Social Behavior W e describe ways in which male and female rodents invest in their young and consider fac tors that might influence the level of care that parents provide Some of these factors pertain[.]
Trang 1Social Behavior
Trang 3We d e s c r i b e way s in which male and female
rodents invest in their young and consider
fac-tors that might influence the level of care that
parents provide Some of these factors pertain to the young
(e.g., degree of development at birth, gender, number of
off-spring), others to the parents (e.g., experience, concurrent
pregnancy, other mating opportunities), and still others
con-cern aspects of the physical environment in which the
pa-rental care is displayed (e.g., from small cages to
seminat-ural environments in the laboratory to field conditions) We
next describe the impact of parental care on the survival and
growth of offspring, and conclude the chapter with a
pre-liminary analysis of the evolution of parental care in voles
(Microtus and closely related species).
Throughout the chapter we focus on studies evaluating
care shown by parents toward their own young from birth
through weaning and beyond By their very nature, such
studies require monitoring parent-offspring interactions for
several weeks We largely omit studies in which an
indi-vidual’s parental responsiveness is evaluated by short-term
tests of exposure to pups Individuals tested in such
exper-iments often are not parents or are tested with unfamiliar
young While our goal was to make a broad phylogenetic
survey of parental care in rodents, such care is best described
for small species of Sciurognathi, particularly for species of
Muridae such as rats, mice, voles, gerbils, and hamsters
Comparatively little information is available for species
within Hystricognathi Finally, because most studies on
ro-dent parental care have been conducted in laboratory
envi-ronments, such studies constitute our major data source
We include relevant field observations whenever possible
Forms of Parental Behavior
Parental behaviors are characterized as either direct or in-direct (Kleiman and Malcolm 1981) Direct parental care
includes behaviors that have an immediate physical impact
on offspring and their survival; in rodents, such behaviors include nursing (and feeding), grooming, transporting (most often retrieving), and huddling with young With the ob-vious exception of nursing, males can exhibit all forms of direct parental care Males of some species show levels of direct parental behavior comparable to those of females, while males of other species show little or no direct paren-tal behavior (see reviews by Elwood 1983; Dewsbury 1985; Brown 1993) Indirect parental care includes behaviors that may be performed by parents while away from the young; these behaviors do not involve direct physical contact with offspring but still affect offspring survival, although perhaps not immediately In rodents, indirect forms of parental care include acquiring and defending critical resources, building and maintaining nests and burrows, caring for pregnant
or lactating females, and defending offspring against con-specifics or predators Working definitions for typical direct and indirect parental behaviors based on comparative stud-ies of voles under seminatural conditions are shown in table 20.1 (see McGuire and Novak 1984, 1986) While
Chapter 20 Parental Care
Betty McGuire and William E Bemis
Trang 4not a specific category of parental behavior, “time in nest”
often provides an estimate of overall direct parental care
(table 20.1)
Direct care
Nursing
Mothers of altricial young are the sole source of early
nu-trition for their offspring (Alberts and Gubernick 1983), but
mothers of precocial young are not Precocial young
typi-cally supplement their diet of milk with solid food within
a few days of birth, although they continue to consume
milk for many weeks (Kleiman 1974; Gosling 1980)
Nurs-ing postures adopted by female rodents vary from
crouch-ing over pups to sittcrouch-ing or lycrouch-ing next to them (Kleiman
1974; Drewett 1983) Whatever form nursing takes,
lacta-tion is energetically costly to female mammals (Hanwell and
Peaker 1977; Stapp et al 1991); lactation also presents
chal-lenges to water balance, although female rodents recover
some of the water and electrolytes lost in milk by
consum-ing the urine of their pups durconsum-ing anogenital groomconsum-ing
(Al-berts and Gubernick 1983) In addition to nutrients, milk
contains antibodies that young rodents cannot produce on
their own until a few weeks after birth (Brambell 1970)
Feeding
When young rodents can eat solid food, mothers of altricial
species may bring food to the nest (e.g., woodchucks,
Mar-mota monax; Barash 1974b) while mothers of precocial
spe-cies may allow young to take food from their mouths (e.g.,
too, feed juveniles: muskrat (Ondatra zibethicus) males
pro-vision juveniles at the home burrow (Marinelli and Messier 1995) and white-footed mice (Peromyscus leucopus) males
accompany weaned young on foraging trips (Schug et al 1992)
Grooming Beginning at birth, pups are groomed extensively by moth-ers and sometimes by fathmoth-ers (e.g., spiny mouse, Acomys cahirinus; Dieterlen 1962; Djungarian hamster, Phodopus campbelli, and Siberian hamster, P sungorus; Jones and
Wynne-Edwards 2000; prairie vole, Microtus ochrogaster;
McGuire et al 2003) Parental grooming of the anogenital region stimulates urination and defecation in young pups until they are about 2 weeks old (Capek and Jelinek 1956; Rosenblatt and Lehrman 1963) In many species, grooming
of offspring continues well beyond when it is physiologically necessary for the young; it is likely that this grooming func-tions in the maintenance of parent-offspring bonds (Kleiman 1974; Libhaber and Eilam 2004)
Retrieving, huddling, socialization, and shoving Other common forms of direct parental care include retriev-ing offsprretriev-ing to the nest (or transportretriev-ing them to another location) and huddling with young, a behavior that provides thermoregulatory benefits Some direct parental interac-tions with offspring have been described as play or social-ization (e.g., green acouchi, Kleiman 1974; hoary marmot,
Marmota caligata; Holmes 1984a) Finally, naked mole-rat
(Heterocephalus glaber) parents shove pups around the
nest; this behavior encourages pups to flee from danger and
to avoid dangerous situations in the future (Stankowich and Sherman 2002)
Indirect care Constructing and defending burrows and nests Burrow or nest construction and maintenance by male and female parents have been described in the field for muskrats (Marinelli and Messier 1995) and for many species in the laboratory (e.g., plateau mouse, Peromyscus melanophrys;
et al 2000) Territorial defense against conspecifics, espe-cially around the nest, is common for most if not all ro-dents, and helps to defend food resources or to protect young from infanticidal conspecifics (Sherman 1981a; Wolff 1993b; Hoogland 1995; Wolff and Peterson 1998) Small size limits most species from defending young against predators, although male and female prairie voles re-acted aggressively to shrews in the vicinity of the natal nest and effectively prevented predation on their pups in
semi-Table 20.1 Categorization of parental behaviors displayed by voles
(Microtus spp.) under seminatural conditions (modified from McGuire and
Novak 1984, 1986)
Direct parental
behavior
attachment
attachment
carrying it back to the nest Indirect parental
behavior
later use Spatial location
re-lated to parenting
overall measure of direct care
Trang 5natural environments (Getz et al 1992) Parental defense
against small predators also has been reported for free-living
black-tailed prairie dogs (Cynomys ludovicianus, Hoogland
1995) and naked mole-rats (Lacey and Sherman 1991)
Sev-eral species warn their young with antipredator calls (e.g.,
Belding’s ground squirrel,Spermophilus beldingi; Sherman
1981b; hoary marmot; Holmes 1984a; black-tailed
flaviventris; Blumstein et al 1997; Blumstein, chap 27 this
parturition in response to the threat of predation (Gosling
et al 1988)
Food caching
Pine vole parents (Microtus pinetorum) carry food to
spe-cific locations where they store it in a pile for later use, and
males bring food directly to the natal nest (McGuire and
Novak 1984; Oliveras and Novak 1986) This behavior by
male pine voles may constitute male provisioning of food
for lactating females
Attendance at the nest
A behavior recently reported for social voles (Microtus
so-cialis guentheri), termed “forced babysitting,” does not fit
the traditional categorization of direct or indirect care, but
is relevant to parental behavior One parent, typically the
male, aggressively drags the other back to the nest to
re-main with the pups while it leaves the nest (Libhaber and
Eilam 2002) Male and female prairie voles coordinate
ar-rivals and departures at the natal nest such that young are
rarely left unattended, but the aggressive dragging of forced
babysitting does not occur (McGuire and Novak 1984)
Factors that Influence Parental Behavior
In this section, we discuss seven factors that influence
parental behavior As in previous sections, most research
on these topics emphasizes sciurognaths and is laboratory
based
Degree of development of young at birth
The degree of development of young varies along a
con-tinuum from altricial species typical of the Sciurognathi to
precocial species typical of the Hystricognathi Altricial
species are born naked with closed eyes and ears, have poor
sensory and locomotor abilities for several days after birth,
and are confined to a nest In contrast, precocial species
have longer gestation periods, and their young are often
fully furred, with open eyes and ears at birth, and can
loco-mote almost immediately (Kleiman 1972; Weir 1974)
Al-tricial young rely exclusively on milk for about the first
2 weeks of life and then gradually begin to consume solid food; in contrast, precocial young may supplement milk with solid food immediately after birth (Kunkele and Trill-mich 1997) Although most sciurognaths are altricial, ex-ceptions occur (e.g., spiny mouse; Dieterlen 1962; Porter and Doane 1978)
Species with altricial young tend to give birth from a sit-ting or lying position and young are expelled in front of the female (e.g., Djungarian hamster and Siberian ham-ster; Jones and Wynne-Edwards 2000; prairie vole; Mc-Guire et al 2003) In several species with precocial young, parturient females assume a standing position and expel the young behind their body (e.g., spiny mouse; Dieterlen 1962; guinea pig,Cavia porcellus; Kunkel and Kunkel 1964; green
acouchi; Kleiman 1972) Kleiman (1972) and Dieterlen (1962) noted that standing postures during parturition are assumed by other mammals with precocial young, such
as ungulates, and suggested that standing during parturi-tion may be an adaptaparturi-tion to the delivery of large, well-developed offspring However, at least one species of rodent with precocial young, the cuis (Galea musteloides), gives
birth from a sitting or lying position (Rood 1972); more data are needed to confirm that differences in birth position correspond to degree of development of young Maternal aggression during and after parturition is characteristic of species with precocial young (Kleiman 1972) and of those with altricial young (Dewsbury 1985; McGuire et al 2003), and likely functions to deter infanticidal conspecifics (Maes-tripieri and Alleva 1990; Wolff and Peterson 1998) Rodents with precocial young often exhibit lower levels
of nest building and pup retrieval than do species with al-tricial young (Kleiman 1974) For example, some species with precocial young do not build a nest (e.g., guinea pig; Kunkel and Kunkel 1964) or build only a temporary nest to which they retrieve young for only a few days after parturi-tion (green acouchi; Kleiman 1972) Mothers of precocial young typically use maternal contact calls to inform their highly mobile offspring of their location and to induce fol-lowing (Kleiman 1972) In contrast, females with altricial young often build an elaborate nest before parturition and maintain the nest through the preweaning period (Nor-way rat, Rattus norvegicus; Denenberg et al 1969; meadow
vole, Microtus pennsylvanicus; pine vole; and prairie vole;
McGuire and Novak 1984) Typically, altricial young first venture from the natal nest a few days after their eyes have opened, and these brief forays trigger initially frequent re-trieval back to the nest by mothers (and fathers in some spe-cies) In several species of voles, for example, eyes open 10 –
12 days postpartum, and a day or two later pups begin to make brief trips from the natal nest; retrieval by mothers occurs frequently during the early forays but then declines
Trang 6in frequency over the next few days, and eventually stops
(McGuire and Novak 1984, 1986)
Despite the apparent independence of precocial
off-spring, mothers significantly influence their physiology and
behavior (Hennessy 2003) For example, many precocial
young start to eat solid food when only a day or two old
and can survive without milk by 1 or 2 weeks, but nursing
frequently continues for several weeks or months (Rood
1972; Kleiman 1972, 1974; Makin and Porter 1984)
Moth-ers of precocial young also continue to groom their
off-spring well beyond the time when such grooming functions
to stimulate urination or defecation (Kleiman 1972, 1974) The continued association between mothers and young, ex-emplified by prolonged nursing and grooming, is appar-ently beneficial to both (Kleiman 1974)
Litter size Mothers spend more time in the nest with small than with large litters (see table 20.2, column In nest) One
explana-Table 20.2 Maternal behavior in relation to litter size among selected rodents
norvegicus)
Ader 1969; Ader and Grota 1970; Grota 1973
Hofer 1973
Driscoll 1981
and Alleva 1990
tus socialis) Eilam 2004
onomys glareolus) 2002
myscus
mani-culatus)
unguiculatus) Broom 1978
(Mesocricetus
auratus)
Nunes 2001
porcellus) Broner 1970
philus citellus)d
NOTES: S higher in small litters; L higher in large litters; X no difference with respect to litter size (modified from Mendl [1988: Tables III, IV] and updated with additional information) A artificial manipulation of litter size, N natural litters Unless otherwise indicated, studies were conducted in the laboratory and patterns of behavior measured
by duration, frequency of occurrence, or percent of the observation period spent performing the behavior Empty cells indicate that the behavior was not recorded in the study.
a Rating of maternal quality which included categories such as response to opening of cage, reluctance to leave litter, retrieval of young, and quality of nest (Seitz 1958); sum of time percentages per observation period for nurse, groom pup, and nest build (König and Markl 1987).
b Attacks by mother directed at unfamiliar male conspecifics.
c Represents time spent by mother in bodily contact with young.
Trang 7tion is that mothers of large litters may need to spend more
time outside the nest foraging to meet nutritional demands
associated with providing milk to a large number of young
(Priestnall 1972; Mendl 1988) Another explanation is that
mothers of small litters must help pups maintain their body
temperature, whereas pups in larger litters may not require
such help because they can huddle with more littermates
(Priestnall 1972; Mendl 1988) Other evidence suggests,
however, that littermates are relatively ineffective at
main-taining a warm nesting environment (Webb et al 1990)
Fi-nally, mothers of large litters may experience problems with
hyperthermia, and so spend more time away from pups,
dis-sipating heat (see Jans and Leon 1983 regarding maternal
hyperthermia) Given the diversity of rodents, the absence
of detailed behavioral studies, and the possibility that more
than one of these explanations may apply to a case, we
can-not establish a single cause for the observed pattern
A second general pattern to emerge is that mothers wean
large litters later than small litters (see table 20.2, column
Age at weaning) Mothers may wean offspring when they
reach a certain minimum weight, and this weight is achieved
earlier in small than in large litters (Cameron 1973; König
and Markl 1987)
No clear patterns emerge concerning litter size and the
time that mothers spend nursing, grooming young, or nest
building (see table 20.2, columns Nurse, Groom pup, Nest
build) This inconsistency is chiefly because there are few
comparable studies and criteria for behavioral categories
differ across studies Two reports indicate that maternal
ag-gression toward unfamiliar male conspecifics increases with
litter size (see table 20.2, column Attack) This result
sup-ports predictions that risks to mothers of defending young
should not change with litter size, but that benefits of such
defense should increase with number of offspring
(Maestri-pieri and Alleva 1990; Jonsson et al 2002)
Much less is known about litter size variation and
pa-ternal care, but some observations are available For
ex-ample, male gerbils (Meriones unguiculatus) exhibited more
frequent pup grooming and body contact when litters were
large but more nest building when litters were small
(El-wood and Broom 1978) Paternal care in social voles is
essentially independent of litter size (Libhaber and Eilam
2004)
Artificially manipulating litter size creates complications
that make interpretation of results difficult Mothers in
na-ture may adaptively adjust their number of offspring
ac-cording to their own condition, abilities, and prevailing
en-vironmental conditions, so measures of parental behavior
may not vary with litter size In contrast, females that
nat-urally give birth to small litters and then have their litter size
experimentally increased may be greatly challenged
Fur-ther, litter augmentation would be a very unusual situation
under natural conditions Although reductions in litter size
would not be unusual in field populations, experimental re-duction to very small litter sizes (e.g., one or two pups) may
be extreme and may disrupt milk production or thermo-regulation in the nest Finally, pups can display fidelity to certain nipples (e.g., in prairie and pine voles; McGuire 1998; McGuire and Sullivan 2001) and transferring pups between litters, even on day 1 postpartum, can disrupt development of such preferences Some researchers have teased apart the adjustments that nursing mothers make us-ing methods to change offsprus-ing food demand (by manipu-lating their access to solid food) without changing litter size, but this approach only works for precocial species such as guinea pigs (Laurien-Kehnen and Trillmich 2003) Additional studies of unmanipulated litters of different sizes are needed
An intriguing cross-species example of litter size varia-tion is reported in naked mole-rats (Sherman et al 1999) While most rodents have mean litter sizes equal to about one-half the number of mammae (Gilbert 1986), naked mole-rat queens raise litters on average equal to the number
of mammae (about 12) Extremely large litters —up to 28 and 27 offspring — are reported in field and laboratory col-onies, respectively Sherman et al (1999) state that such large litters are possible because offspring take turns nurs-ing at the same nipple and colony members feed and pro-tect the queen
Gender of offspring Differential investment by mothers in male and female off-spring has been examined in the context of parental invest-ment theory, especially as it relates to mating systems (Triv-ers 1972; Triv(Triv-ers and Willard 1973; Sikes, chap 11 this volume) In polygynous species (where variance in repro-ductive success is typically greater for males than females) mothers in good condition are predicted to bias their invest-ment toward sons, while mothers in poor condition should invest in daughters Sex-biased parental investment may be reflected in the sex ratio of offspring produced or in dif-ferent amounts of care shown to sons and daughters dur-ing the postnatal period (for reviews see Clutton-Brock
et al 1981; Clutton-Brock and Iason 1986; Cockburn et al 2002) There is some evidence that female rodents adap-tively manipulate the sex ratios of their litters during the prenatal period (e.g., coypus; Gosling 1986; golden ham-sters, Mesocricetus auratus; Labov et al 1986; house mice, Mus musculus; Krackow and Hoeck 1989; Krackow 1997).
Here, we focus on differential parental investment during the postnatal period
Some studies examined postnatal maternal investment in male and female offspring under ad libitum food conditions For example, Gosling et al (1984) found differential invest-ment in male and female offspring in the polygynous coypu;
Trang 8male offspring spent more time than female offspring
suck-ing from the highest-yieldsuck-ing teats, although this pattern
appeared to result from the behavior of young and not from
the mother’s active promotion or discouragement of
par-ticular offspring from sucking from specific teat locations
Clark et al (1990) found that female gerbils rearing all-male
litters were much more likely than females rearing all-female
litters to be in the nest with young and to have pups attached
to their nipples Norway rat mothers and house mouse
mothers spend more time licking the anogenital region of
male than female pups, and also show enhanced nursing and
nest building when rearing all-male litters (Moore and
Mo-relli 1979; Richmond and Sachs 1984; Alleva et al 1989)
Rat mothers appear to use olfactory cues to discriminate
the gender of their offspring (Moore 1981) and the
spe-cific chemosignal comes from the preputial glands of pups
(Moore and Samonte 1986)
Other studies of differential postnatal parental
invest-ment compared mothers with unrestricted access to food to
mothers whose food was restricted during lactation; greater
investment by food-restricted mothers in female offspring
was predicted Food-restricted eastern woodrats (Neotoma
floridana) invested more in female offspring, as evidenced
by higher mortality and reduced growth of male offspring
(McClure 1981) Female-biased investment also is reported
for food-restricted golden hamster mothers (Labov et al
1986) In contrast, Sikes (1995, 1996b) found no evidence
of sex-biased maternal investment in food-restricted eastern
leu-cogaster; also see Sikes chap 11 this volume) Finally, recent
evidence indicates that male-biased mortality in polygynous
species may occur independently of parental discrimination
Moses et al (1998), working with bushy-tailed woodrats
(Neotoma cinerea), suggested that male-biased mortality in
offspring of food-restricted mothers might reflect the greater
energetic demands of male offspring, resulting from sexual
selection for faster growth and greater body size
Compar-ative data for rodents on differential postnatal maternal
investment in male and female offspring remain equivocal
and the topic requires further study
Concurrent pregnancy
Postpartum mating in some groups of rodents results in
con-current pregnancy and lactation (Gilbert 1984) Although
less costly than lactation, pregnancy imposes energetic
costs (e.g., bank voles, Clethrionomys glareolus;
Kaczmar-ski 1966) Levels of maternal care by pregnant females are
generally lower than in nonpregnant females; such
differ-ences arise late in lactation as birth of the new litter
Markl 1987; Norway rats; Rowland 1981; Wuensch and
Cooper, 1981; but see McGuire 1997 for red-backed voles,
Clethrionomys gapperi, and Krackow and Hoeck 1989 for
house mice) Lower levels of maternal care by pregnant fe-males could result from the increased energetic demands faced by such females Other options for pregnant females include diverting energy from young in utero or from them-selves (Oswald and McClure 1987) All studies noted were conducted in laboratory conditions with abundant food nearby, and no temperature stresses
Social environment Many laboratory studies have examined effects of social ex-perience on rodent parental behavior (McGuire 1988; Leh-mann and Feldon 2000; and reviews by Dewsbury 1985; Brown 1993; Kinsley 1994) Here, we discuss how presence
of other males or mating opportunities influences paternal care, and review studies that examine how the composition
of a social group influences parental behavior
Males often disproportionately increase reproductive success by seeking additional matings rather than by pro-viding paternal care (Trivers 1972; Clutton-Brock 1989b) Thus paternal care in rodents should decrease as mating op-portunities increase, and this has been found in the field for two normally monogamous species, hoary marmots (Ba-rash 1975a) and muskrats (Marinelli and Messier 1995) In the laboratory, parent-offspring interactions in polygynous meadow voles were studied in a 2.4 by 1.2 m enclosure (Storey et al 1994) Introduction of an estrous female did not significantly reduce the time fathers spent in the nest with their pups, even though many fathers mated with the introduced females The enclosure’s size may have made
it easy for males to mate with estrous females without sig-nificantly reducing their time in the natal nest (Storey et al 1994) Difficulties observing paternal care in the field and the need to provide extensive space in the laboratory make
it challenging to study the relationship between paternal care and mating opportunities in rodents
Field and laboratory studies show that the presence of one parent can influence care shown by the other parent Pa-ternal presence correlates with decreased maPa-ternal behavior
in species such as rock cavies (Kerodon rupestris, studied
in laboratory cages; Tasse 1986), Norway rats (studied in an outdoor pen; Calhoun 1962a), gerbils (studied in labora-tory cages; Elwood and Broom 1978), red-backed voles (studied in seminatural laboratory environment; McGuire 1997), and muskrats (studied in the field; Marinelli and Messier 1995) The muskrat example is interesting because free-living polygynous males only provided care to young of their first mate, and these primary females displayed lower levels of maternal behavior than did secondary females, who compensated for the lack of male assistance by increasing
Trang 9their investment (Marinelli and Messier 1995) When male
rodents provide care for young, decreased maternal
behav-ior in the presence of males has been interpreted as evidence
of reduced maternal workload When males are present but
do not care for offspring, decreased maternal behavior has
been attributed to disruption caused by paternal presence;
increased maternal care in such circumstances is rare
Un-changed levels of maternal behavior in the presence of
fa-thers are reported for wild house mice (studied in
labora-tory cages; König and Markl 1987), prairie voles (studied
in seminatural laboratory environments; Wang and Novak
1992; Wilson 1982b), meadow voles (studied in
seminat-ural laboratory environments; Storey et al 1994) and
col-lared lemmings (Dicrostonyx richardsoni, studied in
labo-ratory cages; Shilton and Brooks 1989)
Maternal response is a major factor influencing the level
of paternal care For example, females of biparental species
frequently exclude males from the natal nest during
par-turition and for about a day thereafter, but subsequently
permit males to fully interact with young (gerbils; Elwood
McCarty and Southwick 1977b; spiny mice; Porter et al
1980; white-footed and deer mice, Peromyscus spp.; Wolff
and Cicirello 1991; prairie voles; McGuire et al 2003) In
other species, female aggression toward mates may extend
throughout the preweaning period (meadow voles; McGuire
Mc-Guire and Novak 1986; white-footed mice; Xia and
Mil-lar 1988; but see Wolff and Cicerello 1991); in such species,
male interactions with young occur primarily after
wean-ing Indeed, increases in male-offspring interactions with
pup age have been reported for meadow voles (Oliveras and
Novak 1986; Storey and Snow 1987) and montane voles
(McGuire and Novak 1986) in the laboratory, and
post-weaning paternal care of young has been reported in a
nat-ural population of white-footed mice (P leucopus; Schug
et al 1992) and deer mice, P maniculatus (Wolff and
Cici-rello 1991) The duration of maternal aggression toward
fa-thers is not necessarily consistent within a species; for
ex-ample, female red-backed voles vary in the intensity and
duration of aggressive behavior toward fathers, and this
pro-duces variation in levels of paternal care (McGuire 1997)
Few studies have examined experimentally how
mater-nal presence affects patermater-nal behavior (apparently
polygy-nous taxa, such as spiny mice, Makin and Porter 1984 and
collared lemmings, Shilton and Brooks 1989; and
polygy-nous meadow voles, Storey et al 1994) Maternal removal
is problematic because it interferes with suckling and pup
nutrition Such removal is less problematic in species with
precocial young, such as the spiny mouse, for which Makin
and Porter (1984) conducted near-daily observations of
par-ents from day 1 to day 23 postpartum On any given day,
they observed pairs with their young and then temporarily removed mothers to observe paternal behavior Males hud-dled with their offspring more when the mother was absent than when she was present, again confirming that females regulate interactions between fathers and offspring Juveniles also can affect care shown by parents to a younger litter Norway rat mothers attack juveniles before and after the new litter is born, but juveniles still spend time
in the nest with neonates (Gilbert et al 1983) Maternal care in the presence of such juveniles is similar to that dis-played in their absence (Grota and Ader 1969; Gilbert et al 1983) Female spiny mice nest with their mate and juveniles from the previous litter both before and after a new litter is born, but keep both males and juveniles away from the nest
on the day of parturition (Porter et al 1980) Under semi-natural conditions, female meadow voles aggressively ex-clude juveniles from the nest containing the new litter (Wang and Novak 1992); increased nest defense resulted in greater maternal workload compared to females rearing pups with-out juveniles present In contrast, female prairie voles allow juveniles in the natal nest and experience reduced maternal workload in the presence of juveniles if the father is also present (Wang and Novak 1992) Presence of juveniles also may reduce paternal workload in prairie voles, but this is the only species for which data exist (Wang and Novak 1992)
Levels of paternal care positively correlate with paternity (Westneat and Sherman 1993), but this topic has received little attention in rodents, with most studies focusing on in-fanticidal rather than paternal behavior An exception con-cerns work with meadow voles (Storey and Snow 1987) In one experiment, males spent less time in the nest with their mate’s pups when another adult male was housed in a nearby wire enclosure A second experiment compared lev-els of nest attendance by males housed with their mate and pups to that of males housed with a female rearing young
of another male; time spent with pups was much higher for fathers than for nonfathers Thus reduced paternal care in meadow voles correlates with uncertain paternity
Parenting experience Rodents can gain parenting experience by helping to care for a younger litter in their social group (alloparental care)
or by caring for their own young in successive litters In the laboratory, alloparental experience results in enhanced re-productive performance, pup growth, and development in gerbils (Salo and French 1989), but the effects of alloparen-tal experience in other species are slight and often mixed (Solomon and Getz 1997) For example, adult prairie voles with alloparental experience did not differ in their parental behavior from those without alloparental experience, but
Trang 10their pups developed slightly faster (Wang 1991) In still
other species, such as naked mole-rats, it is not known
whether alloparental experience affects subsequent
paren-tal behavior and success in rearing young (Lacey and
Sher-man 1997)
Reproductive experience can influence neuroendocrine
physiology of female rodents For example, experience
causes changes in the endogenous opioid system that
medi-ates olfactory-based interactions between mother and
off-spring (Kinsley 1994) Parity also can influence maternal
behaviors, although effects range greatly No effect of
par-ity is reported for captive female wild house mice (König
and Markl 1987), deer mice, or white-footed mice
(Har-tung and Dewsbury 1979) Social environment may
deter-mine whether parity affects maternal behavior in Norway
rats When rearing young in the absence of males,
multi-parous and primimulti-parous females did not differ in nursing,
nest building, and retrieving (Moltz and Robbins 1965), or
in the overall time spent with litters (Grota 1973)
How-ever, when rearing young in the presence of males,
multi-parous females more effectively switched between neonatal
care and mating during postpartum estrus; such females
also more effectively retrieved pups (Gilbert et al 1984)
Ex-perience also enhances pup retrieval in other species (house
mice; Cohen-Salmon 1987; golden hamsters; Swanson and
Campbell 1979) In a particularly striking example,
multi-parous female prairie voles spend more time caring for
off-spring than do primiparous females, yielding more rapid
physical development and a higher survival rate of young
(Wang and Novak 1994)
Few studies examine the effects of parity on paternal
be-havior Prior parenting experience had no effect on paternal
behavior in prairie voles (Wang and Novak 1994) or
white-footed mice (Hartung and Dewsbury 1979) Minor changes
in a few behaviors are reported for other species, such as
deer mice (Hartung and Dewsbury 1979) and Norway rats
(Brown 1986a) Thus at this time, previous experience as a
male caregiver appears to have little or no effect on
pater-nal care of rodents
Physical environment
Most rodents care for young in underground burrows or
covered nests, making it difficult to observe parent-offspring
interactions in the field, particularly before weaning Direct
field observations are available for some relatively large
di-urnal species (hoary marmots; Barash, 1975a; black-tailed
prairie dogs, Hoogland 1995) and for at least one small
Schradin and Pillay 2003) Even though observations
in-side the nests of striped mice are not reported from the field,
time spent at the nest by parents has been recorded, and
parental interactions with offspring have been studied once young are old enough to venture from the nest (Schradin and Pillay 2003) Other field studies of parent-offspring interactions involve indirect measures such as trap associa-tions and patterns of space use revealed by radiotelemetry (Schug et al 1992)
Testing environments in laboratory studies range from small cages with little or no cover to seminatural environ-ments with extensive space and cover Patterns of nesting and parental care can vary with the size and complexity
of the testing environment For example, when families of meadow and montane voles were studied in small cages in which nesting material was the only source of cover, no sex differences were apparent in the amount of time parents spent in the nest with pups (fig 20.1a; Hartung and Dews-bury 1979) In contrast, when these same species were stud-ied in seminatural environments that provided substantial space and hay cover, females of both species aggressively excluded males from natal nests; males nested separately and spent very little time with young pups (fig 20.1b; Mc-Guire and Novak 1984, 1986; Oliveras and Novak 1986) The latter results are consistent with reports from natural populations of female-only care of young and separate nest-ing by adult males and females durnest-ing most of the breednest-ing season (Madison 1980b; Jannett 1980) Studies on parent-offspring interactions in white-footed mice reveal a very similar pattern; whereas males in small cages show sub-stantial pup care (Hartung and Dewsbury 1979), males in larger enclosures are excluded from nests by females (Xia and Millar 1988), and the latter pattern is more consistent with what is known about nesting and space use by males and females in natural populations (Wolff and Cicirello 1991) Female aggression toward strange males might be interpreted as defense of young, but the reasons why fe-males aggressively exclude mates from the natal nest remain unclear
Conflicting findings, such as those described previously, may indicate that the pup care reported for some species
in small cages is a laboratory artifact (McGuire and Novak
1984, 1986; Wolff 2003c) Alternatively, males of these spe-cies have the potential to display paternal behavior, and may do so under certain conditions (Dewsbury 1985) For example, free-living male and female meadow voles some-times nest together during colder months (Madison et al 1984), and thus paternal care is possible under conditions
of late autumn or winter breeding Indeed, male meadow voles housed under short day lengths displayed longer grooming and huddling bouts with young than did males housed under long day lengths (Parker and Lee 2001) Ad-ditional data on parent-offspring interactions at low tem-peratures are needed from field or seminatural environ-ments to confirm facultative paternal care in this species