Download Why fly The possible benefits for lower mortality

Biological Journal of the Linnean Society (1990), 40: 53-65. With 7 figures
Why fly? The possible benefits for lower
mortality
DEREK POMEROY
Department of <oology, Makerere University, Box 7062, Kampala, Uganda
Received 28 October 1989, accepted for publication 13 June 1989
In adult endotherms-birds and mammals--mortality rates are lower in flying than non-flying
species. Rates vary with size, but allowing for this they are higher in penguins than flying birds, and
in rodents than bats. These observations are most simply explained in terms of predation since flight,
allowing movement in three dimensions, increases the chances of escape.
There are various problems in obtaining and comparing data on rates of mortality and this partly
explains a wide scattering of points. Nevertheless the main results are statistically significant, mostly
at P < O . O O l . Amongst birds, there are several other significant differences. Mortality rates are lower
at lower latitudes, and in aquatic compared to terrestrial species, with cliff-nesters having lower
rates than other aquatic birds and co-operative breeders than other terrestrial ones. No latitudinal
effect was detected in mammals. The exceptionally low rates of mortality in bats and swifts are
attributed to their being particularly hard to catch.
KEY WORDS:-Flight,
advantages -mortality rates
~
mammals - bats - birds - penguins - swifts.
CONTENTS
Introduction . .
Methods . . .
Results . . .
Discussion.
. .
Conclusions . .
Acknowledgements
. .
References
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INTRODUCTION
Flight confers such important advantages to an animal that, were it not for its
complexity, it would surely have evolved in more groups. Yet today, powered
flight is found only in insects, birds and bats.
Three important benefits of flight are suggested.
(1) In travelling from one point to another, flight requires less energy than
walking or running (Alexander, 1982; 129; Peters, 1983). It is also much faster.
This facilitates long distance movements to escape such adverse conditions as
harsh winters and droughts.
(2) Flight gives access to resources unavailable on the ground, e.g. fruit in
trees.
+
0024-4066/90/050053 13 SOS.OO/O
53
01990 The Linnean Society of London
54
D. POMEROY
(3) I t increases the chances of escaping from predators, primarily by allowing
movement in three dimensions, rather than two, but also because flight is
typically faster than running or jumping.
It is the last of these which forms the basis of this paper. Birds may have
evolved flight in the first place as a means of escaping predators. However, this
possibility (Bennett & Ruben, 1979) is disputed by Rayner (1988: 285) who
considers that having “an incipient flight adaptation might render an animal
more vulnerable” to predation. Whether or not this is so, there can be little
doubt that flight helps modern birds to escape predators, particularly non-flying
predators. I t has long been accepted that secondary loss of flight, especially in
birds living on islands, is a consequence of the absence of predators which, if
introduced by man, soon demonstrate the costs of flightlessness. Not only are
these birds unable to fly, but they also lack appropriate behavioural responses,
many being active by day and apparently fearless.
My concern here is to quantify the benefits of flight in terms of survival and
mortality, the main hypothesis being that birds have much lower mortality rates
than non-flying animals of similar size. For this purpose I shall confine the
comparison to mammals, since they are the only non-flying endotherms apart
from secondarily flightless birds. Naturally, bats are a separate category.
There are problems associated with the use of survival data (Anderson,
Burnham & White, 1985), and there have been criticisms of ‘the comparative
method’, although others defend its use (Harvey & Elgar, 1987). Nevertheless, I
propose to compare mortality rates (the complement of survival rates). I n doing
so, the following assumptions are necessary.
(1) Within a particular taxon, survival rates are correlated with body size.
There is good evidence for this, e.g. Brown & Pomeroy (1984) and O’Connor
(1981) for birds; and Calder (1983b) and Peters (1983) for both birds and
mammals. Further evidence appears in this paper.
(2) Basal metabolic rates are broadly similar for birds and mammals
(including bats) of similar body size (Bennett & Harvey, 1987; Nagy 1987;
Peters, 1983) support this view. More importantly, there is also a close
correlation between active metabolic rate and size (Bennett & Harvey, 1987).
(3) Survival rates amongst adult animals are comparatively independent of
age.
(4)Higher survival rates are a result of lower predation rates.
(5) Body mass is an adequate measure of size.
I n later sections the validity of these assumptions will receive further
consideration.
METHODS
The basis of this study is a comparison of mortality rates amongst various
groups of adult endotherms. Most of the data are derived from reviews of the
literature, supplemented by correspondence.
The literature is widely scattered. My original intention was to confine the
search to the Afrotropical and Palearctic Regions. I n the case of the Afrotropical
fauna, the search has been fairly complete. For the much greater Palearctic
literature, I obtained adequate samples without going far beyond standard
works such as Cramp (1985) and Corbett & Southern (1977). I have only
FLIGHT AND MORTALITY
55
TABLE
1 . Summary of data sources
Species included
Group"
Taxa
Geographical range
Number
of
observationsb
Range of
sizes
(8)
Afrotropical
land birds
Aquatic species excluded
Afrotropical Region
38
84400
Eurasian land
birds
Aquatic species excluded
Western Palearctic
Region
64
9-1530
Aquatic birds
Divers, shearwaters,
Western Palearctic
albatrosses, gannets,
and Indian Ocean
cormorants, oystercatchers,
plovers, waders, skuas,
gulls, auks
73
38-9600
7
4100-32 500
13-6000
Penguins
Southern Ocean
Land mammals All terrestrial species;
predominantly rodents
Western Palearctic,
Nearctic and
Afrotropical
Regions
38
Western Palearctic,
Trop Cent America'
16
Bats
All species
3.9-80
"Only flying species are included in the first three groups.
'For some species, there are several independent estimates (up to 5).
'I could find no data for the Afrotropical Region.
included data from other regions where larger sample sizes were needed, or
where there seemed to be interesting differences. There is no obvious reason why
this should introduce a bias.
Categories of data which are included in the main analyses are shown in
Table 1. 'Aquatic' birds are those which depend on aquatic habitats for major
food resources. However, only species of open habitats, such as shores and
oceans, were included.
Four types of data were excluded. These were: (a) species which are
extensively hunted by man, such as rabbits and game-birds; (b) mammals larger
than about 10 kg, which roughly corresponds to the size of the largest flying
birds; (c) data derived from records of longevity of captive animals; and (d) data
from the greatest known ages of ringed birds.
The reliability of the data varies greatly, for several reasons. Very few studies
were dealing with random samples of populations, and many samples were
small. A wide variety of methods are in use. In many cases, estimates of mortality
are simply based upon animals disappearing from the study area and, whilst
they are presumed to have died, a (usually. unknown) proportion may have
emigrated. Some estimates of mortality, especially in long-lived birds, are
exaggerated by loss of rings. Nevertheless, all the data were included, excepting
only one species of Afrotropical bat, where the quoted mortality-rate in a small
sample was three times higher than expected.
Many studies report survival rates rather than mortality rates. The two are of
course complementary when expressed as percentages; I have used mortality
rates, since they are mostly below 50% y&ar-', and consequently are less affected
when an arc sine transformation is applied (see below).
56
D. POMEROY
Where authors providing data on mortality (or survival) rates did not give the
species’ mass, this had to be obtained from a different source, b u t an attempt was
made to use data from the same or a nearby population. I n a few cases the
original data were extensive, for example on the mass of Palearctic birds. For
most species I have used single, modal values for mortality and for body mass.
Inevitably, such approximations hide various sources of variability. Some of
these are discussed by Sibly, Jones & Houston (1987) in the case of mass, whilst
Clobert et al. (1988) and Curio (1989) consider the effects of sex and phylogeny
on mortality rates.
There has been much discussion on the ways in which mortality rates of adults
vary with age, especially in birds. Recent reviews include those of Lakhani &
Newton (1983) and Sauer & Slade (1987). Calder (1984), Curio (1989),
Lakhani (1987) and Sauer & Siade (1987) all had doubts about the constancy of
adult mortality rates; indeed Calder and Curio provide some evidence for its not
being constant. O n the other hand, Coulson & Butterfield (1986), Craig &
Manson ( l979), Gibbs & Grant ( 1987) and Schnakenwinkel ( l970), working
with a wide variety of bird species, all found fairly constant rates. The data of
Fry (1980) show various patterns, but no consistent trend with age. There are
few comparable data for smaller mammals, but Thompson (1987) reported that
survival is, on average, constant with age in pipistrelle bats Pipistrellus pipistrellus.
Lakhani & Newton (1983) thought that a constant adult rate was
“biologically reasonable”, but argued against its being taken as an a priori
assumption. Calder (1984: 33) admits that “the age-dependent increase [in
mortality rates] is comparatively small and therefore difficult to observe”. Since
the empirical data remain equivocal, I shall follow Brown & Pomeroy (1984)
and Mead (1985) in making the simplest assumption, namely that of constancy,
except in old age. For this exception-senescencethere is some evidence
(Clobert et al., 1988; Coulson & Butterfield, 1986; Curio, 1989; Gibbons &
Semlitsch, 1982; Mead, 1985; Partridge, 1987). There is in any case likely to be
variations between species, and probably within species too.
The model shown in Fig. 1 allows for some increase in old age. This increase,
however, will rarely affect the data significantly, since old individuals are a tiny
fraction of the population. And whilst ‘bath tub’ models (Paranjpe & Rajarshi,
1986) could be used to fit such life-history patterns, few sets of data are adequate
to test them. In practice, departures from linearity in the mortality curve
between t, and t, (Fig. 1) would be hard to detect.
In comparing mortality rates of different species latitude as well as size should
be considered, since it has been suggested that tropical species live longer than
those from temperate zones (e.g. Deshmukh, 1986; Fry, 1980). Whilst I have not
found it practicable to consider latitude per se as a variable, the data for the
Afrotropical and Palearctic Regions are presented separately, although
sometimes combined for analysis. One group, the Palearctic-breeding aquatic
birds, contains a large proportion of migrants, many of which actually spend
more than half of the year in the tropics.
Peters (1983) derived an expected relationship between size and mortality rate
where W is
in which the rate for endotherms should be proportional to W-0.25,
the mass. I tried a series of exponents, from W-“” to W-0.40. However, there was
no clear convergence on a best fit, which varied between the different groups of
data. As an alternative, I fitted regressions of the form arc sine (yomortality rate
FLIGHT AND MORTALITY
I
I
1
0
57
+,
Age
Figure 1, The model of mortality rates in animals of different ages, as used in this paper. The rate is
assumed to be constant in adult life until age t,, when it increases as a result of senescence.
year-') on the logarithm of the mass, the latter being in grams. In four cases out
of six, this gave higher values of R2 (the coefficient of determination) than Peters'
formula, whilst in a fifth they were almost identical. I therefore adopted the arc
sine/log mass procedure, using natural logarithms.
RESULTS
Principal results are shown in Figs2-6, regression statistics in Table2 and
comparisons in Table3. Despite the wide scatter of points, four of the six
regressions are highly significant, showing the strong dependence of mortality
rates on body size. (The two non-significant ones were both small samples-7
and 16.) However, it is other variables which are of most interest here.
Estimated adult mortality rates for Afrotropical birds range from around 50%
year-' for a 10 g species, to less than 5% year-' for the largest birds (Fig. 2).
Rates for birds in southern Africa (which is within the Afrotropical Region, yet
TABLE
2. Regression analyses of annual mortality rates (after using a n a r c sine transformation of
percentages) and the natural logarithm of species' mass, in grams
Regression coefficients
Group
n
a
Afrotropical land birds
Eurasian land birds
Aquatic birds
Penguins
Land mammals
Bats
38
64
73
7
38
16
66.2
75.4
64.1
51.5
144.6
40.7
n.s.
=
not significant (P> 0.1).
b
-7.44
- 7.06
- 7.45
-4.13
- 10.51
-5.15
Coefficient of
determination
(R2)
0.437
0.484
0.495
0.412
0.337
0.120
P
< 0.001
< 0.001
< 0.001
n.s.
< 0.001
n.s.
D. POMEROY
58
0 Not tropical (e.9. S.A.)
@
Arc
Sine
%
8C
2
loo
r
Co-operative breeders
Other Afrotropical species
0 Oriental species
Neotropical species
Excluded from
regression
6C
60
x
0
3
i-
4c
a
5
2c
C
D
Mass ( 9 )
Figure 2. Reported mortality rates in adult Afrotropical land birds, together with some from other
tropical regions.
outside the tropics) are similar to those for tropical species. However, nine out of
11 co-operative breeders have mortality rates lying below the calculated
regression. All eleven species weigh between 10 and 100 g, and if we permit all
bird species in this size range to constitute a sample, we can compare their rates
with a Mann-Witney test. This shows that the median rate for co-operative
breeders (30%) is significantly less than that for other species (47%)
(U=31, P<0.05).
Also shown on Figure 2 are mortality rates for some Oriental and Neotropical
species. These are well below those for Afrotropical birds, but there are too few
for any firm conclusion to be drawn. (Note that some are also species of oceanic
TABLE
3. Analysis of covariance of the regressions in Table 2, where values of n are given. The tests
compare, firstly, values of slopes (bi) and secondly, values of intercepts (a,)
~~
Comparison of slopes
Data sets compared
All six
Afrotropical land birds with Eurasian land birds
Eurasian land birds with aquatic birds
Aquatic birds" with penguins
All land birds' with land mammals
All land birds* with bats
'Flying aquatic species.
bAfrotropical plus Eurasian.
n.s. = not significant.
F
1.838
0.055
0.093
2.783
2.633
0.249
P
ns.
n.s.
n.s.
n.s.
0.05
n.s.
Comparison of intercepts
F
P
97.84
19.09
38.18
41.13
21 1.0
48.31
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
59
FLIGHT AND MORTALITY
Mass ( 9 1
Figure 3. Reported mortality rates in adult land birds from the western Palearctic Region.
islands.) It is interesting too that some Neotropical species which are also cooperative breeders have unusually low mortality rates (Brown, 1987).
In many cases the data for Palearctic birds are based upon much larger
samples than the Afrotropical species, although there is again a wide scatter. For
non-aquatic species (Fig. 3), the most striking values are for swifts, which are far
below those of other species.
The term ‘aquatic’ is here used for birds whose typical habitats, when they are
not breeding, are open shores or oceans; data for birds of inland waters other
than ‘game’ species were insufficient and they have been omitted. Mortality
-
Cliff-nesting species
Other flying species
A Penguins
Q
40 -
20
;
*:;.\
. .
..
*
.
.‘A‘
4
B ,@a
0
10
I
I
30
100
,!I
300
. Q *
‘AN--
I
I
1000
3000
..
I
10000
1-
&
I
3000
Mass ( 9 )
Figure 4. Reported mortality rates in adult birds from open aquatic habitats. Apart from the
penguins, most are from the western Palearctic Region, with a few from the Indian Ocean. Some
burrow-nesters are included with the cliff-nesters.
60
D. POMEROY
Mass (9)
Figure 5. Reported mortality rates for adults of land (i.e. non-flying) mammals.
rates for aquatic birds are shown in Fig. 4.The cliff- and burrow-nesting species
are indicated separately. They include cormorants, auks, kittiwake Rissa
tridacQla, gannet Sula bassana and Manx shearwater Pufinus pufinus. These species
are presumed to be less vulnerable when breeding than, for example, most gulls
and waders. For this group, 19 out of the 21 data points are below the calculated
regression, a significant distribution (Sign test, P<O.Ol). Thus it seems that
adults as well as young of these species have higher survival rates.
'Data for tropical bats are confined to species from the Neotropics, but all other
data for tropical mammals are from the Afrotropical Region, whilst all
temperate data are for the Palearctic. Tropical and temperate species are shown
together in Figs 5 and 6 and are combined in the calculated regressions. But for
both land mammals and bats, the scatter of points for tropical species about the
calculated regression lines is similar to that for non-tropical species.
All six regressions are compared in Fig. 7, which reveals striking differences
between groups. Amongst mammals, the mortality rates for bats are less than a
third of those for their non-flying relatives. The lowest rates of all are for the
smaller swifts, those for other birds being rather higher than for bats but still
only about half the rates of land mammals. Palearctic land birds (a few of which
winter in the tropics) tend to have higher mortality rates than tropical species,
whilst the aquatic birds, most of which breed in high latitudes, have rates similar
to tropical land birds.
A statistical comparison of the regressions can be made by using an analysis of
covariance (Snedecor & Cochran, 1967). The null hypothesis that. there is no
difference between the slopes of the six regressions is accepted (Table 3): in other
words they can be considered as parallel. But they are significantly displaced
from each other; that is, they are at different levels. A more detailed analysis
61
FLIGHT AND MORTALITY
~
Arc
Sine
O
%
*
CJ Tropical species
40
-
30
-
20
-
Ol
I
I
I
1
3
10
30
I 0
Moss(g)
Figure 6. Reported mortality rates for adult bats.
shows, firstly, that the mortality rates of Afrotropical birds are significantly lower
than those of the Eurasian species; and secondly that the aquatic species, almost
all of which breed in the Palearctic Region, have lower mortality rates than the
Palearctic land birds.
120-
100
-
80 -
60
-
\
.
40-
-
20-
-
0
3
10
30
100
300
1000
3000
I
MOSS( g 1
Figure 7. A comparison of the regressions in Figs 2 to 6. Regression statistics are given in Table 2,
and the regressions are compared in Table 3.
62
D. POMEROY
If we exclude latitude as a factor affecting mortality in birds, the data for
tropical and temperate birds can be combined and compared with land
mammals and bats. Again the differences are highly significant (Table 3),
although in the case of the land mammals there is also a difference in slope.
DISCUSSION
The data provide strong confirmation for the relationship between mortality
rates and size (Table 2). Four other trends emerge clearly (Table 3).
( I ) Non-flying endotherms have much higher mortality rates than those which
fly.
(2) There is an overall trend in mortality rates, from high in land mammals to
low in bats and swifts.
(3) Mortality rates in tropical birds are lower than for birds of higher
latitudes.
(4)Amongst Afrotropical birds, species which breed co-operatively have lower
mortality rates.
Before considering these statements in more detail, it should be mentioned
that other factors can also affect mortality rates, although I shall not discuss
them here. They include life-history strategies, diet, phylogeny and sex (Curio,
1989; Kozlowski & Weigner, 1987; McNab, 1988).
It can be seen from Fig. 7 that mortality rates in wild birds are much lower
than those of mammals of the same size. Hence life expectancy too is much
greater in birds than mammals. Schmidt-Nielsen (1984) shows that this applies
to captive animals too, contrary to Calder’s (1983a) predictions for maximum
life spans, which suggested only small differences. Longevity in birds and
mammals has also been correlated with the ratios of brain size to body size, and
body temperature to metabolic rate (Sacher, 1978; Haukioja & Hakala, 1979).
However, here I am concerned with wild animals. There are reports of higher
‘field’ metabolic rates in rodents than birds (Nagy, 1987), but the differences are
not great; and at least in captivity, bats have slightly higher rates than rodents
(Elgar & Harvey, 1987).
Whilst it may be intuitively obvious that a bird’s ability to fly gives it a better
chance than a rodent of escaping its predators, there is a lack of direct evidence.
However, observed mortality rates decrease quite logically in proportion to the
apparent risks. Thus fossorial mammals have higher survival rates than surfaceliving mammals (e.g. French, Stoddart & Bobek, 1975), which are heavily
predated by birds (Brown, 1972). The naked mole rat, Heterocephalus glaber,
living almost entirely underground, and weighing some 50 g, has been recorded
to survive for up to 13 years! (Anon, 1986: New Scientist, 22 May: 2 5 ) . Bats, which
are usually well hidden during the day or when hibernating, also seem to have
few predators when they are active.
Amongst birds, mortality rates for penguins are significantly higher than for
other aquatic species, which spend less time in or on the water, with its varied
predators. Amongst flying species, inhabitants of open shores and oceans are
difficult prey, since almost all predators depend to some extent upon surprise.
Most data are for Palearctic species, and their mortality rates are some 10 to
15% lower than Palearctic land birds. But the most striking figures are those for
swifts. Aerial roosting is known to occur in some swifts, such as Apus apus
FLIGHT AND MORTALITY
63
(Cramp, 1985). They are 2 to 3 years old when they first breed, and may spend
most of their lives on the wing except when actually at the nest, which is for only
a few weeks a year. There are reports of swifts being taken by the sparrow hawk
Accipiter nisus (Cramp, 1985), and the fact that falcons are sometimes mobbed by
swifts suggests that they are recognized as potential predators, although there are
few recorded instances.
Fry (1980) was not able to demonstrate lower mortality rates in tropical birds
compared to temperate species, but the more extensive data presented here
provide good evidence for there being a difference. This may result from harsher
environments a t higher latitudes, or the increased costs of migration for some
species (Curio, 1989). I n any case, Figs5 and 6 do not suggest any latitudinal
difference in mortality rates in mammals, although the data are rather few and
variable. The higher mortality rates in birds from northern latitudes are reflected
in their greater reproductive effort (Ricklefs, 1980).
Fry (1980) suggested that mortality rates should be lower in co-operatively
breeding birds than in pair-bonding species. Brown & Pomeroy (1984) found
some evidence for this. Brown (1987) has reviewed the subject in detail and his
conclusion that co-operative breeders are indeed better survivors is further
supported by data in this paper. The explanation may be that by living in a
group, co-operative breeders reduce the risks of predation; and a t the same time
the energy costs of breeding are shared between more individuals and hence
reduced for each. Brown (1987) considers that it is the high survival rate of cooperative breeders which is the cause of the ‘surplus’ birds that become the
helpers.
CONCLUSIONS
Most active predators depend to some extent on an element of surprise in
catching their prey. At the same time, prey are more easily detected in open
habitats. Here I suggest that prey which can fly are more difficult to catch than
those that cannot, and the hardest of all to catch are the ones that spend the
most time in the air.
Thus amongst mammals, we find higher mortality rates in cursorial than
fossorial forms, with the lowest rates in bats which, when not in flight, are often
inaccessible.
Birds of open shores are most at risk to predators during the breeding season,
unlike those which nest in burrows or on cliffs. The main predators of the latter
are marine fish and mammals. Both groups have lower rates than land birds,
many of which are species of woodlands and forests. And amongst the aquatic
species, survival rates are highest in those that nest in the least accessible places.
It is particularly notable that swifts, with their remarkably low mortality rates,
are the most aerial of all birds.
These observations are consistent with the hypothesis that low mortality rates
are largely a result of low predation rates. Loss of flight by some island birds in
the absence of predators provides support for this. There is a clear sequence,
from rats to bats, and penguins to swifts, in which mortality rates are inversely
proportional to the risks of predation. These risks, in turn, reflect the potential
prey’s accessibility and catchability-in
particular, the proportion of its
accessible time spent on the wing.
64
D. POMEROY
Populations of endotherms are often close to their carrying capacities, which
in turn are determined by resource availability. Hence the low reproductive
output which is characteristic of species with high survival rates (Eisenberg,
1981; O’Connor, 1981; Perrins & Birkhead, 1983; Western & Ssemakula, 1982)
can best be considered as a consequence of their success in reducing predation,
especially through flight.
These conclusions do not necessarily conflict with those of Lack (1954), who
saw mortality rates as a consequence of reproductive rates. Obviously species with
high reproductive rates must, on average, have high mortality rates. But where
predation rates are lower, the evolution of lower reproductive rates becomes
possible.
ACKNOWLEDGEMENTS
Steve Albon, Peter Grant, Peter Jewell, Jan Kozlowski, David Pye and
Michael Reiss all commented on a draft of this paper. I am grateful to them, and
to many others who assisted my search for data in various ways.
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