nwlanocarpus females, the mean age at which the vulva opened was 79.3 days (N=6, range: 70-98), and the average age of noticeable scrotal swelling in males was 124.4 days (N=9, range: 86-154). A Wilcoxon's two-sample test on the melanocarpus data indicates that the observed discrepancy between the sexes is significant ( P less than 0.01 ) . Certain environmental and social factors may affect the age of puberty in both wild and laboratory populations of Peromyscus. Slight differences in maturation time between the sexes in some temperate species possibly serve to reduce breeding among litter mates (Layne, 1968). Although it is possible that the observed discrepancy in melanocarpus is an artifact of laboratory conditions, the difference involved (more than a month) suggests that delayed male maturation may serve an important function. In birds, delaved male maturation has been attributed to low probability of reproductive success among young males ( Selander, 1965; 1972). In general, where reproductive success is strongly correlated with age and experience, postponement of sexual maturity in that sex would result in reduced mortality during the period of extended adolescence (Trivers, 1972). Such a situation may exist for melanocarpus either due to strong competition among males for mates, or female selection of experienced males. Generic Trends in Ontogeny and Reproduction Litter Weight and Body Weight in Peromyscus. — Attempts to correlate growth and reproductive data in Peromyscus with species' body size have been only marginally successful. Layne (1968) examined relationships between several factors among a variety of species. No obvious relationship was found between adult weight and litter size, although litter size and neonatal weight were shown to be negatively correlated among the taxa he examined (i-— 0.70). The inclusion of additional data from this study and elsewhere strengthens this correlation (r=-0.80). The relationship between neonatal weight and adult weight was also examined by Layne, and he noted a segregation of the data into two groups, each showing high positive correlation. One inexplicable problem was, however, the aberrant position of the points for megalops and thomasi (Layne, 1968; fig. 1), and with data from additional intermediate sized forms, the situation does not improve. In an attempt to clarify these relationships, I examined litter weight, expressed as a percentage of adult weight, for all the taxa on which data were available. When these values were plotted against adult weight (Figure 4), a strong negative correlation was evident 18 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY (r=-0.83; P less than 0.01). This same relationship has been shown for clutch weight and adult weight in birds of the families Anatidae and Phasianidae ( Rahn et at, 1975) . The above trends indicate that reproductive effort (in terms of relative expenditure by the female as indicated by the weight re- lationships) decreases with increasing body size. A similar trend, involving body size and monthly productivity in Peromyscus, has been reported by Smith and McGinnis (1968) who attributed low reproductive rates in large species to increased longevity. On the average, tropical species of Peromyscus are larger than their tem- perate relatives, and the largest species are generally found in humid tropical forests (e.g. members of the subgenera Mega- dontomys and Isthmomys, and the largest members of the mexicanus species group ) . This indicates that an inverse relationship between 50r 40 I : i H £§ 30 LU 5i- _i QC Z> ?n LU Q L" < H ;„ 10 O o • -a. o V • B T--0.83 ■ A --. 10 20 30 40 50 60 ADULT WEIGHT (GRAMS) 70 80 Key: h-- banderanus* ■- crinitus pergracilis ♦"- c. californicus □= e. eremicus a-- floridanus <$- g. gossypinus a = jepturus** o = leucopus sspp. •-- maniculatus sspp. 9= megalops auritus a = melanocarpus** 9- mexicanus totontepecus"Q- polionotus sspp. <►= X. thomasi a= truei gilbert] y - vucatanicus*** Figure 4.— Relationship between litter weight (expressed as a percentage of adult weight) and adult weight in Peromyscus. Line fitted by least squares method. Data are from Layne (1968) unless otherwise noted. ( "Enders, pers. comm., ""present study, ""Lackey, 1976.) TWO SPECIES OF CLOUD FOREST PEROMYSCUS L9 habitat seasonality and body size may exist. Lower reproductive effort and increased breeding longevity in species from tropical areas of low seasonality and high predictability would be expected under the assumption that the probability of successful future effort is high in these regions. Since energy commitment to reproduction is lower, greater emphasis may be placed on individual maintenance and growth. This results in molt-breeding overlap, and may also account for the associated trend in body size. Effects- of Body Size on Rates of Growth and Development. — Although there is a generally inverse relationship between onto- genetic rates and species' body size, differences in growth rates are not proportional to size differences ( Layne, 1968). In addition, species of similar size (e.g. melanocarpus and mexicanus) may differ significantly in their respective growth schedules. This sug- gests that although body size has some influence, specific aspects of ecology are of primary importance in shaping these rates. It is pos- sible that habitat stability may have a negative effect on growth rates similar to that postulated for litter size and weight, but addi- tional details of species' life histories are required before patterns become clear. Ecology of Cloud Forest Peromyscus Relatively low reproductive effort (as indicated by the small size and low relative weight of litters) together with evidence of post-partum estrus and tendencies toward aseasonal breeding, sug- gest that there is strong selection for repeated reproduction ( breed- ing longevity) in both species. In addition, judging from the slow rates of growth and development, it is probable that both species are relatively long-lived in the wild. Although there are no direct data on population densities, trap success for these species is high, often reaching 40% in some areas (Robertson, 1975). Trap success is lower during the dry season, which may indicate either that there is seasonal fluctuation in density or seasonal variation in bait acceptance (Fitch, 1954). Density fluctuations may be due to seasonality in breeding and/ or food abundance, both of which apparently peak during the end of the dry season and the beginning of the wet season (Robertson, 1975). Laboratory tests show that both species are moderate food hoarders in captivity, indicating that they experience periods of food shortage in the wild (Rickart and Robertson, 1976). Delayed male maturation in melanocarpus may indicate that reproductive success in that sex is correlated with age and ex- perience. General behavioral observations on both species in this study show significant male involvement in parental care, suggest- ing monogamy. Under this mating system, female choice of ex- perienced (older) males may be a factor reducing the probability of breeding success among young males. 20 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY Robertson (1975) has shown that the demographic strategies of rodents from the study region are not in total agreement with the r and K selection model. Both melanocarpus and mexi- canns appear to have rather stable populations maintained at high densities and produce small litters in terms of both size and rela- tive weight. These factors would indicate that both species are K selected. In addition, the tendency toward seasonal breeding and delayed male maturation in melanocarpus could also be indicative of K selection. However, aseasonal breeding in mexicanus and evidence of post-partum estrus and occasional breeding among young (subadult) females of both species (Robertson, 1975) ap- pear to be r responses. Early female maturation has also been re- ported by Layne (1968) for thomasi, another cloud forest species that occurs in the study region. Under the theory of r and K selection, the various aspects of a demographic strategy are interdependent, so that a species' position on the r-K continuum should be predictable on the basis of selected life history parameters (Pianka, 1972). As shown above, the two species in this study show a peculiar mixture of r and K responses, suggesting that this assumption is not always correct. The model may fail to take into account such factors as selection for breeding longevity in stable environments. Similar violations, involving a variety of species, are discussed by Wilbur et al. ( 1974). They suggest that a number of factors, including trophic relation- ships and environmental predictability, are important determinants of life history strategies which are not accounted for under the general theory of r and K selection. Summary Reproduction and ontogeny in Peromyscus melanocarpus and P. mexicanus totontepecus were examined in the laboratory. Both species occur in the humid cloud forest on the Gulf slope of the Sierra de Juarez in northeastern Oaxaca, Mexico. This area is rela- tively rich in rodent species, and the rodent assemblage is diverse with regard to litter size and breeding season. Both species are relatively conservative with regard to reproduc- tive rates. Litter sizes and weights are low and it is thought that the stability and predictability of the cloud forest environment allows for breeding longevity. Rates of growth and development are also depressed in these species, and this too may be related to habitat stability. An examination of data for 16 members of the genus indicates that litter weight, expressed as a percentage of adult weight, shows a strong negative correlation with adult body weight. This suggests a decrease in reproductive effort with increase in body size, which may secondarily be related to habitat stability. Data obtained on the species in this study, together with pub- TWO SPECIES OF CLOUD FOREST PEROMYSCUS 21 Jished information, suggest some interesting characteristics in demographic strategies. Both species appear to maintain rather stable populations at high densities, produce small litters (in terms of both size and relative weight), and in other respects appear to be K selected. However, trends toward aseasonal breeding, evidence of post-partum estrus, and occasional breeding among subadult females are characteristic of r selection. The theory of r and K selection may fail to take into account certain life history factors such as breeding longevity, and this may be the reason for the apparent mixture of demographic characteristics. RESUMEN La reproduccion y la ontogenia de Peromyscus melanocarpus y P. mexicanus tontontepecus fueron analizadas en el laboratorio. Ambas especies habitan la selva hiimeda de la ladera del Golfo de la Sierra de Juarez en el noreste de Oaxaca, Mexico. Este bioma es relativamente rico en especies de roedores; estas especies tienen diversas adaptaciones con respecto al tamano de la camada y a la estacion de reproduccion. Las mencionadas especies son relativamente conservativas con respecto a sus tasas reproductivas. Los tamahos de las camadas tanto como su peso son bajos, ye se cree que la estabilidad y la predictabilidad del ambiente forestal penniten una estension de la vida reproductiva de los animales. Las tasas de crecimiento y desarrollo tambien estan reducidas en estas especies, y esto igual- mente puede estar relationado con la establidad ambiental. Un analisis de los datos provenientes de 16 especies de este genera mostro que el peso de la camada, al espresarse como porcentage del peso de los adultos, mostro una correlacion fuerte- mente negativa con el peso total de los adultos. Esto sugiere una disminucion del "esfuerzo reproductivo," el cual puede estar secun- dariamente relacionado a la establidad del habitat. Los datos obenidos para ambas especies estudiadas, junto a las informaciones bi bliograficas, sugieren algunas interesantes carac- teriisticas en cuanto a las estrategias demograficas. Ambas especies parecer mantener una estabilidad poblacional a un nivel alto, produciendo camadas pequehas (tanto en tamano como en peso); ye en otras aspectos parecen estar seleccionadas de acuerdo a la forma K. Sin embargo, ciertas tendencias hacia una reproduccion no estacional, evidencia de estro post-partum, y reproduccion en hembras subadultas, son caracteristicas de la seleccion de forma r. La teoria de seleccion r y K podria bien fallar al tomar en cuenta ciertos factores de la historia natural tales como la longevidad reproductiva, y esto podria ser la razon del encuentro de caracteris- ticas demograficas mixtas en estas poblaciones. 22 OCCASIONAL PAPERS MUSEUM OF NATURAL HISTORY Literature Cited Fisher, R. A. 1930. The genetical theory of natural selection. Oxford: Clarendon Press (Dover Publications, New York, 1958). Fitch, H. S. 1954. Seasonal acceptance of bait by small mammals. J. Mamm. 35:39-47. Foster, M. S. 1974. A model to explain molt-breeding overlap and clutch size in some tropical birds. Evolution 28: 182-190. King, J. A., Deshaies, J. C, Webster, R. 1963. Age of weaning in two sub- species of deer mice. Science 139:483-484. Lackey, J. A. 1976. Reproduction, growth and development in the Yucatan deer mouse, Peromyscus yucat aniens. J. Mamm. 57:638-655. Layne, J. N. 1968. Ontogeny. Pp. 148-253, in Biology of Peromyscus (Ro- dentia), (J. A. King, ed. ) Amer. Soc. Mamm. Spec. Pub. no. 2, 593 pp. McCabe, T. T., Blanchard, B. D. 1950. Three species of Peromyscus. Santa Barbara: Rood Associates, Publ., 136 pp. Myers, J. H., Krebs, C. J. 1971. Genetic, behavioral and reproductive attri- butes of dispersing field voles, Microtus pennsylvanicus and Microtus ochrogaster. Ecol. Monogr. 41:55-78. Pianka, E. R. 1972. r and K selection or b and d selection? Amer. Nat. 106: 581-588. Rahn, H., Pacanelli, C. V., Ar, A. 1975. Relation of avian egg weight to body weight. Auk 92:750-765. Rickart, E. A., Robertson, P. B. 1976. Seed hoarding behavior in four species of cloud forest rodents from southern Mexico (MS submitted to J. Mamm.). Robertson, P. B. 1975. Reproduction and community structure of rodents over a transect in southern Mexico. Ph.D. dissertation, Univ. of Kansas, Dept. of Systematics and Ecology. Schaffer, W. M. 1974. Selection for optimal life histories: the effect of age structure. Ecology 55:291-303. Selander, R. K. 1965. On mating systems and sexual selection. Amer. Nat. 99:129-141. Selander, R. K. 1972. Sexual selection and dimorphism in birds. Pp. 180-230, in Sexual selection and the descent of man (B. Campbell, ed. ), Aldine- Atherton. Simpson, G. G., Roe, A., Lewontin, R. C. 1960. Quantitative zoology. New York: Harcourt, Brace and Co., 440 pp. Smith, M. H., McGinnis, J. T. 1968. Relationships of latitude, altitude, and body size to litter size and mean annual production of offspring in Peromyscus. Res. Pop. Ecol. 10:115-126. Spencer, A. W., Steinhoff, H. W. 1968. An explanation of geographic varia- tion in litter size. J. Mamm. 49:281-286. Svihla, A. 1932. A comparative life history study of mice of the genus Peromyscus. Misc. Publ. Mus. Zool. Univ. Michigan 24:1-39. Trivers, R. L. 1972. Parental investment and sexual selection. Pp. 136-179, in Sexual selection and the descent of man (B. Campbell, ed. ), Aldine- Atherton. Wilbur, H. M., Tinkle, D. W., Collins, J. P. 1974. 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