2. _Procyon cancrivorus:_ (1) semiaquatic/crustacivore,
molluscivore, insectivore, piscivore, carnivore.
3. _Nasua nasua:_ (1) terrestrial/insectivore, arachnidivore,
carnivore, frugivore.
4. _Bassariscus astutus:_ (1) terrestrial/carnivore, insectivore,
frugivore.
5. _Procyon lotor:_ (1) terrestrial/carnivore, granivore,
frugivore, insectivore; and (2) semiaquatic/crustacivore,
molluscivore, insectivore, piscivore, carnivore.
FOOD HABITS AND BASAL METABOLISM.--The most important foods in the
diet of _Procyon lotor_ are vertebrates, nuts, seeds, and fruits
(Table 9). These are the same foods that are eaten by those dietary
specialists that have [.H]_{b}'s equivalent to, or higher than, values
predicted for them by the Kleiber equation (McNab, 1986a). The most
important foods in the diets of _Potos flavus_, _Procyon cancrivorus_,
and _Nasua nasua_ are invertebrates and fruit (Table 9), and these
foods are eaten by dietary specialists that have lower than predicted
[.H]_{b}'s (McNab, 1986a). Major foods in the diet of _Bassariscus
astutus_ are terrestrial vertebrates, insects, and fruit (Table 9).
Dietary specialists that eat terrestrial vertebrates have higher than
predicted [.H]_{b}'s, whereas those that feed on insects have [.H]_{b}'s
that are lower than predicted (McNab, 1986a). Year-round utilization of
vertebrates by _Bassariscus astutus_ suggests that it also should have
a metabolic rate that is equivalent to or higher than predicted, rather
than lower (McNab, 1986a). However, perhaps year-round inclusion of
insects in its diet (Martin et al., 1951; Taylor, 1954; Wood, 1954;
Toweill and Teer, 1977; Trapp, 1978), plus water- and energy-conserving
advantages of a low metabolic rate, each exert a stronger selective
influence on [.H]_{b} than do vertebrates in its diet.
SUMMARY.--The basal metabolic rate of these procyonids does appear to
be influenced by diet. But, it is apparent from this family's
evolutionary history and tropical origins that climate also has had a
profound influence on its member's metabolism. The history of the
family and the data presented here (Table 7) suggest that lower than
predicted [.H]_{b} is a feature that evolved very early as the primary
metabolic adjustment to a tropical climate. From this perspective, it
could be argued that climate would have been the major selective force
determining [.H]_{b}, whereas food habits would have had a secondary
influence.
_Basal Metabolism and Intrinsic Rate of Natural Increase_
BACKGROUND.--McNab (1980a) suggested that if food is not restricted
during an animal's reproductive period, the factor that will limit
growth and reproduction will be the rate at which energy can be used
in growth and development. Under these conditions, an increase in
[.H]_{b} would actually increase r_{max} because it would provide a
higher rate of biosynthesis, a faster growth rate, and a shorter
generation time. Hennemann (1983) tested McNab's (1980a) premise and
found a significant correlation between r_{max} and metabolic rate,
independent of body size, for 44 mammal species. A low correlation
coefficient for this relationship, however, indicated to him
(Hennemann, 1983) that factors such as (1) food supply, (2) thermal
characteristics of the environment, and (3) brain size also contribute
toward shaping a species' reproductive potential, particularly when
these factors strongly influence rates of biosynthesis or growth or
for some reason alter generation time. Results of our estimates of
r_{max} for procyonids are presented in Table 10.
_Procyon lotor._--This species had the highest [.H]_{b} and D_{d}, and
also had the highest r_{max} (1.34; Table 10). Such a high r_{max} may
infer that this trait evolved under conditions where food and
temperature were not limiting to reproduction. Under these conditions
selection could have favored those reproductive characteristics
sensitive to a higher [.H]_{b} (biosynthesis, growth, and generation
time; McNab, 1980a). _Procyon lotor_'s high reproductive potential is
due to its early age of first female reproduction and its large litter
size, characteristics that may reflect metabolically driven increases
in both biosynthesis and growth.
_Bassariscus astutus._--This species has a low [.H]_{b} but an r_{max}
that was 124% of expected (Table 10). This suggests that r_{max}
evolved under conditions where food and temperature were not
limiting to reproduction. Reduced litter size should restrict this
species' reproductive potential and may be a reflection of its low
[.H]_{b}. The factor that is responsible for increasing its
reproductive potential, however, is its early age of first female
reproduction. _Bassariscus astutus_ is the smallest of these
procyonids, and even though it has a low [.H]_{b}, its small mass
may contribute to its ability to reach adult size and sexual maturity
in its first year. The high quality of its diet (a high proportion of
small vertebrates; Table 9) also may be a factor that is permissive to
early female reproduction. Thus, small body size and diet may be
factors that have allowed this species to evolve a higher than expected
reproductive potential in spite of its low [.H]_{b}.
_Nasua narica._--This species is one of the largest procyonids
(Table 7), and it possesses characteristics that should limit its
reproductive potential: lower than predicted [.H]_{b} (Table 7), a
relatively low-quality diet (Kaufmann, 1962:182-198; Table 9), and
delayed time of first reproduction (Table 10). In spite of this,
_Nasua narica_ has a higher than expected r_{max} (111% of predicted;
Table 10). The life history feature that enhances _Nasua narica_'s
reproductive potential, and increases r_{max} beyond expected, is its
large litter size. In this species females live in bands. Each year
just before their young are born these bands break up, and each female
seeks out a den for herself and her litter. Once the young are able to
leave the den (approximately five weeks), bands reform. In this
situation, females not only care for their own young but also for those
of other females in the band (Kaufmann, 1962:157-159, 1982, 1987;
Russell, 1983). This social structure may contribute to this species'
ability to produce large litters and in this way increase its
reproductive potential.
TABLE 10.--Intrinsic rate of natural increase (r_{max}) of several
procyonids. (a = potential age of females producing first young;
b = potential annual birth rate of female young (= average litter
size/2; average litter size was calculated from the published range
of litter sizes for each species); n = potential age of females
producing their final young; r_{maxe} = intrinsic rate of natural
increase expected from body mass (Hennemann, 1983); r_{maxr} = ratio
of calculated to expected intrinsic rate of natural increase
(r_{max}/r_{maxe}).)
---------------------+------------------------------------------------
|
Species |Body mass a b n r r [a] r [b]
| (g) max maxe maxr
---------------------+------------------------------------------------
_Procyon lotor_ | 4940 0.83 2.25 16 1.34 0.53 2.52
|
|
|
_Bassariscus astutus_| 900 0.83 1.50 14 1.02 0.82 1.24
|
|
|
_Nasua narica_ | 3900 2.50 2.25 14 0.62 0.56 1.11
|
_Nasua nasua_ | 3850
_Procyon cancrivorus_| 1160 0.83 1.50 15 1.02[c] 0.77 1.32
| 1.75 0.65[c] 0.84
_Potos flavus_ | 2490 1.75 0.50 12 0.30 0.63 0.48
|
_Bassaricyon gabbii_ | 1600 1.75 0.50 15 0.32 0.71 0.45
|
---------------------+------------------------------------------------
---------------------+------------------------------------------------
|
Species | References
---------------------+------------------------------------------------
_Procyon lotor_ | Dunn and Chapman (1983); Eisenberg (1981:489);
| Kaufmann (1987); Lotze and Anderson (1979);
| Nowak and Paradiso (1983:981); Sanderson
| (1987); Stains (1956:28-31); This study
_Bassariscus astutus_| Kaufmann (1982, 1987); Nowak and Paradiso
| (1983:979, 980); Poglayen-Neuwall and
| Poglayen-Neuwall (1980); Poglayen-Neuwall
| and Toweill (1988); Russell (1983)
_Nasua narica_ | Kaufmann (1982, 1987); Nowak and Paradiso
| (1983:983); Sanderson (1983)
_Nasua nasua_ | Chevillard-Hugot et al. (1980)
_Procyon cancrivorus_| Crandall (1964:312); Poglayen-Neuwall (1987)
|
_Potos flavus_ | Ford and Hoffmann (1988); Nowak and Paradiso
| (1983:984)
_Bassaricyon gabbii_ | Eisenberg (1981:489); Nowak and Paradiso
| (1983:985)
---------------------+------------------------------------------------
[a] r_{maxe} = 4.9.m^{0.2622}, where m is body mass in grams.
[b] Regression of r_{max} on body mass (m). Assume r_{max} = 1.02 for
_Procyon cancrivorus_: r_{max} = 0.00005.m + 0.623; R = 0.19;
R squared = 0.03; Regression of r_{maxr} (Table 10) on H_{br} (Table 7);
assume _Nasua nasua_ has the same r_{maxr} as _Nasua narica_:
r_{maxr} = 3.35.H_{br} - 1.11; R = 0.93; R squared = 0.86.
[c] Estimate based on females reproducing in their first (a = 0.83) or
second (a = 1.75) year.
_Nasua nasua._--Unfortunately, there is not enough reproductive data
to allow calculation of r_{max} for _Nasua nasua_ (Table 10), therefore,
it is not possible to compare the reproductive potential of this South
American coati with its North American relative, _Nasua narica_. Given
its low [.H]_{b} and relatively low-quality diet of fruit and
terrestrial invertebrates (Table 9), however, r_{max} of _Nasua nasua_
may be very similar to that of _Nasua narica_.
_Procyon cancrivorus._--The age of first female reproduction for
_Procyon cancrivorus_ has not been reported. However, if one assumes
females can reproduce in their first year, r_{max} for _Procyon
cancrivorus_ would be 1.02 (132% of expected; Table 10). If, on the
other hand, first female reproduction is delayed until the second year,
r_{max} would be 0.65 (84% of predicted; Table 10). _Procyon
cancrivorus_ has a low [.H]_{b}, reduced litter size, and small body
mass. Its low [.H]_{b} may limit litter size, but as with _Bassariscus
astutus_, the quality of its diet (a high percentage of small
vertebrates; Table 9) and its small body size may make it possible for
females to reproduce in their first year and thus increase the species'
reproductive potential. This reasoning would argue that _Procyon
cancrivorus_ probably enjoys higher, rather than lower, than expected
r_{max}.
_Potos flavus._--In addition to a low [.H]_{b}, this species possesses
other characteristics that limit its reproductive potential:
low-quality diet, delayed reproduction, and birth of a single young
each year. Because there does not appear to be any other feature of
its life history that can counteract the influence of these factors,
r_{max} in _Potos flavus_ has evolved to be only 48% of expected
(0.30; Table 10). Its close relative, the olingo, _Bassaricyon gabbii_,
appears to share the same condition (Table 10).
SUMMARY.--This brief survey illustrates that, with the exception of
_Potos flavus_, procyonids tend to have values of r_{max} that are
higher than those predicted for them on the basis of mass (Table 10).
Regression analysis indicates that, within the family, body mass
accounts for only a small amount (3%) of the variation in r_{max},
whereas the positive slope of the correlation between r_{maxr} and
H_{br} (R = 0.93) suggests that low metabolism has a limiting effect
on r_{max} (see Table 10, footnote f). The implication here is that
low [.H]_{b} would be associated with a lower rate of biosynthesis,
a slower growth rate, and a longer generation time. Procyonids with
low [.H]_{b} but higher than expected r_{max} must possess other
traits that serve to offset the effects of low metabolism. Our survey
indicates that the following features compensate for low [.H]_{b} and
help increase r_{max}: (1) a high-quality diet may make biosynthesis
and growth more efficient, thus optimizing the time element associated
with each of these processes; (2) larger litter sizes and cooperation
in care of the young may increase survivorship in spite of a slower
growth rate; and (3) an early age of first reproduction, a long
reproductive life span, and moderate-size litters (two to four young)
may in the long run add as many individuals to the population as a
shortened generation time. Our survey also suggests that, at the other
extreme, factors such as a low-quality diet, reduced litter size,
absence of cooperative care of the young, delayed age of first
reproduction, and shortened reproductive life span all serve to
decrease r_{max}. Thus, it is obvious that diet, litter size, social
structure, reproductive strategy, and reproductive life span can operate
synergistically with [.H]_{b} to magnify its influence on r_{max} (as
with _Procyon lotor_ and _Potos flavus_), or they can function in
opposition to [.H]_{b} to change the direction of its influence on
r_{max} (as with _Bassariscus astutus_, _Procyon cancrivorus_, _Nasua
narica_, and perhaps _Nasua nasua_).
_Basal Metabolism and Climatic Distribution_
_Procyon lotor._--The evolution of a higher [.H]_{b} (Tables 7, 8) may
have been the physiological cornerstone that enabled _Procyon lotor_
to break out of the mold being exploited by other procyonids and to
generalize its use of habitats and climates. Once this basic
physiological change was in place, selection for appropriate
alterations in thermal conductance, capacity for evaporative cooling,
diversity of diet, and energy storage would have provided this species
with the suite of adaptations needed to extend its distribution into
other habitats and climates. Support for this concept follows from the
fact that high levels of [.H]_{b} are associated with (1) cold-hardiness
in mammals that live in cold-temperate and arctic climates (Scholander
et al., 1950c; Irving et al., 1955; Irving, 1972:115, 116; Shield, 1972;
Vogel, 1980; Golightly and Ohmart, 1983); (2) the ability to utilize a
wide variety of food resources and to occupy a large number of different
environments and habitats (McNab, 1980a); and (3) a high intrinsic rate
of natural increase (McNab, 1980a; Hennemann, 1983; Lillegraven et al.,
1987; Nicoll and Thompson, 1987; Thompson, 1987).
OTHER PROCYONIDS.--Other procyonids (_Potos flavus_, _Procyon
cancrivorus_, _Nasua narica_, and _Nasua nasua_) have lower than
predicted [.H]_{b}'s (Table 7), a characteristic that is considered to
be an energy-saving adaptation for those that live in relatively stable
tropical and subtropical habitats (Mueller and Kulzer, 1977;
Chevillard-Hugot et al., 1980; Mueller and Rost, 1983). However,
_Bassariscus astutus_ is found in tropical, subtropical, and temperate
climates. This species is found from tropical Mexico to temperate
regions of the western United States (Kaufmann, 1982, 1987; Nowak and
Paradiso, 1983:979). In the northern part of its distribution,
_Bassariscus astutus_ lives in habitats that are unstable (arid
regions), that are low in productivity, and that characteristically
have marked seasonal changes in temperature. Its lower than predicted
[.H]_{b} could be an important water-conserving adaptation at times when
temperatures are high (McNab and Morrison, 1963; McNab, 1966; MacMillen
and Lee, 1970; Noll-Banholzer, 1979) and an important energy-conserving
mechanism when cold weather may limit food availability and hunting time
(Scholander et al., 1950c; Wang et al., 1973). As will be seen later,
_Bassariscus astutus_ is unique among procyonids with lower than
predicted [.H]_{b}'s in that it also has a lower than predicted
C_{mw} (Table 7). This allows it to use less energy than expected for
thermoregulation at low temperatures. Another species with a similar set
of adaptations (lower than predicted [.H]_{b} and C_{mw}) is the arctic
hare, _Lepus arcticus_ (Wang et al., 1973), which lives in one of
the coldest and least-productive regions on earth. Wang et al. (1973)
suggest that this combination of adaptations allows _Lepus arcticus_
to better match its energy requirements to the low productivity of its
environment. A similar relationship may hold for _Bassariscus astutus_,
particularly in colder arid portions of its distribution, and may be the
reason that it, but not other procyonids with low [.H]_{b}'s, has been
able to inhabit temperate climates.