Part 7

-----------+-------------------------------------------------------------- |Potos Procyon Nasua Nasua Bassariscus Procyon Food |flavus cancrivorus nasua narica astutus lotor -----------+-------------------------------------------------------------- Mammalia | + | # ++ ||| ++ || Aves | ++ | + || Birds' eggs| ||| Reptilia | + | + ||| # + | + | Amphibia | + | # + | Pices | ++ || ++ || Insecta |++ | + ||| ++ ||| # + || ++ || Arachnida | ++ ||| # + | + | Chilopoda | ++ ||| Diplopoda | # + | Crustacea | ++ ||| # ++ ||| Mollusca | + || # + || Annelida | # + | Nuts | ++ || Grains | ++ || Buds | + | Fruit |++ ||| ++ # || ++ ||| Leaves | + | Grass | + | -----------+--------------------------------------------------------------

FOOD HABITS OF PROCYONIDS.--Food habits of six procyonids for which metabolic data are available are presented in Table 9. All six species clearly have mixed diets. Compared to other species, Procyon lotor is highly catholic in its diet, taking food from almost twice as many categories as Nasua narica, three times as many as Procyon cancrivorus, Nasua nasua, and Bassariscus astutus, and nine times as many as Potos flavus.

For those species for which food habit data are quantified, we used Eisenberg's (1981:247-251) substrate/feeding matrix method, where "substrate" is analogous to McNab's (1986a) "behavior," to construct the following feeding categories that are based on the major food groups utilized by each species (Table 9).

1. Potos flavus: (1) arboreal/frugivore, insectivore.

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 r | (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 0.77 1.32 | 1.75 0.65 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) ---------------------+------------------------------------------------

r_{maxe} = 4.9·m^{0.2622}, where m is body mass in grams.

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; R² = 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; R² = 0.86.

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 (Müller and Kulzer, 1977; Chevillard-Hugot et al., 1980; Müller 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.