REPRODUCTIVE BIOLOGY OF
WLOMYS AND OTOTYLOMYS

Dissertation for the Degree ”of Ph. D.
WOMAN STATE UNIVERSITY
jOHN DAMEL HELM III
1973

This is to certify that the

thesis entitled

REPRODUCTIVE BIOLOGY OF
TYLOMYS AND OTOTYIDMYS

presented by

John Daniel Helm III

has been accepted towards fulfillment

of the requirements for

Ph’ D ' degree in

Zoology

 

 

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ABSTRACT
REPRODUCTIVE BIOLOGY OF TYLOMYS.AND OTOTYLOMYS

By
John Daniel Helm III

The major concern of this paper is to describe and compare the
reproductive biology of two Neotropical climbing-rats, Eylomys and
Ototqugys. The lygggyg'were descended from animals caught from Rio
Grande and Valle Nacional, Oaxaca, Mexico and from captives donated by
R. Tesh from El Acquacate, Panama. The Ototylomys were offspring of
animals live-trapped from Campeche, Mexico. All of the animals were
maintained in the Michigan State University Live Animal Colony. Date
collected from both genera included determination of the estrous cycle,
gestation length, occurrence of postpartum estrus, and prenatal and post—
natal development.

vaginal smears were collected from Tylogys exposed to two lighting
conditions. The average interval between cornified cell periods was 6.8 t
0.4 days under natural lighting and 12.0 i 2.5 days when exposed to 12-
hours of light and 12 hours of darkness. Ototylomys kept in 14 hours of
light and 10 hours of darkness had an average estrous cycle of 8.8 i 0.5
days. A postpartum estrus was observed for all littering females of both
genera, as evidenced by the presence of sperm in smears taken within 2n
hours after the discovery of new litters.

The earliest recorded mating for female lyggmy§_was 90 days of age
while the earliest recorded mating for female Ototylomyg was 29 days of
age. The earliest recorded mating for males was 14% days for Tyiomys and

175 days for Ototylomys.

John Daniel Helm III

The gestation period for Tylogys was 40.6 i 0.5 days and 52.8 i 2.1
days for Ototylogys. No statistical difference was found between the mean
gestation lengths of lactating and non-lactating females for either genus.
Both the minimum and maximum extremes in gestation length were Observed in
lactating females of both Tylcgys and thtylgmyg, Embryos were first
detected by palpation of Tylogys on day 7 of gestation and of Ototylggge
on day'l4 of gestation. The fetal head was initially distinguishable at
28 days in both genera.

The ratio of males to females at birth was 95.6:100 and 115:100 for
gylgggg,and Qtotylomys, respectively. Tylgmy§_had an average of 2.3 young
per litter and Ototylomys had an average of 2.4 young. The range in
litter size was 1-4 in both genera. Statistical analysis of the standard
measurements at birth for the Mexican and Panamanian lylggyg_p0pulations
did not reveal any differences at day one; therefore, the data were
pooled. The standard measurements, in millimeters, for Eylggzg'were:
total length, 134.1 1 1.0; tail length, 50.0 1 0.7; hind foot, 18.0 t 0.2;
ear, 8.5 t 0.04. For Ototylogys they were: total length, 119.5 i 0.9;
tail length, 47.1 i 0.8; hind foot, 16.4 i 0.2; ear, 9.4 i 0.2. lo 5
weighed 20.2 i 0.3 grams and Ototylomys 10.2 i 0.3 grams at birth. The
least variance over time was observed in the length of head and body,
without tail, and was therefore most valuable for comparisons of growth
rates over time. At birth, Tylomys measured 84.3 t 0.7 mm and Ototqugys
measured 67.0 1 3.2 mm. Head and body length of Eylomys from Mexico was
34.9 per cent of adult body length; those from.Panama were 35.8 per cent
and Ototyiomys were 46.4 per cent of their adult body lengths. No
statistical differences were found between males and females at birth

for either genus.

John Daniel Helm III

For approximately 30 days after birth, the neonates of both genera.adhere
tenaciously to their mother's inguinal teats. Both gylomys and Ototylgmmg
young are precocial, with Ototylomys young being the more precocial. The
greatest number of Tylomys were initially able to respond to loud noises
between days 8 and 9 while the largest number of Ototylomys initially
responded by day 2. Eye opening occurred for the greatest number between
days 10 and 11 in Eyicmys and day 6 for Ototylcmys. Hearing preceded eye
Opening in all but four cases.

zygomme from Mexico have attained 50 per cent of adult body length
by day 14 and those from Panama between days 12 and 14. Ototylgmyg reach
50 per cent of their adult body length by day 2. Ninety per cent of'adult
body length is reached at 120 days in the Mexican Iylcmys while the
Panamanian group grew to 90 per cent of their adult body length by 116
days. Ototylomys grew to 90 per cent of their adult body length by 58

days of age.

REPRODUCTIVE BIOLOGY OF TYLOMYS AND OTOTYLOMYS

By

John Daniel Helm III

A DISSERTATION

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Zoology

1973

; ACKNOWIEDGMEN’IS

I would like to thank my fellow graduate students for their
continuous interactions during the various phases of my graduate program.
my graduate committee, Drs. Rollin Baker, lynwood Clemens, Edward Convey,
and Richard Dukelow, has been helpful with advice and has made available
resources for the collection of data for this dissertation. Special
thanks go to Dr. Rollin Baker for his guidance, criticisms, and
inspiration throughout my doctoral program.

My wife, Nancy, merits special admiration for her tolerance of my
whims while pursuing my graduate career and for her help in the
preparation of this manuscript.

I am indebted to the Department of Zoology for supplying materials.
Field work for acquiring animals for study was financed by the National
Science Foundation (GB 2227 to R. H. Baker), the Museum's Warren and
Jameson funds, and the Ford Foundation (through the MSU International
Programs). A Biomedical Institutional Grant (NIH) provided the means for

maintaining my live animal colony.

ii

TABLE OF CONTENTS

LIST OF TABLES . . . . . . . . . .
LIST OF FIGURES . . . . . . . . .
INTRODUCTION . . . . . . . . . . .
MATERIALS AND METHODS . . . . . .
RESULTS . . . . . . . . . . . . .
Tyicmye . . . . . . . . . . .
Estrous Cycle . . . . .

Sexual Maturity . . . .

Gestation . . . . . . .

Prenatal Development . . .

Birth . . . . . . . . .
Hearing and Eye Opening
Growth . . . . . . . . .
Pelage . . . . . . . .
Ototylomys . . . . . . . . .
Estrous Cycle . . . . .
Sexual Maturity . . . .
Gestation . . . . . . .
Prenatal Development . .
Birth . . . . . . . . .

Hearing and Eye Opening

iii

Page

«a ~c «a {r F4 5.

10
10
10

13
13
13
l7
l7
17
18
l8
l8
l9

Growth .
Pelage .
DISCUSSION . . . .
SUMMARY . . . . . .

LIST OF REFERENCES

TABLE

OF CONTENTS

iv

(Continued)

Page
20
20
23
32
35

 

 

li‘llnll‘l I! III

LIST OF TABLES

 

 

 

Table Page
1. Vaginal cytology (days: Y'i Sx) of 15 Tylomys and 14
0t 0 tyl OMS O O O O O O O O O O O O O O O O O O O O O O 8
2. Revolutions per day (I i Sx) for 5 Tylomys and 6
OLD tyl OMS e e e a e e o e e e e e a e e o a e e e o e 9
3. Prenatal development of 51 Tylomys and 35 Ototylomys
11

individuals as determined by palpation (mm) . . . . . .

LIST OF FIGURES

 

 

 

Figure Page
1. Distribution of Tylomys and Ototylomys . . . . . . . . . . 3
2. Eye Opening and first response to loud noises . . . . . . . 14
3. Growth of‘zylomys from Mexico and Panama (Y'i Sx) . . . . . 15
4. Body length (head and body minus tail) and weight of

Tylomys (X i Sx) . . . . . . . . . . . . . . . . . . . 16
5. GrowthofOtotylom(Yi-Sx)............... 21
6. Body length (head_and body minus tail) of

Ototylomys (X i 8x) . . . . . . . . . . . . . . . . . 22
7. Gestation lengths of peromyscines and neotomines . . . . . 26
8. Growth of body length (semi-log) of Tylomys and

Ototylomys through 28 days of age .'. . . . . . . . . 28

vi

INTRODUCTION

The purpose of this paper is to describe and compare the reproductive
biology of two NeotrOpical climbing-rats, Tylggy§_and Ototylggyg. 'Within
the framework of these comparisons, considerations will be made of the
possible ecological and evolutionary significance of this biology.

Mbssman (1953) and Keys (1954; 1958) proposed that the physical
mechanisms of implantation and subsequent development of placental
membranes have possibly more evolutionary significance than do the
morphological criteria now being used, since adaptation to external
environment contributes little to the development of placentation. ‘Within
the genus Pero sous, Layne (1966) found that body size and environment
were the most influential factors governing gestation length and postnatal
development. To further illucidate evolutionary and reproductive
relationships found in rodents, two closely related animals feund in
similar environments, Tylomys and Otot lo , were examined and the
results are described herein.

2310523 and Ototylo_mys belong to an assemblage of Neotr0pica1
cricetine rodents of obscure ancestry. The genera, Tyggmy§,and Ototylgggg
were considered to be related to Neotoma by Hooper and Musser (1964) and
have been placed in the same subfamily as Neotoma. A later study by
Lawlor (1969) shows that Tylomys and Ototylomys are probably'more closely
related to each other than to Neotoma or Nelsonia, the other two members

of the subfamily Neotominae. The latest compilations (Cabrera, 1961: 435;

Hall and Kelson, 1959: 573-6) list eight species in the genus Tylcms.
However, some of these species may ultimately be reduced to subspecific
status (£93 Goodwin, 1969; Handley, 1966; and Schaldach, 1966). On the
other hand, Ototyloms is monotypic, with all populations assigned to
Q. mnotis (Lawlor, 1969). Only generic names will be referred to in
this paper.

M and Ototylomys are generally considered to be scansorial, but
their autecologies are poorly known. Figure 1 shows the distribution of
both ylogzs and Ototylogrys. They are found in both moist and arid
forested areas, along rocky ledges, and from sea level to 1820 meters
above sea level (Anthony, 1916; Baker and Petersen, 1965; Burt and
Stirton, 1961; Disney, 1968; Goodwin, 1931, 1942, 1946, 1955, 1969; Hall
and Dalquest, 1963; Hall and Kelson, 1959; Handley, 1966; Lawlor, 1969;
Peters, 1866; Schaldach, 1966; Tesh, 1970; Ramirez-Pulido and Sanchez-
Hernandez, 1971). Animals of both genera are thought to be nocturnal,
although activity-wheel performances show 2210313 to also have diurnal
activity. The animals of both genera used in the present study are from
seasonally dry localities. glows have been reared in captivity by Tesh
(1970) in Panama. Baker and Petersen (1965) reported on some laboratory
behavior of Tylogzs, and postnatal development of five male and three

female Ototyloms were described by Disney (1968).

 

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Ototylonrvs

 

 

 

 

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Distribution of 1210318 and Ototylonws

Figure 1.

MATERIALS AND METHODS

The Tqumys used in this study were descended from Mexican animals
caught 8 kilometers east of Rio Grande at an altitude of 30 meters,
Oaxaca; 16 kilometers south of Valle Nacional, at an altitude of 1280
meters, Oaxaca; and from.captives donated by R. Tesh from.El Acquacate,
Panama. The Ototylcmys were all offspring of animals live-trapped by
James A. Lackey and Thomas Nelson, 7% kilometers west of Escarcega,
Campeche, Mexico. The animals were maintained in the Michigan State
University'NMSeum.Live Animal Colony'in cages measuring 91.5 cm.x 45.5 cm
x 45.5 cm, Sawdust was used as bedding, and each pair of animals was
furnished with a nest-box. Their diet consisted chiefly of Zimmerman
Laboratory Rat Chow which was supplemented periodically with fruits. Room
temperature was 21 degrees Centigrade. From September 1970 until March
1971, the colony was subjected to natural lighting. From.March 1971 until
December 1972, the controlled lighting was 12 hours of light and 12 hours
of dark. Each animal was toe-clipped at birth for easy identification.

Data for postnatal development were obtained from 95 individual
Tyiogys (including more than 45 litters) and 86 individual Ototylomys
(including 36 litters). Total length, tail length, hind foot length, ear
length, and body weight were measured weekly for all animals from the day
of birth (day 1) to three months of age and then monthly until six months
of age. Timing of incisor erruption, of first hearing response (flinching
to finger snapping), and separation of eyelids were also recorded for
these animals. Mean measurements of Tylomys from.Mexico and Panama were
compared by one—way analysis of variance to evaluate the significance of

differences.

vaginal smears were obtained from 33 Tylggy§.and 14 Ototylggys in an
effort to measure the lengths of the estrous cycle and gestation and as an
aid in the determination of the onset of implantation. Smears were scored
by the methods of Long and Evans (1922) and Papanicalou, as modified by
wachtel (1969) and Zarrow (1964). Vaginal smears were taken during four
different time periods. The first were collected from 29 October 1970 to
15 April 1971, when samples were obtained daily from 22 female 113%
between 0900 and 1100 and stained with Geimsa Solution (Zarrow, 1964).

The second collection period was between 16 July 1971 and 1 October
1971 and involved 11 Tylomys. Six males and five females were put into
Unifab Rat Activity Cages, Series 450, in an isolated room. The cage
dimensions were 24 cm.x 19 cm x 19 cm, with a freely rotating wheel 36 cm
in diameter and 13 cm deep. The lighting schedule was 14:10, light:dark.
The animals were disturbed only between 0800 and 0900 and 1700 and 1800
daily when food and water were checked. Smears of the six females were
taken each morning from 6 September 1971 to 1 October 1971. The samples
are stained with toluidine blue and scored as to cell types, i.e. ..
nucleated epithelial cells, cornified epithelial cells, combination of
cells, or predominately leucocytes (Long and Evans, 1922). Comparisons of
estrous phenomena and cycles of running activity were made.

The third collecting period involved only Ototylomys. Between
17 OctOber 1971 and 9 February 1972, six male and six female Ototylggyg
were placed in activity cages and subjected to the same procedures as the
gylggy§_in the previous period. vaginal smears were taken only between
27 December 1971 and 9 February 1972.

The fourth collecting period extended from 21 October 1972 until

21 December 1972. vaginal smears were taken from eight non-pregnant and

one lactating 111m and from eight non-pregnant Otot lo 3, between 1400
and 1600. All animals were kept in the same room in the Museum Live Animal
Colony with a lighting schedule of 14:10, 1ight:dark. The smears were
stained by the Papanicalou method (Wachtel, _p. 3%.). Each smear was
observed under the microsc0pe at 150x. A representative section of the
slide was selected and the total number of cells seen in the field of
vision was counted. The calculated percentages of red, orange, blue, and
green cells were plotted against time to see if any cyclical patterns
existed.

Females with sperm in their vaginal smears were considered bred. The
date of sperm discovery was designated as day 1 of gestation. Animals
were palpated weekly until parturition, and the neonates were measured at
this time. Thirty 111013.23 litters (including 51 individual offspring) and
15 Ototylgrgzs litters (including 35 individual offspring) were sampled by
this method.

Five yloms females were examined to determine the time of
implantation, three by laparoscopy (Dukelow e_t_ 511., 1971), two by

laparotonry. Three Ototylomys were examined by laparotomy.

RESULTS

10 s

Estrous Okla

The vaginal cytology of Tylomys does not show predictable cyclicity.
Leucocytes are present at all times. The average interval between
cornified cell stages was found to be 6.8 i 0.4 days when the animals
were exposed to natural lighting. Exposure to a lighting schedule of
12:12, 1ight:dark, resulted in an average interval of 12.0 i 2.5 days
between cornified cell periods. An increase in the duration of smears
with predominately'leucocytes was attributed to the increase in overall
cycle length (Table 1).

0n the day immediately preceding the finding of cornified cells in
vaginal smears, only leucocytes and nucleated epithelial cells could be
found in varying ratios. Sperm was found in smears which consisted
predominately of nucleated epithelial cells and leucocytes. No specific
vaginal smear could predict when a female would accept a male for mating.

The handling of the animals when vaginal smears were obtained did not
seem to disrupt their use of the exercise wheel. The length of time
between maximum periods of wheel activity varied in a fashion similar to
that found in the smears (Table 2). The model intervals were two and
three days for all Tylomys females sampled. No predictions about running
activity could be made from vaginal cytology.

Tylomys females have a postpartum estrus, and mating occurs within
24 hours, as indicated by the presence of sperm in smears taken at this

time.

 

 

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10

Sexual Maturity

The earliest recorded mating for females occured at 90 days of age
and for males 144 days. This compares favorably to the age of earliest
sexual maturation observed by Tesh (1970). Small (5 x 3 mm) copulatory
plugs were discovered discharged into the litter in only four instances.
Sperm was found in all of the vaginae, and two of the four females

carried their litters to term.

Gestation

The overall gestation period for Tylomys is 40.6 i 0.5 days with a
range of 35-51 days (including 47 litters). For non-lactating females
the gestation period is 39.2 i 0.5 days with a range from 37-43 days
(including 18 litters). For lactating females the gestation period is
40.6 i 0.7 days with a range from 35-51 days (including 29 litters).
There is no statistical difference between the means implying no delayed
implantation due to lactation. Tesh (1970) found a minimum gestation

length of 39 days for one lactating female.

Prenatal Development

The earliest noticeable indication of implantation observed by
laparotomy or laparoscopy in Tylogys was four days after sperm were first
found in the vagina. Day 7 of gestation was the earliest time that
embryos could be detected by palpation. The fetal head was first
palpatable at 28 days. Fetal growth, as determined by palpation, was
approximately 10 mm per week (in crown-rump length) until birth at about
40 days. At that time, the crown-rump length was 50-60 mm. Table 3

summarizes the embryo size distribution through time.

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The ratio of male to female neonates in my colony was 95.6:100 and
for 68 neonates in Tesh's colony, 46:100. The average litter size was
2.3 young with a range of 1-4 in my colony and 2.67 in Tesh's colony.
Statistical comparisons of the measurements taken on the‘Tylggyg
populations from Panama and Mexico revealed no difference at day 1;
therefore data were pooled.

'Weight at birth was 20.2 i 0.3 gm. Birth weight for animals examined
by Tesh (1970) ranged from 15-25 gm, with an average of 19.9 gm.
Measurements at birth were: total length, 134.1 i 1.0; total length of
tail vertebrae, 50.0 i 0.7; length of hind foot, 18.0 1 0.2; height of ear
from notch, 8.5 i 0.04. The length of head and body without tail measured
84.3 i 0.7 mm. At birth the length of head and body without tail was 34.9
per cent of the mature body length in Tylogys from Mexico and 35.8 per cent
for Tylomys from Panama. There were no significant differences in body
weight or linear body dimensions between males and females at birth.

The skin of Tylomys at birth is gray-black on the dorsum and pink on
the venter. The dorsum is finely furred at birth. The guard hairs measure
about 2 mm in length, while the underfur is less than 1 mm. The length
of verbrissae at birth ranges from 18-22 mm. The internal organs are not
visible through the skin. The ears are erect at birth. The toes are not
fused, and the tubercles on the feet of some animals are pigmented.
Incisors have errupted at birth and are separated by almost 1 mm.

The neonates adhere tenaciously to their mother's teats and remain
in the fetal position. Young which are separated at birth from the

mother are capable of self-locomotion.

13

Hearing and Eye @ening

The newborn do not respond to loud noises and have closed eyelids.
First ability to respond to finger snapping varied from day 6 to day 13
with the greatest number of Tylomys being able to hear first on day 8 or
9. Eye opening occurred between days 8 and 14 with the greatest number
occurring on days 10 and 11. The hearing response preceded eye opening
in all instances. Figure 2 is a histogram representation of the timing

of eye cpening and hearing.

9mm
Changes in body weight and linear measurements are shown in Figures
3 and 4. The measurements from day 84 to day 180 for the two populations
are represented separately, since statistical differences between the
samples from Mexico and from Panama are found for body length and weight
at 180 days. Tylomys from Mexico attain 50 per cent of adult body length
by day 14. The Panamanian population attains 50 per cent of adult body
length between days 12 and 14. Ninety per cent of adult length is
reached at 120 days in the Mexican Tylogys while the Panamanian lylogrys

reach 90 per cent adult body length about seven days earlier.

Pelage

Hair coloration changes from gray and white to a mottled gray-brown-
white between 10 and 17 days. The guard hairs are white along the sides
and black on the dorsum. The underfur is gray with black, brown, and
white tips. By 46 days, coloration of the dorsum has become a uniform
gray-brown. The sides are paler brown than the dorsum; the guard hairs
tend to be pale in color while the underfur is gray with brown tips. By
3 months, the change to adult pelage is complete with no specific molting

sequence noted.

NMnber of Individuals

l4

 

 

 

 

 

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Figure 2. Eye opening and first response to loud noises.

Length (mm)

440

420

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380 -

360

340 —

320

300
280

260

240

220

200
180

160

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120

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Figure 3. Growth of Tylomys from Mexico and

Panama (Y i Sx)'

16

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17

Ototylomys

Estrous Cycle

The vaginal cytology of Ototylogys does not show predictable
cyclicity. The average interval between cornified cell stages was found
to be 8.8 t 0.5 days (Table 1). On the day'immediately preceding the
finding of cornified cells in vaginal smears, leucocytes and nucleated
epithelial cells in varying ratios and mucosal secretions could be
found.

For all animals, activity decreased markedly when the vaginal smears
were taken (Table 2). The average interval between activity peaks in the
six females studied was 3.9 i 0.4 days when the animals were permitted to
run undisturbed and 4.1 i 0.4 days during the period when vaginal smears
were being collected. No predictable sequential activity pattern was
found fer any of the animals, nor was vaginal cytology predictive of
running activity.

The only consistent vaginal phenomenon was that smears with sperm
present stained red using the Papanicalou staining method. Other cells
present with the sperm varied from 100 per cent leucocytes to a mixture
of nucleated epithelial cells, cornified epithelial cells, and leucocytes.

Ototylomys females have a postpartum estrus. Mating had taken place
within 24 hours after delivery, as indicated by the presence of sperm in

these smears.

Sexual Maturity
Vaginal opening occurred from day 21 until 70 days. The earliest

recorded mating for a female occurred at 29 days of age. This resulted

in a pregnancy which terminated 52 days later. Testicular descent

18

occurred between 15 and 38 days. The earliest recorded mating for a male
was at 175 days. Disney'(l968) indicated both sexes reached sexual
maturity within 30 days. In two instances, a small (less than 5 mm.x 2 mm)
vaginal plug was discovered while taking vaginal smears. Additional

efforts were unsuccessful in discovering copulatory plugs.

Gestation

The overall gestation period for Ototylogys is 52.8 i 2.1 days. For
non-lactating females, the range is 50-52 days (including 6 litters) and
for lactating females this range is more variable and is 49-69 days
(including 9 litters). There is no statistical difference between the
average of 51 i 0.6 days for non-lactating and 53.6 i 7.6 days for
lactating females. Disney (gp.lgi§.) reported a gestation length of 52
days for a captive-born female. He also suggested that delayed
implantation might occur since another female was isolated in the

laboratory for 174 days after which she had a litter of two.

Prenatal Development

The earliest noticeable enlargements of the uterus observed by
laparotomy'were at day 8 of gestation. Day 14 was the first day when
embryos could be palpated. At this time the embryos were about 5 mm long.
'Weekly development thereafter was 5-10 mm until parturition at 52 days.
The head was first distinguishable by palpation between 21 and 28 days of

gestation. Table 3 gives the size distribution of both Ototylogys and
Tylomys.

Birth
The ratio of males to females at birth was 115:100. The average

litter size was 2.4 with a range of 1—4. Disney'(gp, git.) reported

19

average litter sizes to be 2.3 and 2.2 for two groups of wild-trapped
Ototylggys. No sex ratio was reported. Disney also noted that larger
females tended to have larger litters; however, this was not confirmed by
data from.my colony.

At birth, Ototylomys weigh 10.2 i 0.3 gm. Their standard measurements
are: total length, 119.5 f 0.9; total length of tail vertebrae, 47.1 i
0.8; hind foot length, 16.4 i 0.2; height of ear from notch, 9.4 i 0.2.
The length of the head and body (without the tail) is 67.0 i 3.2. The
least variance over time seems to be observed in length of head and body.
This parameter is especially valuable when the animals get older since
there is a tendency for tails of laboratory raised Ototylggys to become
necrotic and fall off. At birth, the body is 46.4 per cent of the adult
length. Males tend to be 1 or 2 mm shorter than the females although
differences between means are not significant. Males and females weigh“
the same at birth. The length of verbrissae is about 20 mm and both pairs
of incisors are present at birth. The tubercles of the fcrefeet do not
tend to be pigmented, while those on the hind feet do tend to be pigmented.
Both feet have unfused toes.

Ototylomys young are quite precocial at birth. They adhere strongly
to one of the mother's four inguinal teats and assume a fetal position.
When separated from the mother, the young can walk quite well and are

able to hang suspended from objects.

Hearing 9g Eyg yning

The newborn Ototylomys do not respond to loud noises and have closed
eyelids. The largest number of young Ototylomys respond to finger
snapping (hear) by'day 2. One animal could not hear until day 6. The

largest number cpened their eyes on day 6. The earliest eye openings

20

were on day 2. 'With the exception of four animals, ability to hear
preceded eye cpening by at least one day. Both phenomena were observed
on the same day in these animals. Figure 2 is a histogram representation

of the timing of hearing and eye cpening.

Ma
Figures 5 and 6 show growth rate measurements including total tail,

body, hind foot, ear length, and body weight. Ototylomys reach 50 per

cent of their adult body length between days 1 and 2. They have reached

over 90 per cent of adult length by 58 days of age.

Pelage
The skin of neWborn Ototylogys is graysblack on the dorsum and pink

on the venter, and both the dorsum.and venter are sparsely haired. The
internal organs are not visible through the skin. Hair on the dorsum.
range from 2-4 mm in length and are black with white tips, giving an
overall gray appearance to the hair. The hair on the venter is white and
less than 1 mm long. The tail is also bicolored and is covered.with fine
hairs. The ears are erect at birth and a large white spot is found under
each ear. These spots remain throughout adulthood.

At about 21 days, the gray hair of the sides begin to be replaced by
brown hair. By 43 days adult coloration has been attained. No definite

molting pattern Was observed.

Length (mm)

300

280
260
240
220
200

180

160

140
120

100
80
60
40

20

21

 

   

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Days

Figure 5. Growth of Ototylomys (I 1' sx).

” Hind foot
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22

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DISCUSSION

Ms and Ototylogzs are members of a group of Central American
cricetine rodents, Neotominae (based on phallic material: Hershkovitz,
1962; Hooper and Musser, 1964; Lawlor, 1969). The evolutionary trends
for all of the Percmscus-like rodents, including Neotominae and
Peromyscinae, have been diagramed by Hooper and Musser (93. gi_t_.: 55).
Within the neotomines (including Xenoms, Neotoma, Nelsonia, films, and
Ototylms), Tyloms and Ototylomyg are the most primitive. The
neotomines are more primitive than the percnvscines (including Scotin s,
Baioggzs, Onychoms, Ochrotomvs, Neotomodon, Peromyscus, and
Reithrodontogzs ) .

My data indicate that neither m nor Ototyloms have a regular
or predictable estrous cycle. 2210323 did not seem to be disturbed by
being handled in the laboratory (as evidenced by the activity wheel
experiment). On the other hand, manipulations of Ototyloms in the
laboratory proved to be a traumatic experience (as evidencdd by the
activity wheel experiments). Another member of Cricetidae (but not a
peromyscine or neotomine), Sigmodon hispidus was shown by Meyers and
Meyers (1944) to have an increased estrous cycle length when exposed to
a disturbed environment.

The only member of the neotomines whose cycle has been definitely
determined is Neotoma floridana (Chapnan, 1951). The most common cycle
was from 4 to 6 days in length. Chapman found that increased frequency
of handling the animals did not alter the length of their cycles. He
also did not find any difference between the cycle of females kept in the
laboratory and the cycles of females kept in outdoor enclosures.
Perogzscus maniculatus, the only peromyscine whose cycle has been

23

24

determined, was fOund by Clark (1936) to have an estrous cycle of 4.8
days in the laboratory.

The significancd'which can be attached to the findings of my study
and to the findings of other studies on estrous cycles of'myormorph
rodents is difficult to assess since so little information is available
from.which conclusions can be made.

The gestation lengths of’Tylomyp and Ototylggys are significantly
different from.each other and from those known for other genera of
Perggyscus-like rodents (tested by the MannAWhitney U—test, Sokal and
Rohlf, 1969: 392). ‘Within the neotomines, there is a slight tendancy
toward reduction of gestation length as one proceeds along the branch
which includes m and Ototylms (Figure 7). Within the
peromyscines, a similar reduction in gestation length is seen as one
proceeds toward the more modern animals (Figure 7). The larger
neotomines tend to have longer gestation lengths than do the smaller
peromyscines.

There seems to be a correlation of gestation length with a decrease
in body size within the neotomines. Tyggmy§_is the largest animal,
Otogylomys the smallest, and Neotoma the intermediate. Their gestation
lengths parallel this trend in body size. The peromyscines, as a group,
do not show such a trend, although Layne (g9, 223,) did find that the
larger members of the genus Perggxsous had shorter gestation lengths than
the smaller animals. He postulated that some phylletic relationship was
being expressed.

Examination of the suborder Rhomprpha reveals that only five species
have been reported as having gestation lengths as long as that found in
m: Motoms sumichrasti (Birkenholz, 1966), {Estrogzs W

25

References, Figure 7: *

l.

2.

Present study.

Present study.

Egoscue, 1957, 1962; Hamilton, 1953; Olsen, 1968.
Horner, 1968; Pinter, 1970; Taylor, 1968.

Brand and Rykman, 1968; Drickamer and Bernstein, 1972;
Layne, 1968; Rood, 1966.

Asdell, 1964: 259.
Linzey'and Linzey, 1967.

Blair, 1941.

Linzey, 1970;

* Arrangement of neotomines and peromyscines from Hooper and MMsser,

1964.

 

26

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27

(Hall at 51., 1967), Mesembriom gouldii (Crichton, 1969), m
dimidiatus (Walker, 1969: 935), and Tacmflctes mandae (Rahm, 1969).
No phyletic trends are seen in this small group of rodents. The
gestation length of Ototylgms is exceptionally long for the Myomorpha.
The Hystrichomorpha is the only group of rodents where gestation lengths
of 50 days er longer are found for animals whose body size is comparable
to that of Ototylogzs (§_e_e_ Tesh, 1970: 199; 1970: 201; Weir, 1970).

Ecological implications of the elongated gestation lengths found in
m and Ototylom are even more difficult to make than the
plwlogenetic ones. A prolonged gestation has been judged to be more of
an advantage for animals living in xeric habitats than for those living
in tropical habitats (Eisenberg and Isaac, 1963; Layne, 22. Ed. The
prolongation of gestation results in the production of more precocial
young which are better able to cope with their environment while placing
less strain upon the mother's resources (Layne, _p. 9213.; Smith and
McGinnis, 1968). Similar adaptive significance has also been postulated
for arboreal rodents living on specialized diets (Hamilton, 1962). Of
those animals with gestation lengths as long as Mg, only Mystrms
inhabits a xeric climate; the rest are of moist tropical origin.
Proechm’ semispinosus (Tesh, 1970: 201) and Diplogzs darlingi (Tesh,
1970: 199) are two tr0pical Hystrichomorpha with gestation lengths similar
to that of Ototylogzs. Many more data are needed on the gestation lengths
of tropical rodents before any conclusions can be made about the
ecological implications of gestation length.

Comparison of the postnatal growth of the lengths of head and body
(less tail) of m and Ototy’ lggzs for the first 28 days are

represented in Figure 8. Growth rates are parallel. An F-test

28

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29

comparison of the regression coefficient (by.x) for these two lines shows
these growth rates to be significantly different (0.05(p<0.025):
by.x=1'802fl'299 for Ototylonws and by.x=2.323-_|-O.2045 for M.

On the average, the eyes of m open at about the same time as
do the various species of Neotoma while Ototylms' eyes open from four to
eight days earlier. Eye opening occurs between 12 and 18 days for all of
the peromyscine group. 1% eye opening falls within this range while
Ototylms' eyes open 6 to 10 days earlier. All of the neotomines have
erupted incisors at birth. The peromyscines show incisor eruption from
12 to 18 days of age.

ELI-(M reaches 50 per cent of adult body weight at about the same
time as all of the other peromyscine rodents, i.e. about 14 days of age.
Fifty per cent of adult body weight is attained by Neotoma between 26 and
90 days of age. Ototyloms have attained 50 per cent of adult body weight
by two days of age. Fifty per cent of adult body length was reached by
M at about the same time time as other Permscus-like rodents
while Ototylms has grown to this extent at least four days earlier than
any of the other species in this group. No attempt has been made to
compare first response to finger snapping observed for m and
Ototylms to the other Perogzscus—like rodents, since this parameter is
not reported by the authors used as references for this paper (for
Neotoma, gag Egoscue, 1957, 1962; Hamilton, 1953; Rainey, 1956;
Richardson, 1943; for other peromyscines fl: Blair, 1941; Brand and
IVckman, 1968; Drickamer and Bernstein, 1972; Homer, 1968; Horner and
Taylor, 1968; Linzey, 1970; Linzey and Linzey, 1967; Layne, 22. gig).

Nipple-clinging observed in M and Ototylms appears to be a

common trait in Cricetidae and Muridae (Crichton, _p. cit.; Homer and

30.

Taylor, 9:9. 9:9,). Crichton (op. 'c_it_.) hypothesized that this trait
developed at an early time in the evolution of the murid group
Pseudomyinae. That a similar trend also occurred in Cricetidae is
evident by the fact that all members of the peromyscines and neotomines,
whose reproductive biology has been reported, exhibit nipple-clinging.
The adaptive significance would be two-fold. ~First, nipple-clinging young
have access to an immediate supply of nutrients, a necessary factor for
survival (Crichton, 92. gi_t.; Horner and Taylor, _p_. .c_i_t.; Layne, gp.
git.). Second, nipple-clinging young can be transported from one nest to
another or from potential predators with little wasted energy (Birkenholz,
1965; Egoscue, 1962; Layne, _p, 213.; Taylor and Horner, 1970). At the
same time, it might be argued that the added burden of nipple-clinging
young would hinder the mother's movements and therefore make her more
vulnerable to predators. If the young are sufficiently precocial to be
able to run along with the mother, rather than being dragged by her, the
awkward locomotion would tend to be streamlined and thus reduce her
vulnerability to predators. Ototylomys nest, have their young on the
ground, and utilize the trees for food and protection (Disney, 1968;
Williams, 1970). Laboratory observations have revealed that the young of
Ototylgmys do in fact run after their mother almost from birth.
Unfortunately, the field biology of Txlogys has not been examined as
thoroughly as Disney and Williams did for Ototylomys. I can therefore
only postulate that Tylomys occupies a more uniform environment than does
Ototylomys, i.e. primarily in trees, or among rocks or on the ground.
Species of Neotoma have been shown to occupy fairly uniform niches within
their habitats (s22: Egoscue, _p, git,; Finley, 1958; Murray and Barnes,

1969; Rainey, 1956). Tylomys postnatal development compares closely to

31

that of Neotoma. However, Eylomys gestation is longer than that of
Neotoma, and Tyggmyg young are somewhat more precocial than those of
Neotoma.

The exact evolutionary significance of these findings is not clear.
Tylogys and Ototylomys seem to be atypical forms within Cricetidae and,
more specifically, within Neotominae. Their long gestation lengths appear
to be primitive in form, especially as compared to other neotomines and
peromyscines, as does the nipple—clinging behavior of their young. The
reproductive biology of Tylomys is probably most adaptive for animals
concentrating their activities in one dimension of their environment but
still moving between two or more dimensions. Ototylomys has best adapted

for scansorial living.

SUMMARY

To summarize, the reproductive biology of two Neotropical climbing
rats, Tylomys and Ototylomys, were described and compared. Data
collectedifrom both genera included determination of the estrous cycle,
gestation length, occurence of postpartum estrus, and prenatal and post-
natal development.

Vaginal smears were collected from Tylogys exposed to two lighting
conditions. The average interval between cornified cell periods was 6.8
i 0.4 days under natural lighting and 12.0 i 2.5 days when exposed to 12
hours of light and 12 hours of darkness. Ototylogys kept in 14 hours of
light and 10 hours of darkness had an average estrous cycle of 8.8 t 0.5
days. A postpartum estrus was observed for all littering females of both
genera, as evidenced by the presence of sperm in smears taken within 24
hours after the discovery of new litters.

The earliest recorded mating for female Tylomys was 90 days of age
while the earliest recorded mating for female Ototylomys was 29 days of
age. The earliest recorded mating for males was 144 days for gylogys and
175 days for Ototylomys.

The gestation period for Tylogys was 40.6 i 0.5 days and 52.8 i 2.1
days for Ototylomys. No statistical difference was found between the mean
gestation lengths of lactating and non-lactating females for either genus.
Both the minimum and maximum extremes in gestation length were observed
in lactating females of both Tylomys and Ototylogys. Embryos were first
detected by palpation of Tylomys on day 7 of gestation and of Ototylomys
on day 14 of gestation. The fetal head was initially distinguishable at

28 days in both genera.

32

33

Only five other species included within the suborder Myomorpha were
found to have gestation lengths similar to Tylogys. The gestation length
of Ototylomys was exceptionally long for the Evomorpha, and only a few
species of Hystrichomorpha were found to have equivalent gestation lengths.
The sparsity of comparative information prevented speculation concerning
the ecological ramifications of the prolonged gestation length observed
for Tylomys and Ototylomys.

The ratio of males to females at birth was 95.6:100 and 115:100 for
Tylomys and Ototylomys, respectively. Tylogys had an average of 2.3
young per litter and Ototylomys had an average of 2.4 young. The range
in litter size was 1-4 in both genera. Statistical analysis of the
standard measurements at birth for the Mexican and Panamanian Tylogys
populations did not reveal any differences at day 1; therefore, the data
were pooled. The standard measurements, in millimeters, for Tylomys
were: total length, 134.1 i 1.0; tail length, 50.0 i 0.7; hind foot,
18.0 i 0.2; ear, 8.5 i 0.04. For Ototylomys they were: total length,
119.5 1 0.9; tail length, 47.1 i 0.8; hind foot, 16.4 i 0.2; ear, 9.4 i
0.2. Tylogys weighed 20.2 i 0.3 gm and Ototylomys 10.2 i 0.3 gm at birth.
The least variance over time was observed in the length of head and body,
without tail, and was therefore most valuable for comparisons of growth
rates over time. At birth, Tylomys measured 84.3 i 0.7 mm, and
Ototylomys measured 67.0 i 3.2 mm. Head and body length of gylogys from
Mexico was 34.9 per cent of adult body length; those from Panama were
35.8 per cent and Ototylomys were 46.4 per cent of their adult body
lengths. No statistical differences were found between males and females

at birth for either genus.

34

Semi-logarithmic plots of the regression coefficients for the
lengths of head and body of Tylomys and Ototylomys for the first 28 days
are parallel but significantly different.

For approximately 30 days after birth, the neonates of both genera
adhere tenaciously to their mother's inguinal teats, as do the young of
the neotomines and peromyscines. Both Tylomys and Ototylomys young are
precocial, with Ototylomys young being the more precocial. The greatest
number of Tylomys were initially able to respond to loud noises between
days 8 and 9, while the largest number of Ototylomys initially responded
by day 2. Eye opening occurred for the greatest number between days 10
and 11 in Tylomys and day 6 for Ototylomys. Hearing preceded eye opening
in all but four cases. The timing of eye opening observed in 10 s is
about the same as that observed for Neotoma and for the peromyscines.
Ototylomysl eyes Open four to ten days earlier than all other species
examined.

Tylomys from Mexico have attained 50 per cent of adult body length
by day 14 and those from Panama between days 12 and 14. This is at least
ten days earlier than that observed for Neotoma and about the same time
as the other peromyscines. Ototylomys reach 50 per cent of their adult
body length by day 2, at least four days earlier than any other closely
related species. Ninety per cent of adult body length is reached at 120
days in the Nbxican Tylomys while the Panamanian group grew to 90 per cent
of their adult body length by 116 days. Ototylogys grew to 90 per cent
of their adult body'length by 58 days of age.

The entire reproductive processes of Tylomys and Ototylomys were
judged to be primitive in form and best adaptive for animals utilizing

two or more dimensions of their environment.

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Nat. Hist. Bull., 35(20):357-376.

Asdell, S.A. 1964. Patterns of mammalian reproduction, second edition.
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Brand, Leonard and Raymond E. Rychman. 1968. Laboratory life histories
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Mamm., 49(3)3495-5Ol-

Burt, William Henry and Ruben A. Stirton. 1961. The mammals of El
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Cabrera, Angel. 1961. Catalgo de los mammiferos de America del Sur.
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Clark, Frank H. 1936. The estrous cycle of the deermouse, Peromyscus
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Chapman, Arthur 0. 1951. The estrous cycle of the woodrat, Neotoma
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Conaway, C.H. 1971. Ecological adaptation and mammalian reproduction.
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Crichton, Elizabeth G. 1969. Reproduction in the Pseudomyine rodent
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Disney, R.H.L. 1968. Observations on a zoonosis: leishmaniasis in
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. 1962. The busy-tailed woodrat: a laboratory colony.
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Eisenberg, John F. and Donald E. Isaac. 1963. The reproduction of
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. 1969. Mammals from Oaxaca. Bul. Am. Mus. Nat. Hist.,
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Hall, E. Raymond and walter W. Dalquest. 1963. Mammals of Veracruz.
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and Keith R. Kelson. 1959. The mammals of North
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Hamilton, W;J. 1953. Reproduction and young of the Florida woodrat,
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. 1962. Reproductive adaptations of the red tree mouse.

J.Mwmqlaflfldfi65mh

 

Handley, Charles 0. 1966. Checklist of the Mammals of Panama, In
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37

Horner, B. Elizabeth. 1968. Gestation period and early develOpment in
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and J. Mary Taylor. 1968. Growth and reproduction
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