Behavioral Ecology
and Sociobiology

Behav Ecol Sociobiol (1987) 20:377-382

9 Springer-Verlag 1987

Male parental care and monogamy in snow buntings
Bruce E. Lyon*, Robert D. Montgomerie, and Linda D. Hamilton*
Department of Biology, Queen's University, Kingston, Ontario K7L 3N6,Canada
Received September 10, 1986 / Accepted February 4, 1987

Summary. We experimentally removed males froma random sample of 14 snow bunting (Plectrophenax nivalis) pairs to determine the influence ofmale parental care on reproductive success. Widowed females increased their rate of food delivery
to nestlings by increasing their feeding visit rate
but not their load size. However, Widows were
only able to achieve 73% of the food delivery rateof Control pairs and, as a result, they raised fewer
offspring of lower quality (i.e. lower mass at fledging). Total brood mass raised by Widows was only
55% of that of Control pairs. Thus, in the yearof our experiment, male parental care in the nestling period almost doubled the reproductive success realized from a brood. Our experiment, however, was done in a year of poor food availability
and data from the previous year, when food supply
was higher, indicate that males may not always
be so important. Since nestling food supply appears to be unpredictable at the time of pair formation, we suggest that monogamy is a bet-hedging
strategy in case of poor food availability. As aconsequence the importance of male parental carein some years may explain why snow buntings arealmost always monogamous.

Introduction
M o n o g a m y is the common avian mating system(exhibited by 90% of bird species; Lack 1968), in
striking contrast to all other animal taxa in whichmonogamy is exceptional (Lack 1968; Trivers
1985). Wittenberger and Tilson (1980) outlined
5 hypotheses for the evolution of monogamy, and* P r e s e n t a d d r e s s : Department of Biology, Princeton University, Princeton, NJ 08544, USAreviewed the available evidence in their support.
Although they discussed other factors that may
favour its evolution (e.g. skewed sex ratios), they
concluded that male parental care has been an important force in the evolution of monogamy inmost avian species, as suggested earlier by Lack(1968).
Although there is a correlation between monogamy and male parental care in birds, it is possiblethat male care in some species may be a consequence of monogamy, rather than a cause. For example, if some factor other than male care imposesmonogamy, then the cost of male parental carewith respect to the loss of additional matings (Trivers 1972) may be greatly reduced. Thus, the simple observation that male parental care occurs ina monogamous species does not confirm that itenhances reproductive success sufficiently to account for the evolution of monogamy. Only experimental studies can reveal whether male parental
care has an important influence on reproductive
success and, therefore, whether or not females areable to completely compensate for the loss of malecare if their mates desert them.
The few experimental studies done to date haverelied on male removals to assess the importanceof male parental care in birds, and the results havevaried. In one study, male parental care was foundto be essential for any reproductive success (Erckmann 1983), while in others, male care was notessential, but was useful in that it had a positiveeffect on reproductive success by reducing the riskof nest predation (Hannon 1984) or increasing thenumber and quality of offspring produced (Weatherhead 1979; Smith et al. 1982). Interestingly, studies of some species have found that removal ofthe male had no detectable influence on a female's
reproductive performance (Gowaty 1983 and references therein). Thus factors other than male paren- 9

378

tal care may have played a role in the evolutionof monogamy in these species. As Mock (1986)
points out, there is a need for similar experiments
on a variety of bird species living in different ecological situations.
In this study, we examine the significance ofmale parental care in the snow bunting (Plectrophenax nivalis), a monogamous finch that breeds
in the high arctic. We first compare the relative
effort devoted to raising offspring by male andfemale buntings in a natural situation by examining nestling feeding rates and load sizes brought
in by each sex. We then present the results of aremoval experiment designed to reveal the influence of male parental care on reproductive successand we discuss the potential effects of year-to-year
variation in food supply on monogamy in general.
Methods
Animals and study area
We studied parental care in snow buntings at Sarcpa Lake
(68~ ' N, 83~
on the Melville Peninsula of Canada's
Northwest Territories in 1982 and 1983. Buntings are normallymonogamous at Sarcpa Lake, but as in other areas (Tinbergen1939), some males (up to 5% of the population) are polygynous
in some years, almost certainly as a consequence of a slightfemale bias in the sex ratio (Lyon and Montgomerie 1987).
As a result of the short snow-free season, breeding is highly
synchronous with all pairs beginning egg laying within the same
2-week period each year (Lyon and Montgomerie 1987). Bothsexes provide parental care throughout the nesting cycle; females incubate the eggs and brood young chicks, males feed
females during incubation (Lyon and Montgomerie 1985) andboth sexes feed the chicks until independence. Thus, given thehigh degree of nesting synchrony, a male mated to two females
would be forced to feed nestlings at both nests. We have described the general breeding biology of this species at Sarcpa
Lake elsewhere (Montgomerie et al. 1983; Lyon and Montgomerie 1985).

Experimental removals
In 1983 we created 14 Widow females by removing their mateseither at the onset of incubation ( n = 7) or at hatch (n = 7).
In an earlier analysis of these data, we found no differences
between these 2 sets of Widows in any post-hatch indices ofreproductive success (see Table 2 in Lyon and Montgomerie1985) so the data are pooled for analysis here. Widows werechosen randomly from the study population in 1983, leaving
11 Control nests for comparison. Widows and Controls did
not differ in either clutch size (Mann-Whitney U=68.5, P =0.63, n = 1 4 , 11) or date of clutch completion (Median test,
Z~ = 0.62, P = 0.44, n = 14, 11). For some of the variables measured in this study, our sample size was lower than the total
number of birds in the Widow and Control groups becauseof either predation or inaccessibility of the offspring for measurement.

Food delivery rates
In both 1982 and 1983, almost all nests were found before
clutch completion and most nests were monitored every second

day through to fledging. To quantify male and female parental
care, we observed nests for 1-h observation periods to document
both the rate of feeding visits to the nest and the amount offood delivered by each sex. Each nest was watched for at least
three 1-h sessions on different days during the nestling period.
We observed males and females at 4 Control nests in 1982,
and at 5 Control and 11 Widow nests in 1983.
To quantify the load sizes brought to nestlings, we assigned
loads to 3 size categories relative to the number of craneflies
carried: small = 1, medium = 2 or 3, and large-- 4 or more craneflies. The diet of nestling buntings at Sarcpa Lake was comprised almost entirely of craneflies (Tipulidae). For all but
3 parents, we observed at least 3 loads; for the others we observed only 2 loads (n = 1) or 1 load (n = 2). We used the product of feeding visit rate and our load size index as an estimateof the overall rate of food delivery for each parent studied.
For analysis of both load sizes and feeding rates we used themean values for each individual to avoid potential problems
with pseudoreplication (Hurlbert 1984).

Reproductive success
We used several indices of reproductive success to examine theconsequences of male parental care; number of chicks fledged,
absolute growth rate (g/d), fledging mass (g), brood mass (g),length of nestling period (d). Chicks were weighed every second
day to the nearest 0.1 g on a Pesola spring balance. F r o m thesedata we calculated the absolute growth rate (KA/4) of eachchick that survived to fledging. KA/4 is not nearly as sensitive
to a variable asymptote (A) as the relative growth index, K(Hussell 1972; see Lyon and Montgomerie (1985) for details
on our calculations of absolute growth rate). The length of
the nestling period is the time from the hatching of the firstegg to the fledging of the first chick in each nest. Because nests
were sometimes visited every other day, there could have been
as much as 48 h error in the calculation of nestling period for
an individual nestling. To minimize this error in analysis, weused the average of the minimum and maximum estimate ofnestling periods for each nest.
For analysis we used the mean chick growth rate for eachnest. We have shown elsewhere that there was a significant
effect of ' n e s t ' on offspring growth in snow buntings (Lyonand Montgomerie 1985). Thus the growth rates of young withina nest were not independent.
We also weighed as many of the adult females as possible
just prior to fiedging to determine whether loss of male careaffected their condition. Because Widows were selected at random, we assume that there was no difference in the body mass(or condition) of Widows and Controls at the start of incubation in 1983.
For statistical comparisons between Widows and Controls,
we used one-tailed tests. Because we expected Widows to try
to compensate for the loss of their mates, we predicted that
their rates of food delivery would be higher than those of Control females but lower than those of Control pairs. We also
expected a decline in the condition of Widows, a reduction
in b o t h the number and quality (growth rate and fledging mass)of their chicks, and a lengthening of their nestling period.

Food availability
As part of a longer term study, we have monitored the insect
food available to birds for 5 years (1981-1985) at this study
site. To sample insects, we used 0.1 m x 1.0 m boards coveredby plastic sheets coated with a sticky resin (Tanglefoot| seealso Hussell 1972). We used 8 such boards in 1981 and 20
boards in the subsequent 4 years. In each year we placed boards
in all of the habitats visited by foraging finches. Craneflies379
Table 1. Feeding visit rates (feeds/h), load sizes (food units),
and food delivery rates (food units/h) of male and female buntings feeding nestlings. Load sizes are expressed as food units
where 1 = small, 2 = medium, and 3 = large loads (see Methods)

FemaleMale

Comparison"

Mean Range

Mean Range

z

P

6.6

5.1-7.1

1.46

0.14

1.7-2.1
2.2 2.0-2.4
9.8-19.5 14.4 11.8-16.8

1.83
0.73

0.06
0.47

4.5

3.3-6.0

4.6

3.0-7.0

0.00

0.30

1.9
9.0

1.0-2.4
2.7
4.0-14.6 13.2

2.2-3.0
9.0-18.6

2.02
0.94

0.04
0.35

1982 (n = 4 pairs)
Feeding visit
8.5
rate
Load size
1.9
Food delivery 15.7
rate

5.8-10.9

1983 (n : 5 pairs)
Feeding visit
rate
Load size
Food delivery
rate

a Wilcoxon matched-pairs signed ranks tests (2-tailed)captured on the boards were counted every 4 d, at which point
the resin-covered plastic was replaced.

or 1983 (Table 1). Males, however, brought inlarger loads than females but this did not resultin significantly higher food delivery rates in either
year or for both years combined (Table 1). Thus
paired males and females delivered approximately
equal amounts of food to their nestlings. Overall,
females that had male help delivered 48% of thefood taken to their nestlings.
Widows, on the other hand, significantly increased their feeding visit rate above that of Control females (1983 data), although they did notchange the size of loads brought to the nest (Table 2). As a result of the increase in feeding visit
rate by Widows, they delivered more food to thenest than Control females but still significantly lessthan Control pairs (Table 2). Thus, although Widows increased their feeding visit rate from 49%(i.e. Control female rate) to 77% of the rate ofControl pairs, this resulted in an increase in actual
food delivery rate to only 62% of that of pairs(Table 2). This increase in effort by Widows apparently did not affect their overall condition as Widow and Control females did not differ in bodymass at the end of the nestling period (Table 2).

Results

Reproductive success
Parental effort
The feeding visit rates of males and females at Control nests did not differ significantly in either 1982

The loss of male parental care had a striking effecton both the quantity and quality of offspring
fledged. Widows fledged an average of 2.7 chicks

Table 2. Indices of parental effort, female condition and reproductive success for Widow and Control buntings during the nestling
period. For analyses of feeding rates and load sizes, we used mean values for each individual; for growth rates and fledging
masses, we used the mean value per nest. Total feeds per hour is the pooled feeding rate of males and females at Control
nests

WidowsControls

Comparison"

Mean

Range

n

Mean

Range

n

U

P

7.1
7.1
1.8

4.3-11.8
4.3-11.8
1.3-2,3

11
11
10

4.5
9.2
1.9

3.3-6.0
6.7-10.6
1.0-2.4

5
5
5

6.5
13.0
18.0

0.008
0.05
0.20

13.3
13.3

5.9-21.3
5.9-21.3

9
9

9.0
21.3

4.0-14.6
15.6-26.8

5
5

12.0
4.0

0.04
0.01

32.1

29.6-35.2

7

32.2

29.7-34.6

5

15.0

0.38

3.9
24.9
75.1
12.6

2.3-5,920.8-29.7
43.5-148.5
10.5-14.2

11
11
11
7

4.4
30.4
135.4
12.4

3.1-5.7
22.6-35.2
90.5-181.3
11.0-13.7

9
9
9
8

35.0
8.0
8.0
24.0

0.19
0.001
0.001
0.35

Parental effort
Feeds/h (females only)
Feeds/h (total)
Load size
Food delivery rate:
females only
total
Female condition
Female mass (g)Reproductive success
Growth rate (g/d)
Fledging mass (g)Brood mass (g)Nestling period (d)Mann-Whitney U-tests (one-tailed)380
Laying}ontrol
oo
+-,
o9

2

60

"0

t-

On

O

Nestling

84

5O

40

o
30

rb

9

2

~/idow

E
Z

9
c

o

4

I .....

0

i

i

i

2

i

i

i

4

i

6

I

8

Number of chicks fledged
Fig. 1. The number of chicks fledgedby 13 Widowfemalesand
11 Control pairs in 1983

per nest versus 4.5 chicks per nest fledged by Control pairs (Fig. 1) and this difference is highly significant (Mann-Whitney U=17.5, P<0.002, n =13, l 1). Since there was no difference in the clutch
sizes laid by Widows and Controls (see Methods),
this difference must have been the result of brood
reduction due to the nestling starvation that we
observed. In addition, the mean fledging mass ofchicks from Widow nests was only 82% of thatof chicks fledged by Control pairs. As a result,
the total brood mass fledged by Widows was, on
average, only 56% of that of Controls (Table 2).
Growth rates of Widow chicks were also lower
than those of Controls, but not significantly so,and the 2 groups of females did not differ innestling period (Table 2).

Food availability and clutch size
If females adjust clutch size to food availability
during the nestling period, then male parental careshould always be useful (Lack 1968). However, if
clutch size is determined by factors other than thefood supply for nestlings then male parental care
may have little effect on reproductive success inyears of abundant food. By chance, our male removal experiments were done in the year with thelowest availability of craneflies during the 5 years
that we have been monitoring food supply. As an
index of the availability of food for nestlings, we
calculated the average number of craneflies captured per sticky board for the 4 sampling days during the nestling period each year (Fig. 2). During
these 5 years, this index of cranefly availability varied 30-fold from a low in 1983 to a high in 1982

2O

10

r-

r

14

22

,

i

i

i

i

30

8

16

24

June

,

July

Fig. 2. Seasonal abundance of craneflies on the study area for
5 consecutiveyears. Plotted are the mean number of craneflies
captured per sticky board during the previous 4-day period.
Eight boards were sampledin 1981 and 20 boards were sampled
in the other 4 years. The egg-laying and nestling periods of
63 nests found over the 5 years of this study are indicated one outlyingnest was removed from each end of this distribution(Fig. 2). The difference between 1982 and 1983 inavailability of food for nestlings is reflected in boththe total (male plus female) feeding visit and fooddelivery rates of pairs (Table 1). Both total feeding
visit rate (15.1 vs 9.2 feeds/h; J982 vs 1983) andtotal food delivery rate (30.1 vs 21.3 food units/h;
1982 vs 1983) were significantly higher in 1982
(P<0.05, Mann Whitney U-tests), the year of
more abundant food.
Despite this year-to-year variation in the foodsupply, there was no correlation between the average annual clutch size and the index of cranefly
availability in the same year (Spearman rank rs =0.100, n = 5, P = 0.63). We conclude, therefore, thatfemales do not appear to be able to adjust clutch
size to the availability of food for nestlings.
Discussion

Importance of male parental care
It is clear from our results that male snow buntings
are useful in that they enhance female reproductive
success but they are not essential for the rearing
of at least some offspring, even in a year of poor
food availability. Widows were able to fledge only
about 60% of the number of young raised by pairs(Fig. 1) and these young had, on average, a significantly lower mass at fledging (Table 2), suggestingthat they were in poorer condition. The average

381

mass of entire broods raised by Widows was only
slightly more than half of that fledged by Control
pairs. If we use brood mass as an index of boththe quality and quantity of offspring produced,
then male parental care effectively doubled the reproductive success realized from a brood.
It is interesting that widowed females were able
to compensate somewhat for the loss of theirmates, especially since they suffered no decline inbody condition as a result of their increase in feeding visit rates (Table 2). This suggests that whenboth members of the pair were present, females(and probably males, too) did not work at theirmaximum capacity. The ability of widows to increase their food delivery rate is particularly surprising in a year of poor food availability and indicates that pairs are capable of raising more offspring than they do. It is unlikely that the compensation was achieved at the expense of brooding,since the chicks are normally only brooded for the
first two to three days.
Moreover, clutch sizes at our study area were
not correlated with overall nestling food supply
and may instead have been determined by foodconditions at or before the time of egg laying.
Thus, in many years the number of eggs laid ina clutch may be somewhat lower than the maximum number of nestlings that the parents could
successfully raise. Hussell (1972), for example,
found that snow bunting pairs could successfullyraise broods experimentally enlarged to 7 or 8
chicks.

Monogamy in snow buntings
Wittenberger and Tilson (1980) suggested that,even when males are not essential for the raisingof some offspring, male parental care may still favour monogamy when a female that mates withan unmated male realizes a higher reproductive
success than she would have if she had mated withan already-mated male. In snow buntings, bigamy
is too rare to permit a comparison of bigamousand monogamous pairs but we can use the resultsof our removal experiments to assess the consequences of polygyny for female reproductive success. If we assume that males and females eachcontributed 50% of the effort required to raise abrood (Table 1), and were working at their maximum capacity, then a secondary female would realize, at best, only about 75% of the reproductive
success of a monogamous female (assuming thatthe male divides his time equally between the 2broods). Thus, to achieve the same reproductive
success as a monogamous female, a secondary fe-

male would have to contribute about 75% of theeffort required to raise a brood. Even when working at their presumed maximum capacity, widows
were able to bring their nestlings only about 62%of the food delivered by monogamous pairs. We
conclude, therefore, that females, on average, benefitted from monogamy in the year of our experiments.

Monogamy in variable environments
Despite the theoretical importance of male parental care to the evolution and maintenance of monogamy (Wittenberger and Tilson 1980), few experimental studies of altricial birds have assessed theability of females to raise young alone after maleremoval. Even in these few studies the apparent
importance of male parental care has varied. For
example, two different studies of European tits
(Parus spp.) found that widows raised significantly
fewer and lighter chicks than monogamous pairs(Bjorklund and Westman 1986; Sasvari 1986). In
experimental studies of both song sparrows (Melospiza melodia; Smith et al. 1982) and savannah
sparrows (Passerculus sandwichensis ; Weatherhead1979), on the other hand, lone females raised only
46% and 82%, respectively, of the number of offspring raised by females that had male help, butneither of these differences was significant. Gowaty(1983) found that widowed bluebird (Sialia sialis)
females actually raised more fledglings than did
pairs, although this difference, too, was not significant.
There are 3 possible reasons for the inconsistency of results among these various experimental
studies. First, there may simply be variation among
species in the importance of male parental careand thus monogamy may be favoured for someother reason (see Wittenberger and Tilson 1980).
Second, even though the results of Weatherhead(1979) and Smith etal. (1982) were suggestive,
large variances in fledging success coupled withsmall absolute differences between their control
and experimental groups may have obscured potentially significant effects. Thus, male parental
care may often be important in monogamous birds
but just difficult to document with relatively small
samples. Third, the importance of male parental
care may vary from year-to-year but, because of
unpredictability of food supplies, monogamy may
be the best long-term strategy that maximizes lifetime fitness. This explanation has not previously
been proposed but it has important implications
for the conclusions that can be drawn from short-382

term studies on the adaptive significance of maleparental care and its influence on mating systems.
Five of these six studies (including ours) weredone in a single year and the other study (Sasvari1986) was done in 4 different years but the data
were all pooled for analysis. Thus, it is impossible
to assess the effects of year-to-year variation infood supply on the role of male parents. Our experiments, however, were done in a year when nestling
food supply was extremely low (Fig. 2). It is therefore not surprising that our removals revealed thatmales were very important to female reproductive
success. Given the small year-to-year variation in
clutch size, it is possible that, in years of abundantfood, females alone could easily provide enoughfood for their offspring and polygyny would not
be disadvantageous to them. Why, then, are snow
buntings almost always monogamous even whenfood supply is apparently abundant?
In a variable environment like this, we mightalso expect females to maximize clutch size withrespect to nestling food supply such that full maleparental care would always be useful. In our study,
however, year-to-year variation in snow bunting
clutch size did not track the variation in food supply, suggesting that the food availability during
the nestling period was not predictable at the timeof laying.
Since nestling food supply does not appear tobe predictable at the time of pair formation in midJune (see Fig. 2), we suggest that monogamy islargely a bet-hedging strategy due to the potential
importance of male parental care. Such a strategy
may also explain the failure of some short-term
studies of monogamous birds (e.g. Gowaty 1983)
to find any apparent value to male parental care.
Thus short-term studies cannot be used to reject
the hypothesis that male parental care sometimes
enhances female reproductive success. In an unpredictable and fluctuating environment, selection will
favour the mating system that yields the highest
lifetime fitness, even when that mating system does
not seem to be adaptive in some years. As a result,
the real influence of male parental care on the evolution of monogamy can only be assessed by examining the adaptive value of monogamy during theentire lifetime of individuals.
Acknowledgements. This research was funded by a grant fromthe Canadian Wildlife Service (to BEL), a Northern Scientific
Training Grant from the Department of Indian and Northern

Affairs, Canada and both an operating and equipment grantfrom the Natural Sciences and Engineering Research Councilof Canada (to RDM). The Eastern Arctic Scientific Resource
Center at Igloolik, N.W.T. provided logistic support for ourstudies at Sarcpa Lake. Rob McLaughlin initiated the census
of craneflies and collected most of the insect data for 1981
and 1982. This work has benefitted from discussions with Dov
Lank and Rob McLaughlin and by comments from Pat Weatherhead on the manuscript.

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