Nordic Society Oikos
Body Size, Breeding Season Length, and Life History Tactics of Lagomorphs
Author(s): Robert K. Swihart
Source: Oikos, Vol. 43, No. 3 (Dec., 1984), pp. 282-290
Published by: Blackwell Publishing on behalf of Nordic Society Oikos
Stable URL: http://www.jstor.org/stable/3544145 .
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OIKOS43: 282-290. Copenhagen1984
Body size, breedingseasonlength, and life historytacticsof
lagomorphs
Robert K. Swihart
Swihart,R. K. 1984. Body size, breedingseason length, and life historytacticsof
lagomorphs.- Oikos 43: 282-290.
Patternsof reproductionwere investigatedfor 22 species of lagomorphs(rabbits,
hares, pikas). Neonatalbody mass, gestationtime and maternalreproductiveeffort
duringgestationscaled allometricallywith body mass of adult females. In keeping
with theirrelativelyaltricialstate at birth,Sylvilagus(Gray)exhibitedshortergestation periods and lighter neonatal body masses than comparablesize-independent
values for Lepus (L.).
of lagomorphswas explainedby
Muchof the variationin reproductivecharacteristics
body size and phylogeny.However, analysisby principalcomponentsrevealedreproductiveparametersthat were largelyindependentof body size. Examinationof
these second-orderstrategiesshowed that lagomorphsdiffer regardingrates of developmentandthe mannerin whichoffspringare produced(i.e., littersize, maternal
investment).Breedingseasonlengthis a primarydeterminantof this differentiation.
Selectionhas favoreda reproductivestrategyin highlyseasonalenvironmentscharacterized by fewer, larger litters, whereas long breeding seasons permit increased
productivityvia reducedage at first reproductionand increasediteroparity.
The meanfetal growthrate of lagomorphswas morerapidthanratesof otherorders
of eutherianmammals,but maternalreproductiveinvestmentduringgestationwas
similaramongorders.
R. K. Swihart, Museum of Natural History and Dept of Systematics and Ecology,
Univ. of Kansas, Lawrence, KS 66045, USA.
(KPOJMKOB, 3akMeB,
HccnenoBaH xapaKTep pa3MHoxKeHHI y 23 BH.OB 3atneo6pa3HDU
rnuyx) . HeoHaTa.rIHasI Macca Te/na, ATHITeJIbHOCTb epeMeHHOCTH H pePrpoAyKTHBHb1I
H3MeHqeTCH C MaCCOT TeJIa y
ycnex caMOK 3a oqgHy 6epeMeHHOCTb annoMeTpIqecKH
"rITeHIOBbM" COCTOHHemMrnpH
B3pOCTbhX CaMoK. B COqeTaHHH C MX OTHOCHTe.TIbHO
6epeMeHHOCTH, MeHbllaR
pcmneHHH, y Sylvilagus
(Cray) 6onee KopOTKHe nepHoai
HeOHaTaJibHafI Macca TenIa, IeM cpaBHIHMe He3aBHCHMle OT pa3Mepa BeJI-NWHb y
B xapaKTepHCTHKax pa3MHO)eHIH y 3aftueo6pa3BoEnbUMHCTBO BapHaLar
(L.).
Lepus
Hb)X O6'bCHoKT pa3MepaBM Tena H jinoreHMHet.
OgHaKO, aHanIH3 no IrpHHLni,Ha&IbHba
Macarra6ax
HeKOMnIOHeHTaM
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noKa3ana,
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B OTHCLIIeHPH
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pa3snnaioTcH
pa3Mepz nIoMeTa, MaTepHHCKEH BKJIa,) . npo0no0rrrpoH3BOgCTBa nOTOMCTBa (T.e.
3TOfi HI4XepeHLUpOBKH.
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C pe3KO BbpaBxeHHOR ceOT6Op CTHMyJnpyeT perlpO,
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IOCH
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rIpo,Q1DHITeJTbHieb ce30oH pa3MHOcKeHH noI3BTOJio)T yBeBaTb amIPOIyKTHBHOCTb
CHIwKeHH1B03paCTa gOCTH5KeHLHnonIOBOf 3penIOCTH H nOBbIleHi4H IaCTOTbI pa3MHO)KeHHH. CpeDHFH31 gMpHOHaJIbHaq CKopOCTb pocTa y 3aiH.eo6pa3HbIX
Bbiie, qeM y nrpe,CTaBHTeJIef4 3qpyrHx OTapgAOB nTa.eHTapHbix MneKonHTaKIw4X, HO MaTepHHCKHH perlpo$ryKTHBHbIBKJIa BO BpeMfv 6epeMeHHOCTH TaKOI )Ke, KaK B pWyr,X OTpIHax.
Accepted 4 November1983
?
282
OIKOS
OIKOS 43:3 (1984)
1. Introduction
Recent studies have elucidated generalized life history
strategies in mammals (Millar 1977, 1981, Blueweiss et
al. 1978, Eisenberg 1981, Zeveloff and Boyce 1980,
McNab 1980). By documenting "typical" mammalian
life history traits, these studies promote critical examination of strategies for more closely related taxa (e.g.,
Marmotini by Armitage 1981; Canidae by Bekoff et al.
1981), particularly taxa exhibiting atypical strategies
(Clutton-Brock and Harvey 1978).
Reproductive characteristics of the order Lagomorpha (rabbits, hares, pikas) provide a striking example of divergence from basic mammalian life history
tactics. Relative to other eutherian mammals, lagomorphs exhibit extremely rapid fetal and neonatal
growth rates (Millar 1977, 1981, Case 1978, Eisenberg
1981), short gestation periods (Millar 1981), and low
maternal investment in offspring (Millar 1977, Zeveloff
and Boyce 1980). The nearly cosmopolitan distribution
of lagomorphs (Walker 1975) attests to the success of
their high-fecundity approach (McNab 1980). However,
patterns of variation in reproductive parameters within
this order have not been evaluated.
Allometric scaling of life history traits with body size
is fundamental in distinguishing traits arising solely as a
consequence of size (first-order strategies) from traits
that vary between populations and environments (second-order strategies) (Western 1979). However, interrelationships among life history parameters may complicate interpretations of univariate scaling (Millar 1981).
Principal component analysis (PCA) provides a means
of examining uncorrelated variables (minor components) after eliminating body size as a confounding factor. That is, PC1, the major component, typically represents a multivariate assemblage of first-order strategies,
whereas minor components represent independent second-order strategies shaped by environmental factors. I
use principal components to examine reproductive
strategies within the Lagomorpha and among several
orders of mammals.
Specifically, objectives of this paper are to (1) collate
and summarize data on reproductive characteristics of
lagomorphs, (2) describe interspecific differences in life
history traits among lagomorphs, and (3) compare reproductive characteristics of lagomorphs with other
mammalian orders.
2. Methods
2.1. Lagomorphlife historytraits
Reproductive characteristics of 22 species of lagomorphs (Tab. 1) were obtained from over 150 literature
sources. For seven species, data were sufficient to enable partitioning into geographically distinct regions;
mean species values were computed in all other instances. When possible, post-breeding season body
19* OIKOS 43:3 (1984)
masses of adults were used. Breeding season is defined
as the intrannual interval from first conception to last
parturition. Similarly, number of young produced per
female in a breeding season is defined as the total number of litters possible (assuming postpartum estrus;
Asdell 1964) multiplied by mean litter size. Clearly, this
value overestimates female productivity (e.g., Lechleitner 1959, Flux 1981); however, it circumvents methodological disparities in calculation of female productivity among studies and serves as a useful index.
Several indices of maternal reproductive investment
were computed (cf. Armitage 1981). Reproductive index at birth (RIB) is neonatal body mass divided by
adult female body mass. RIB is a mass-specific measure
of maternal investment prior to parturition. Likewise,
reproductive index at weaning (RIW), the body mass of
one young at weaning divided by adult female body
mass, is an index of the relative effort of a female to
produce one independent juvenile. Specific reproductive effort at birth (SREB) and at weaning (SREW) are
mean litter size multiplied by RIB and RIW, respectively. Hence, SREB represents a mass-specific index of
energetic expenditure during gestation, whereas SREW
is a mass-specific index of total resources committed to
reproduction (i.e., during both gestation and lactation).
Fetal growth rates (FGR) were calculated by
FGR = W"33/(G- cG)
(Huggett and Widdas 1951), where Wn = neonatal body
mass (g), G = gestation time (days), and c = 0.4 for
lagomorphs (see Millar 1981). Postnatal growth rates
(PGR) were computed as
PGR = (ln Ww- In Wn)/L
(Simpson et al. 1960, Whitworth and Southwick 1981),
where Ww = body mass at weaning (g) and L = lactation time (d).
Proportion of adults present in the population prior
to the breeding season was used as an index of annual
adult survivorship (Petrides 1949).
After logarithmic transformations, principal component analysis with orthogonal varimax rotation
(BMDP4M; Dixon 1981) was performed using neonatal
and adult female body mass, gestation period, litter
size, number of young per season, age at first reproduction, RIB, and SREB. Values for RIW, SREW, FGR,
and PGR were too few to permit incorporation into the
multivariate analysis; however, correlations between
these variables and scores for each principal component
were computed. Components with eigenvalues less than
one were not included in the analysis.
2.2. Mammalianlife historytraits
Adult and neonatal body masses, gestation period, litter
size, and fetal growth rate for 328 species of nonvolant,
283
Tab. 1. Life historytraitsof 22 species of lagomorphs.Wf = adult female mass, Wm = adult male mass, Wn = neonatalmass, G =
gestationperiod(days), AFR = age at firstreproduction(days),FGR = fetal growthrate (g.33/day),PGR = postnatalgrowthrate (Ing
d-l).
Body mass (g)
Growthrates
Litter Young Breeding
Wf
Wm
Wn
G
AFR
FGR
PGR
size
per
season
Sylvilagus aquaticus (1).....
S. aquaticus (2) ..........
S. audubonii ............
S. bachmani ..............
S. floridanus (1) ..........
S. floridanus (2) ..........
S. floridanus (3) ..........
2169
1993
948
648
1413
1288
1208
2238
1977
891
626
1398
1203
1124
55.1
56.0
33.0
30.0
34.6
30.5
31.8
37
39
28
27
28
27
28
230
152
130
159
80
98
130
0.169
0.159
0.189
0.190
0.192
0.194
0.186
0.055
0.077
0.069
0.065
0.087
2.9
2.8
3.4
3.4
5.3
5.1
3.2
14.5
16.8
27.2
23.8
42.4
40.6
25.6
S. nuttallii ................
790
720
S. palustris ................
1246
1179
952
906
30.0
28
Lepus alleni ...............
L. americanus (1) .........
L. americanus (2) .........
L. americanus (3) .........
L. arcticus ................
L. californicus (1) .........
L. californicus (2) ........
L. europaeus ..............
3719
3629
1430
1550
1307
1201
1700
3664
3728
2210
2450
2718
2332
4130
4230
105.5
52.0
57.9
70.0
105.0
68.7
63.7
141.0
42b
36
37
36
50b
42
43
42
228
214
255
315
144
198
-
3540
3710
110.0
42
2099
4813
2922
2110
3521
1520
1844
4751
2721
3147
1680
100.0
87.3
110.0
100.0
34.0
1573
1597
418
471
138
184
Speciesa
S. transitionalis ..........
(North America)
L. europaeus ..............
(Britain)
L. nigricollis ............
L. othus ..................
L. timidus ................
L. tolai ..................
.
L. townsendii ...........
Oryctolagus cuniculus (1)...
(Europe)
0. cuniculus (2) ...........
(Australia)
Brachylagus idahoensis.....
Romerolagus diazi .........
Ochotona princeps (1)......
0. princeps (2)............
0. rufescens ..............
462
132
166
250c
-
-
-
29
90
38
183
-
-
91
0.183
0.060
Adult
season survivorship
202
244
214
198
214
216
233
0.17
0.19
0.28
0.23
5.0
20.0
103
3.0
27.0
330
4.5
27.0
180
1.9
3.8
2.9
4.4
5.8
3.6
2.1
1.9
15.2
15.2
11.6
13.2
5.8
18.0
12.6
11.4
335
139
154
111
53
197
274
256
0.43
0.24
0.185
0.170
0.172
0.188
0.155
0.160
0.153
0.203
0.062
0.075
0.098
0.046
0.093
-
244
0.187
0.074
2.7
18.9
290
46b
50
46
42b
29
320
300
320
258
105
0.166
0.128
0.171
0.181
0.184
0.060
0.067
0.071
1.8
6.3
2.5
3.8
4.1
4.4
6.3
10.0
14.2
16.4
17.6
365
50
214
172
148
148
36.3
30
105
0.182
-
3.8
26.6
205
0.46
45.0
10.0
11.7
11.4
39
30
30
25
226
0.119
0.125
0.150
0.082
0.062
0.068
6.0
2.5
2.3
3.1
6.0
18.0
4.6
9.3
-
116
63
100
-
0.42
0.55
0.56
303
-
0.30
0.23
0.45
0.19
0.23
0.68
0.45
0.35
0.43
a. Numbersin parenthesesrepresentrelativegeographiclocalitiesof populationsfor a species, with (1) indicatingthe northernmost
population.
b. Approximatevalues.
c. Sex-specificmasseswere not available.
3. Results
3.1. Interrelationships
of life historyvariables
terrestrial mammals were extracted from the literature
(primary sources were Millar 1981, Eisenberg 1981, Armitage 1981, and Bekoff et al. 1981). In addition, RIB
and SREB were calculated for these species. Principal
components were generated using these 7 variables, and
between-order comparisons of mean component scores
were conducted using GT2 a posteriori comparisons
(Sokal and Rohlf 1981). Note that a comparison of
results from the lagomorph and mammalian principal
component analysis is not strictly valid, because different combinations of life history variables were used
in the two analyses.
284
Numerous significant correlations exist among lagomorph life history traits (Tab. 2). Adult female body
mass is highly correlated with neonatal body mass and
gestation period and negatively correlated with SREB.
SREB, SREW, RIW, and litter size were negatively
correlated with length of the breeding season. In addition, number of young per female per season was negatively related to age at first reproduction, SREW, and
adult survivorship. Age at first reproduction was
positively correlated with SREW and adult survivorship
(Tab. 2).
Basal metabolic rate in mammals is proportional to
adult body mass raised to the 0.75 power (Kleiber
1975); thus, life history traits governed by metabolic
OIKOS 43:3 (1984)
Tab.2. Correlationmatrixof lagomorphlife historytraits.Abbreviationsare definedin Tab. 1. See text for definitionsof SREB, RIW and
SREW. Only significantr values (P < 0.05) are shown. Samplesize for each correlationmay be obtainedfrom Tab. 1.
Wf
Wf (female mass).....
Wn(neonatalmass)...
G (gestation).........
AFR................
FGR ................
Littersize ...........
Young/season........
Adult survivorship....
SREB ...............
1.00
0.95
0.73
Wn
G
1.00
0.84
0.51
1.00
0.77
0.44
AFR
FGR
1.00
-0.58
1.00
-0.79
0.59
0.61
0.84
0.69
-0.40
0.42
Tab.3. Comparisonof meanstandardizedresidualsvia analysis
of variancefor threegeneraof lagomorphs.Adultfemalemass
was the predictorvariablein each regression.Means with a
commonsuperscriptform homogeneoussubsets(a = 0.05).
*P < 0.01.
OIKOS 43:3 (1984)
F
5.89*
0.55
11.19*
1.00
-0.51
SREW Breeding
season
1.00
1.00
0.60
-0.51
-0.62
rate should scale with adult body mass in a similar
manner. Using adult female mass as the predictor variable, a regression was conducted on log-transformed values for neonatal mass. The neonatal mass:female mass
regression yielded a slope (0.74; R2 = 0.90, P < 0.001)
that was not different from 0.75 (P > 0.05). Massspecific basal metabolic rates scale to the -0.25 power
(McNab 1980). SREB, a mass-specific trait, scaled with
female body mass to the -0.28 (R2 = 0.39, P < 0.001),
suggesting that total maternal investment at birth is
dependent on metabolic rate. The time required to do a
unit of metabolic work is proportional to adult body
mass raised to the 0.25 power (Stahl 1962). However,
the slope of 0.17 (R2 = 0.53, P < 0.001) for gestation:female mass was significantly less than 0.25 (P <
0.05).
To test for scaling differences among genera, standardized residuals from each regression on adult female
body mass (predictor variable) were subjected to analysis of variance with GT2 a posteriori comparisons (Tab.
3). This approach permitted comparison of values of
dependent variables in each regression by controlling
for the influence of adult female mass. Three genera
were used in each test: cottontail rabbits Sylvilagus,
hares Lepus, and pikas Ochotona (Link). Average neonatal body mass of Sylvilagus was less than that predicted by the regression equation (log Wn = -0.66 +
Neonatal mass ....
............
SREB
Gestation time ....
RIW
1.00
-0.62
RIW ................
SREW ..............
Breedingseason......
Dependent
Variable
SREB
Adult
Litter Young
size
per survivorship
season
Sylvilagus Ochotona Lepus
-0.65a
-0.28a
0.46ab
0.12a
0.55b
0.23a
-0.73a
1.10b
0.54b
-0.64
-0.74
-0.57
0.42
0.68
-0.77
1.00
0.59
-0.73
1.00
-0.83
1.00
Tab. 4. Sorted rotated factor loadingsfor 8 lagomorphlife
historytraits. Loadingsless than 10.5001were omitted. Numbers in parenthesesrepresentthe proportionof variationexplainedby each component.
Variable
Adult female mass.........
Neonatalmass............
RIB .....................
Gestationtime............
Age at first reproduction...
Youngper season .........
Littersize ................
SREB....................
VP ....................
PC1
0.989
0.849
-0.758
0.631
2.967
(0.371)
PC2
PC3
0.545
0.742
0.963
-0.882
2.891
(0.361)
0.884
0.861
1.556
(0.195)
0.74 log Wf) and significantly (P < 0.05) smaller than
observed body masses of Lepus neonates, corrected for
adult size (Tab. 3). Sylvilagus also exhibited shorter
gestation periods than predicted, and these periods
averaged less than similar size-independent values of
Lepus and Ochotona (log G = 1.01 + 0.17 log Wf; Tab.
3). Residuals were similar among genera for the
SREB:female body mass regression (log SREB =
-0.04 - 0.28 log Wf; Tab. 3), indicating a compensatory increase in litter size by Sylvilagus associated with
proportionately smaller neonates.
3.2 First- and second-order strategies of lagomorphs
Three principal components explained 92.7% of the
variation in the 8 life history traits subjected to multivariate analysis (Tab. 4). PC1 represents a general size
variable; large scores on PC1 are characteristic of large
species with a relatively low energetic investment in
individual young prior to birth (e.g., L. californicus, L.
othus). Long gestation periods and large young also
typify these species. PC2 is primarily a developmental
variable; large scores on this component typify species
285
-
Fig. 1. Results of a principal
component analysis,
illustrating segregation of
genera of lagomorphs with
regard to the second-order
strategies developmental
rate (PC2) and litter sizeoverall maternal investment
(PC3). Dashed boundaries
depict (from left to right)
Orystolagus,Sylvilagus,
Lepus, and Ochotona.
Sylvilagusand Orystolagus
_
s
Fetal
SREB
VP
....................growth
...
_
/
0.956
(0.465)
3.255
rate ...
...
s
\
(0.289)
2.024
0.970 (0.188)
1.319
-
,
;' floridonus (1 )
> >
tronsitionolis >_
_
olo
_
_
_
,
tolca;
_____
vX
bachmani J
_
arcticus '
, americanus (3)
0.8 z
xfloridanus (2)
-
othus
I
-
', townsendii /
_
^
\
z
- n xaudubonTio,tamericonus
- g cuniculus (1)} C .
_--,'
(1)
americanus (2
"
W)'
-
0 cuniCulus (2)1
differ significantly from
Lepusalong PC2.
/
f
{californicus (1)
lf Ipnnceps (1)
)
-
-
-0.8
-
z
floridanuA (3)
-__
',<europoeus
__
aquoticus (2) * . j }
- _ aqucticus (1 ) o X
\
timidus
-1 .6 -
^)
-
/
tucalifornicus (2) ,
_
,
-0.75
1 .25
0.25
PC2
with slow developmentalrates (gestation time, age at
first reproduction)and few young per season (e.g., O.
princeps,
L. tolai,L. arcticus).
Large scores on PC3
characterizespecies with largelittersand a high overall
energetic investment at birth (e.g., L. arcticus,
L.
othus,
S.floridanus
(1)).
PC1is an assemblageof first-order(i.e., size-related;
Western1979)characteristics.The notion thatvariables
with high loadingson PC1 are causallyrelatedto body
size is reinforcedby observingthat all three of these
traits(Wn,RIB, G) scale allometricallywith Wf in approximatelythe mannerpredictedby body-sizeenergetics. Conversely, PC2 and PC3 representuncorrelated
measuresof reproductiveattributesthat are largely(although not entirely) independent of body size (i.e.,
second-order characteristics).This orthogonalityenables comparisons of reproductive strategies (PC2,
PC3) that are essentiallyuncoupledfrom the influence
of body size. Significantdifferentiationof genera occurredalong PC2 (F = 3.56, df = 2,18, P < 0.05) but
not along PC3 (F = 0.03, df = 2,18, P > 0.25) (Fig. 1).
Comparisonof mean scores revealed that both Sylvilagus
(x = -0.81) and Orystolagus
(x = -1.17) differed significantly(P < 0.05) from Lepus
(x = 0.66)
with regardto the developmentalcomponent,PC2.
PC2 was negativelycorrelatedwith fetal growthrate
(r = -0.67, P < 0.001), thus supportingthe interpretation of PC2 as a generalizeddevelopmentalvariable.
PC2 also was positively correlatedwith SREW (r =
0.62, P < 0.02) and RIW (r = 0.82, P < 0.001). Further,
RIW (r = 0.74, P < 0.001) and SREW (r = 0.55, P <
0.05) were correlatedwith PC3. None of these variables
was correlated significantly with PC1; in addition,
286
postnatalgrowthrate was correlatedwith neither PC2
(P > 0.20) nor PC3 (P > 0.20).
3.3. First- and second-order strategies of mammals
Threecomponentsaccountedfor 94.2%of the vanation
presentin the 7-variablemammaliandata set (Tab. 5).
As with the lagomorphdata, PC1 representsbody size
and that portion of reproductivecharacteristicscorrelated with body size. PC2 representsmaternalreproductive effortat birth,andPC3 representsfetal growthrate
(Tab. 5).
Meancomponentscoresfor 13 ordersdifferedsignificantlyfor PC2 (F = 48.1, df = 12, 313; P < 0.0005) and
PC3 (F = 33.0, df = 12, 313; P < 0.0005). Marsupials
(Diprotodonta and Polyprotodonti
a) differed signifi-
Tab. 5. Sorted rotated factor loadings for 7 mammalian life
history traits. Loadings less than 1° 5°°l were omitted. Numbers in parentheses represent the proportion of variation explained by each factor.
Variable
Neonatal mass ....................
Gestation time ....................
Adult mass ....................
Litter size ....................
RIB ...
PC1
PC2
PC3
0.974
0.936
0.891
-0.751
0.981
OIKOS 43:3 (1984)
Fig. 2. Segregation of 13
mammalian orders with
regard to maternal
reproductive effort at birth
and fetal growth rate, as
revealed via principal
component analysis. Note
the divergence of
Lagomorpha along PC3 and
the separation of
metatherians from
eutherians along PC2.
Lagomorpha
a
1.25
'I
a
Carnivora
Perissodactyla
4I
.(0
L
A
^
Artiodactyla
0.25 -
-
Rodentia
Polyprotodontia
o,
A
Scandentia
A
Insectivora
,
Edentata
3 -0.75
A
A
Macroscelidea
0.
Hyracoidea
- Diprotodonta
I
!I
,
Primate
I
I
,
I
I
I
A
A
I
0.25
-0.75
-1.75
-2.75
-3.75
PC2 - Maternal Reproductive Investment
Tab. 6. Mean PC2 and PC3 scores for 13 orders of mammals.
Orders sharing a common superscript form homogenous subsets (a = 0.05).
Order
Polyprotodontia ........
Diprotodonta..........
Insectivora ............
Edentata ..............
Macroscelidea .........
Lagomorpha ...........
Rodentia ..............
Hyracoidea ............
Scandentia ............
Primate ...............
Carnivora .............
Perissodactyla .........
Artiodactyla ...........
n
PC2
6
6
20
5
3
18
123
2
3
40
58
6
36
-2.92a
-0.15ade
-4.53b
0.44d
-0.17cd
-0.67acf
--0.60acde
0.91cd
-0.68acde
0.07cd
1.46b
0.09d
-1.12acde
0.44d
0.16cd
0.43cd
0.11d
-0.54c
-0.20cd
0.17d
PC3
-1.42ac
-0.25abcd
-1.47c
0.68be
0.37df
0.28de
cantly from each other and from all other orders with
respect to maternal investment prior to birth (Tab. 6,
Fig. 2). Also, carnivores invested significantly less in
offspring during gestation than artiodactyls, primates,
insectivores, or rodents (Tab. 6, Fig. 2). Differences
among mean scores for PC3 were complex (Tab. 6).
Briefly, lagomorphs and carnivores exhibited the highest fetal growth rates, whereas slowest rates were exhibited by primates and diprotodont marsupials.
OIKOS 43:3 (1984)
4. Discussion
of life historytraits
4.1. Interrelationships
Life history traits coevolve (Stearns 1976, 1983); thus,
interrelationships among various traits are inevitable.
Although dependencies among variables demand a cautious approach to interpretation of simple correlations
(Millar 1977, 1981), several relationships in Tab. 2 deserve closer inspection.
Traits that depend on rates of metabolic activity
should correlate with body size (Western 1979). Hence,
it is not surprising that gestation period and fetal growth
rate are related to adult female mass (Tab. 2). Neonatal
mass and SREB scale with adult mass in a manner
similar to basal metabolic rate, suggesting that neonatal
size and reproductive effort at birth are governed at
least partially by body-size energetics in lagomorphs. In
addition, larger females invest relatively less in each
offspring (Tab. 2). Similar relationships have been discovered for ground squirrels (Armitage 1981).
Females with a fixed allocation of resources presumably face an evolutionary tradeoff in determining the
number of young to produce each season and the outlay
of maternal investment that maximizes numbers of surviving offspring (Burley 1980, Tallamy and Denno
1982). Inverse correlations between number of young
per season and two measures of maternal investment,
RIW and SREW, illustrate this point (Tab. 2). The
length of the breeding season influences production of
young and maternal investment; longer breeding seasons permit production of more young per season, born
in smaller litters, and characterized by faster develop287
ment (Tab. 2). Short breeding seasons force concentration of maternal resources into a few large litters;
hence, species with short breeding seasons (e.g., L.
othus, L. arcticus, 0. princeps) are characterized by
large values for maternal investment indices (Tab. 2),
even though maternal investment over the entire breeding season may be larger in species with long breeding
seasons (e.g., L. alleni, L. europaeus; see Flux 1981).
Random variation in reproductive success should
favor increased adult survival, lower fecundity, and
later age at first reproduction (Murphy 1968). Among
lagomorphs, long-lived species are characterized by
fewer, larger offspring per season and by delayed maturation (Tab. 2). For instance, swamp rabbits S. aquaticus produce a few, large young per season, display fairly
high adult survivorship, and are characterized by a later
age at first reproduction than other congeners (Tab. 1).
Nestling mortality due to flooding occurs intermittently
in this species (Sorenson et al. 1972); thus, reproductive
success may vary greatly over time.
Lagomorphs commonly are envisioned as reproductive specialists, unsurpassed among mammals in their
ability to produce large numbers of offspring. However,
reproductive characteristics within the Lagomorpha are
not uniform; genera differ with respect to several reproductive traits (Tab. 3). On a mass-specific basis,
Lepus exhibits relatively larger offspring and longer
gestation times than Sylvilagus. This pattern is consistent with generic differences in development at birth;
neonatal hares are well-furred, alert, and mobile
(Grange 1932, Haskell and Reynolds 1947, Reynolds
and Stinson 1959, Banfield 1974), whereas neonatal
cottontail rabbits are sparsely furred, blind, and lacking
motor coordination skills (Ingles 1941, Orr 1942, Ecke
1955, Hunt 1959). In contrast, Millar (1981) reported
below average birth weights for Lepus and above average birth weights for Sylvilagus when compared with
mammals from 10 orders. From this he concluded that
differences in developmental patterns were not reflected in reproductive traits of lagomorphs. The lack of
concordance between the present findings and those of
Millar (1981) probably arose because he used taxonomically diverse groups of mammals when computing
"average" values for reproductive parameters (see
Stearns 1983).
physiological and morphological factors (Lindstedt and
Calder 1981).
Body size and phylogeny do not explain all the variation in life history tactics, though. A portion of the
residual variation is undoubtedly due to noise resulting
from errors in estimation of reproductive parameters.
In addition, some of the variation that is not explained
by body size may be explained by environmental factors
(Vitt and Congdon 1978, Western 1979). In lagomorphs, variation in rate of development, maternal investment at birth, and litter size appear to be influenced
much more by environmental variables than by body
size (Tab. 4).
Although phylogenetic constraints may play an important role in determining developmental rates (see
above), I believe that rates of development are largely
second-order strategies in lagomorphs (Tab. 4), because
gestation time and age at first reproduction may be
subjected to intense selection (Murphy 1968, Gadgil
and Bossert 1970, Sacher and Staffeldt 1974). First reproduction is achieved prior to 6 months of age in only 1
of 12 populations of Lepus and Ochotona, whereas 9 of
10 Sylvilagus populations are capable of reproducing at
this age (Tab. 1). Not coincidentally, the majority of
cottontail populations examined inhabit relatively mild
regions (30-45? N lat.) in the eastern United States.
Conversely, pikas occupy talus slopes at high elevations
(Broadbooks 1965, Smith 1978), and North American
hares are limited to arid grassland, desert, boreal forest,
and tundra environments (Hall 1981). Furthermore,
number of young per season in lagomorphs is governed
primarily by breeding season length, not by litter size
(Tab. 2).
I believe that litter size and SREB, characteristics
closely associated with PC3 (Tab. 4), are predominantly
second-order strategies also, because breeding season
length dramatically affects both of these traits (Tab. 2).
In highly seasonal environments, lagomorphs opt for a
big-bang reproductive strategy coupled with relatively
great maternal investment in offspring (e.g., L. othus,
L. arcticus). Long breeding seasons promote a strategy
characterized by increased iteroparity and reduced investment per litter (e.g., S. aquaticus, L. alleni, L.
europaeus) (Sadleir 1969; but see Flux 1981). For instance, L. othus, an occupant of the Arctic tundra,
produces one litter of 6.3 young per breeding season (50
d). Conversely, L. europaeus averages 2.7 young per
4.2. Influence of body mass, phylogeny, and breeding season
litter and theoretically is capable of producing 7 litters
In many mammalian groups, body size and phylogeny per breeding season (290 d) in the milder climate of
are the features that most strongly influence evolution Great Britain.
of life history characteristics (Western 1979, Stearns
In addition to body size and phylogeny, then, pat1983), and lagomorphs are no exception to this pattern. terns of life history tactics in lagomorphs are influenced
Over 37% of the variation in lagomorph reproductive greatly by breeding season length. Seasonal reproducstrategies can be explained by these two factors (Tabs 3, tion presumably evolved to maximize offspring survival
4). The influence of body size on so many life history and to minimize costs of reproduction (in terms of adult
parameters explains at least in part why these life his- survivorship) (Stephan 1982, see also Browne 1982).
tory traits coevolve (Stearns 1976), for an evolutionary Hence, environmental severity and seasonality appear
change in body size necessitates changes in a host of
288
OIKOS 43:3 (1984)
to be important forces molding reproductive strategies
in lagomorphs.
Glass, M. L. Johnson, H. Levenson and an anonymousreviewerfor providingcriticalcommentson earlierdraftsof the
manuscript.
4.3. Mammalianlife historystrategies
Nearly half of the variation in reproductive characteristics of terrestrial mammals was explained by a general
body size variable (PC1, Tab. 5). PC1 is a first-order
strategy; gestation time, neonatal body mass, and litter
size may be related to uterine capacity (Millar 1981) and
hence to adult size. Conversely, maternal investment
prior to birth (PC2) and fetal growth rate (PC3) appear
to be less tightly constrained by body size in mammals.
My primary intent in this section was to compare
lagomorph reproductive tactics to those of other orders,
but a few other generalizations seem warranted. First,
PC2 segregates Diprotodonta and Polyprotodontia
from all eutherian orders (Tab. 6, Fig. 2). This dichotomy can be explained by physiological and morphological differences in reproduction between metatherians and eutherians (Moors 1974, Luckett 1975,
Tyndale-Biscoe 1973). Among eutherians, rodents, artiodactyls, insectivores, and primates displayed the
greatest mean maternal investment, significantly
greater than mean maternal investment of carnivores
(Tab. 6, Fig. 2). Although other studies (Millar 1977,
Zeveloff and Boyce 1980) found that maternal investment by lagomorphs was low, the present analysis indicates that lagomorphs exhibit an intermediate level of
maternal investment relative to other eutherian orders
(Fig. 2).
Rate of fetal growth is a conservative mammalian
trait (Sacher and Staffeldt 1974, Millar 1977). Thus,
considerable overlap of PC3 scores among orders might
be expected (Tab. 6, Fig. 2). Nonetheless, differences
do exist, most notably among lagomorphs, rodents, and
primates. Intrauterine growth rate is positively associated with basal metabolic rate in mammals (McNab
1980); thus, it is no surprise that orders with high mean
fetal growth rates (e.g., lagomorphs, carnivores, ungulates) are also characterized by high basal metabolic
rates (McNab 1980). Ultimately, food habits may underlie differences in fetal growth rates (McNab 1980).
For instance, lagomorphs typically feed on succulent
grasses and forbs during the breeding season (Bear and
Hansen 1966, Korschgen 1980), whereas numerous species of primates subsist on leaves, a relatively low
quality food (Montgomery 1978, McNab 1980), thereby
restricting their basal rates of metabolism (and hence
fetal growth rates).
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