Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 CHAPTER 13 Interspecific Interactions ■ INTRODUCTION Because organisms depend on each other for food and other biotic factors, they inevitably interact with each other. Although the most intense relationships exist between mem- bers of the same species, individuals do not live apart from members of other species. Living in close association, dif- ferent species may compete for a shared resource such as food, space, or moisture. These interactions can be classified into several categories: competition, symbiosis (commensal- ism, mutualism, parasitism), predation, and human interac- tions. In competition, both species are affected adversely; in commensalism, one species benefits and the other is unaf- fected; in mutualism, species benefit each other; in parasitism and predation, one species benefits and the other is harmed. Human interactions may benefit both species, only one species, or possibly, either species. ■ COMPETITION The concept of interspecific competition is one of the corner- stones of evolutionary ecology. Darwin based his idea of nat- ural selection on competition, the struggle to survive. Whenever different species occupy the same place at the same time, there will likely be competition for common resources such as food, water, or space that are in limited supply. Such interspecific competition consumes both time and energy. Stress caused by such competition may decrease growth and birth rates and/or increase the death rate; if intense, competition can slow or even halt population growth and cause the population to decline. If ecological require- ments of two species are similar but not identical, selection pressure will tend to cause the species to diverge from each other through morphological, physiological, and/or behav- ioral specializations. However, if two species have identical ecological requirements, they will not be able to coexist because of competition for limited resources. Competition is difficult to study and demonstrate in nature because it is such an ephemeral phenomenon. The fundamental role of an organism in the community is its niche (Elton, 1927). The niche is the occupational sta- tus of the species in the community—what it does and its relation to its food, its competitors, and its enemies. It is an abstract concept that has not yet been defined and fully mea- sured. A niche should not be confused with a habitat, the physical place where an organism lives. The niche is partially defined by characteristics of the habitat, but also by what the organism eats; how, when, and where it finds and captures its food; the time of the year and time of the day when it is most active; the optimal and extreme climatic factors (heat and cold, sun and shade, wet and dry) it can withstand; its parasites and predators; where, how, and when it reproduces; and so forth. Every aspect of an organism’s existence helps define that organism’s niche. Interspecific competition may play an important role in shaping a species’ niche. Niches of different species may overlap either temporally or spatially. Niche overlap may promote interspecific com- petition, but the special adaptations that each species has for its own specific niche should protect it from extinction. For example, downy woodpeckers (Picoides pubescens) and hairy woodpeckers (P. villosus) are found in similar habitats from Newfoundland to the Gulf of Mexico. Although they often feed on the same tree at the same time, downies feed among the upper and smaller branches, while hairies locate their food on the trunk and larger branches. Niche overlap may occur on the medium-sized branches, but competition is minimized because the primary foraging microhabitat is slightly different. If there is complete niche overlap between two or more species, intense competition for the niche will occur, and one species will outcompete the others. The unsuccessful species will either be excluded from the habitat or forced to shift its niche—usually to a suboptimal habitat. This concept is often known as Gause’s Rule after the Russian G. F. Gause, who published a study in 1934 showing that when cultured Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 376 Chapter Thirteen together, one species of Paramecium drove a second, com- peting species to extinction. Hardin (1960) proposed the name competitive exclusion principle for this phenomenon. Although competitive exclusion has been demonstrated clearly in the laboratory, it probably is rare in nature because different species seldom compete for precisely the same niche in the same habitat (Mares, 1993). Fishes may adapt to different foods and to water of different depths, temperatures, salinities, and oxygen con- tents. Terrestrial species use elevational, macrohabitat, and microhabitat differences as well as food-size partitioning. Studies of plethodontid salamanders in the Appalachian Mountains, for example, have revealed habitat partition- ing based on elevation and moisture gradients (Hairston, 1949, 1980, 1983; Dumas, 1956; R. Jaeger, 1971). Daily (diel) and seasonal activity cycles, differences in micro- habitats (terrestrial, arboreal), and characteristics of the environment such as temperature or moisture are used by anurans to partition the environment. Within a breeding pond, the difference in time of breeding, egg development, and larval development of different species avoids direct competition with other species. Natural selection favors those individuals that breed at such a time as to avoid com- petition. Adaptive modifications of salamander larvae and tadpoles, including distinct interspecific differences in mouth structure and whether they inhabit still or flowing water, permit them to gather food in different macro- and microhabitats (see Fig. 6.30). Anoles of the Greater Antilles (Cuba, Hispaniola, Jamaica, and Puerto Rico) illustrate a classic case of adap- tive radiation (Losos and de Queiroz, 1998). Each of six species is adapted to its own ecological niche, in particular to the substrate on which it lives and moves. Anoles that live in the grass have slender bodies and very long tails, whereas a closely related species that must maintain its balance on narrow twigs has evolved a short body and stubby legs. A shorter-limbed species with large toe pads inhabits the upper trunk and canopy of trees, whereas a large species with large toe pads lives high in the crowns of trees. Some prefer shade; others seek out sunny basking sites. Although some overlap occurs, each species consumes differing food items. Garter snakes and ribbon snakes (both members of the genus Thamnophis) often inhabit the same general area (sym- patric). Competition between them, however, is reduced by differences in food requirements. Garter snakes feed exten- sively on earthworms; ribbon snakes usually shun earth- worms, but are fond of salamanders, frogs, and small fish. Interspecific competition is evident among introduced starlings (Sturnus vulgaris) and house sparrows (Passer domes- ticus) and native species in North America. Both European species compete with native American hole-nesters such as eastern bluebirds (Sialia sialis) and purple martins (Progne subis) for suitable nest sites. Due to their aggressiveness, both introduced species often usurp or evict the native species from their nest sites. BIO-NOTE 13.1 A Competitive Interaction An interesting example of competitive interaction was reported between bluebirds (Sialia) and chickadees (Parus). A pair of chickadees began building a nest of green moss in a bluebird house. The next day, the blue- birds entered the house and carried some of the moss away. These actions were repeated. Then the chickadees deposited a single egg on the nearly bare floor. The male bluebird went inside the box and came out with the egg in his beak. He flew to a large tree limb, where the egg balanced momentarily, before falling to the ground below. This action was repeated a second time, after which the chickadees left and did not return. Reed, 1989 MacArthur’s (1967) study of five species of warblers revealed they all fed on the same species of caterpillar prey, but they partitioned spruce trees into preferred foraging regions (Fig. 13.1). Although some overlap occurred, com- petition was minimal, and all five species were able to coex- ist during the breeding season. Among mammals, interspecific competition occurs in some areas between black bears (Ursus americanus) and griz- zly bears (U. horribilus), between red squirrels (Tamiasciurus) and gray squirrels (Sciurus), and between southern flying squirrels (Glaucomys volans) and northern flying squirrels (G. sabrinus) (Weigl, 1978; Flyger and Gates, 1983). This com- petition may be a function of territorial behavior (Layne, 1954; Ackerman and Weigl, 1970; Flyger and Gates, 1983). In the southern Appalachians, four closely related species of mice (Peromyscus leucopus, P. maniculatus, P. gossypinus, and Ochrotomys nuttalli) inhabited a 6-ha study area (Linzey, 1968). The mice partitioned the habitat by means of spatial orientation (terrestrial vs. arboreal) and by food preference. Both native and domestic mammals may be affected by indirect competition, a more subtle type of interspecific inter- action. Small mammals, such as mice, rabbits, prairie dogs, ground squirrels, gophers, and others, affect the growth of forage plants without competing directly with livestock or game animals for some of the aerial parts of plants. These small mammals consume the roots and early growth of grasses and forbs, and their presence can result in lower for- age yields above ground. Long-term investigations of the interactions among rodents, birds, and plants in the Chi- huahuan desert of southeastern Arizona have shown a per- sistent and steady competition among species despite the importance of climatic effects on the numbers of individuals (Brown et al., 1986). Brown et al. (1986) stated: “Our exper- iments suggest a view of community organization in which virtually all species affect each other through a complex web of direct and indirect interactions. These relationships are Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Interspecific Interactions 377 (a) Bay-breasted warbler (b) Cape May warbler (c) Blackburnian warbler (d) Black-throated green warbler (e) Myrtle warbler Coexistence of competing species. Robert MacArthur found that five species of warblers were able to coexist by partitioning spruce trees into pre- ferred foraging regions: (a) bay-breasted warbler (Dendroica castanea); (b) Cape May warbler (D. tig- rina); (c) Blackburnian warbler (D. fusca); (d) black- throated green warbler (D. virens); (e) myrtle warbler (D. coronata). FIGURE 13.1 highly asymmetrical, nonlinear, and influenced importantly by the physical environment as well as by other species.” ■ SYMBIOSIS Symbiosis (sym, “together,” and bios, “life”) is the term applied to an intimate relationship between members of different species. Such interactions may be beneficial to one or more members (commensalism, mutualism); other interactions may be detrimental (parasitism). Participants in symbiotic associ- ations often have coevolved with one another and continue to do so. Commensalism A commensal relationship exists when one member of the association benefits while the other is neither helped nor harmed. Here are some examples: Some fishes, such as jack- fish (Caranx) and pilot fish (Naucrates), seek protection in the vicinity of larger fishes such as barracudas, sharks, and rays (Moyle and Cech, 1996). In most cases, the larger fishes derive no advantage from their companions. A com- mensal relationship exists between gopher tortoises and many amphibians, reptiles, and mammals that inhabit their burrows (Lips, 1991) (Table 13.1) (Fig. 13.2). Woodchuck (Marmota monax) burrows also are used by a wide variety of vertebrates and invertebrates. Turtles often deposit their Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 378 Chapter Thirteen TABLE 13.1 Summary of Captures of Amphibians, Reptiles, and Mammals in Gopher Tortoise Burrows in Four Habitats in South-Central Florida HABITATS Scrubby Flatwoods Species Turkey Oak Sand Pine Scrub Burned Unburned Total Amphibians Southern toad (Bufo terrestris) 0 1 0 0 1 Greenhouse frog (Eleutherodactylus planirostris) 101 70 12 27 210 Narrow-mouthed toad (Gastrophryne carolinensis)011 02 Gopher frog (Rana areolata) 9 5 1 0 15 Subtotal 110 77 14 27 228 Reptiles Green anole (Anolis carolinensis)10618 Six-lined racerunner (Cnemidophorus sexlineatus) 1 5 4 0 10 Black racer (Coluber constrictor)32218 Eastern indigo snake (Drymarchon corais)02002 Southeastern five-lined skink (Eumeces inexpectatus)1830324 Eastern coachwhip snake (Masticophis flagellum)11204 Eastern coral snake (Micrurus fulvius)0 0 1 01 Pine snake (Pituophis melanoleucus)00101 Fence lizard (Sceloporus woodi)368522 Subtotal 27 19 24 10 80 Mammals Florida mouse (Podomys floridanus)11709 Cotton rat (Sigmodon hispidus)10001 Spotted skunk (Spilogale putorius) 0 0 1 0 1 Subtotal 2 1 8 0 11 Total 139 97 46 37 319 From K.R. Lips, Journal of Herpetology, 25(4):477–481, 1991. Copyright © Society for the Study of Amphibians and Reptiles, Oxford, OH. Reprinted by permission. eggs in alligator nests. The eggs presumably benefit from the alligator’s defense of the nest from predators. Aquatic turtles may hibernate inside a beaver lodge. Small birds sometimes construct their nests among the branches and twigs of an eagle’s nest. A unique commensal relationship exists between a bird and a lizard in New Zealand (Carr, 1970). Sooty shearwa- ters (Puffinus griseus) often share their burrows with tuataras (Sphenodon) (Fig. 13.3). The diurnal shearwaters occupy their burrows at night while the nocturnal tuatara is out foraging. The tuatara occupies the burrow during the day while the shearwater is fishing. When the bird migrates, the tuatara hibernates in the burrow. An unusual commensal relationship exists between fos- sorial blind snakes (Leptotyphlops dulcis), which feed on insect larvae in screech owl (Otus asio) nests, thus potentially reduc- ing larval parasitism on nestling owls (Gehlbach and Baldridge, 1987). Nestling owls in such nests had a higher survival rate, grew 19 percent faster, and fledged earlier than those in nests without snakes (Table 13.2). Owls transport live snakes to their nests and gain a benefit. There is no evi- dence, however, that the snakes gain any benefit by being in the nests rather than in the soil. Squirrel monkeys (Saimiri sciureus) find it advanta- geous to associate with capuchin monkeys (Cebus) because the latter provide a better predator warning system than squirrel monkeys possess (Terborgh, 1985). The recipro- cal benefit for the capuchins is minimal or nonexistent. Rats (Rattus rattus and R. norvegicus) and house mice (Mus musculus) have benefited by using structures built by Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Interspecific Interactions 379 Indigo snake Florida (gopher) mouse Gopher tortoise Pallid cave cricket Gopher frog Beetle Five-lined skink FIGURE 13.2 The long, cool burrow of the gopher tortoise (Gopherus polyphemus) in Florida provides refuge for a variety of vertebrate and invertebrate species. The tortoise derives neither benefit nor harm from these commensal relationships. Slender beetles feed on tortoise dung; cave crickets eat beetle dung as well as fungus. Gopher frogs (Rana capito) eat insects that wan- der or fall into the burrow. The nocturnal gopher mouse (Peromyscus floridanus) may excavate a side burrow in which it constructs its nest. Even the sandy dump pile may provide refuge for a five-lined skink (Eumeces inexpectatus). Sometimes, the gopher tortoise defends its burrow against a predatory snake by blocking the entrance with its shell. Source: Carr, The Reptiles, Life Nature Library. FIGURE 13.3 Sooty shearwaters (Puffinus griseus) often share their burrows with tuataras (Sphenodon). This unique commensal relationship allows the diurnal shearwaters to occupy their burrows at night while the nocturnal tuatara is out foraging. The tuatara occupies the burrow during the day while the shearwater is fishing. When the bird migrates, the tuatara hibernates in the burrow. humans and reach their highest densities in agricultural and urban areas. Large grazing animals such as zebras, cat- tle, buffalo, and horses stir up insects as they feed. Birds, such as cattle egrets (Caserodius albus) (see Fig. 11.9) and cowbirds (Molothrus ater), live among these mammals and feed on the grasshoppers, leafhoppers, and other insects disturbed by the grazing animals. Mutualism In the type of symbiotic relationship known as mutualism, both partners benefit from the association. Clownfishes live among anemones. They are not affected by the anemone’s sting, which serves to provide them a protected habitat. In turn, the clownfishes defend their homesite from other species that feed on anemones, and also provide anemones with scraps of food. Many other species of fishes allow them- selves to be cleaned by cleaner fishes (Fig. 13.4). Some even change color, a procedure that indicates a safe time to be cleaned and also makes parasites more easily visible against a contrasting background. Some pilot fish clean the mouths of manta rays. Reef fishes have been recorded cleaning algae or ectoparasites from sea turtles, and blacknose dace (Rhinichthys atratulus) have been observed apparently clean- ing wood turtles (Clemmys insculpta) (Kaufmann, 1991). Kuhlmann (1966) observed a toothed carp (Gambusia) clean- ing the mouth of a crocodile (Crocodylus acutus). Cleaning symbioses were reviewed and discussed by Feder (1966). The small ground finch (Geospiza fuliginosa) of the Galapagos Islands searches for ticks on marine iguanas. Oxpeckers (Buphagus africanus) remove ticks, botfly larvae, and other parasites from zebras, rhinoceroses, and other large mammals (Fig. 13.5). The intestines of most vertebrates, including humans, provide a suitable environment for beneficial bacteria that aid in food digestion and synthesize certain vitamins. Her- bivores, such as cattle, sheep, and deer, depend on bacteria and Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 380 Chapter Thirteen FIGURE 13.5 Yellow-billed and red-billed oxpeckers (Buphagus sp.) perch on the rump of a plains zebra (Equus sp.) in Masai Mara National Reserve. The birds help zebras by plucking off ticks and other pests. protozoans to help them digest the tough cellulose cell walls of the plant material on which they feed. Dickman (1992) noted: “Commensal and mutualistic associations among terrestrial vertebrates are clearly dynamic, and form and dissolve under different conditions of predator risk, resource levels, competition, and many other factors. An important assumption is that these associations are favoured only when the benefits to individuals exceed the costs.” Parasitism Parasitism is a vital interspecific interaction in which one member—the parasite—benefits while the other member— the host—is harmed in some way. Lampreys parasitize fish by sucking out their blood and body fluids (see Fig. 4.12). Cowbirds of the New World and cuckoos of the Old World are social parasites (Milius, 1998a) (see Fig. 8.72). They both lay their eggs in nests of other bird species, often removing one egg from the host’s nest prior to laying their own. Female cuckoos usually lay an average of eight eggs a year. Eggs are laid on alternate days and usually in two batches, separated by several days rest (Davies and Brooke, 1991). Their decep- TABLE 13.2 Nestling Growth Dynamics in Eastern Screech Owl Nests With One, Undisturbed (by Us), Live Blind Snake at Fledging Time Versus Same-Season Nests Without Blind Snakes but Same-Size Broods. Mean + SD and F values are from two-way ANOVAs, N = 6 each group a Snake Present Snake Absent Fp Nestling growth rate 4.52±0.54 3.79±0.61 Between groups 49.8 <0.001 (g/day) Among broods 11.5 <0.001 Fledging weight 121.3±7.19 123.3±7.73 Between groups 1.1 NS (g) Among broods 4.5 <0.01 From F. R. Gehlbach & R. S. Baldridge, “Live Blind Snakes (Leptotyphlops dulcis) in Eastern Screech Owl (Otus asio) Nests.” in Oecologia, 71:560–563. Copyright © 1987 Springer-Verlag, New York. a N=10 per group in a comparison without brood-size equality; however, mean number of nestlings is no different (3.3±0.7 vs. 2.8±1.0, F=1.6, NS) and results are the same; F=54.8, 7.2 (p <0.001) for growth rate and F=0.8 (NS), 2.5 (p <0.02) for fledging weight, between groups vs. among broods, respectively. This Nassau grouper (Epinephelus striatus) is being cleaned by two gobies. Cleaning symbiosis is a common mutualistic relationship between marine animals. FIGURE 13.4 Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Interspecific Interactions 381 FIGURE 13.7 Vampire bat (Desmodus rotundus) feeding on the foot of a cow. Observations of vampires indicate that this stance and area of assault illustrate the most frequent method of attack. The stance shows the quadrupedal relationship of bats. White wagtail Cuckoo Meadow bunting Cuckoo Redstart Cuckoo Great Reed warbler Cuckoo FIGURE 13.6 Cuckoo eggs often mimic the appearance of the host’s eggs. Source: Faaborg Ornithology, 1988, Prentice-Hall, Inc. tion involves surveillance, stealth, surprise, and speed. In less than 10 seconds, the female cuckoo alights on a nest, lays her own egg, removes one host egg, and is gone. The eggs often mimic the appearance of the host’s eggs (Fig. 13.6). Cuckoo eggs have been found in nests of at least 125 bird species in Europe (Wyllie, 1981). Many researchers have thought that cuckoos imprint on their foster parents and, when adult, choose to parasitize the same host species. However, studies in which newly hatched cuckoos were transferred into nests of other species failed to demonstrate host imprinting (Brooke and Davies, 1991). Besides having a shorter incubation period than their host species, cowbirds (Molothrus ater) hatch before many hosts by disrupting incubation of smaller eggs and, possibly, hatching in response to stimuli from host eggs (McMaster and Sealy, 1998). In addition, young cowbirds and cuckoos are usually larger than the natural young in the parasitized nest, and they either take the lion’s share of the food or eject the host young from the nest (see Fig. 8.72). Friedmann and Kiff (1985) recorded 220 species as having been parasitized by brown- headed cowbirds, with 144 species actually rearing young cow- birds. This difference in the number of species parasitized versus those actually rearing cowbirds is due to host recogni- tion and counter-strategies: deserting the nest, rejecting the cowbird egg, or depressing the egg into the bottom of the nest. In Virginia, 39 percent of dark-eyed junco (Junco hye- malis) nests contained at least one cowbird egg (Wolf, 1987). Cowbirds laid an average of 1.7 eggs per nest and removed an average of 1.2 junco eggs per nest. Smaller species such as cedar waxwings (Bombycilla cedrorum), Baltimore orioles (Icterus galbula), and warbling vireos (Vireo gilvus) remove the cowbird egg by puncture-ejection (entire cowbird egg removed or pieces of shell removed after egg contents are consumed) (Sealy, 1996). Larger species generally remove cowbird eggs by grasp-ejection. In the early 1980s, half of all nests of the least Bell’s vireo (Vireo bellii pusillus) on the Camp Pendleton military base in southern California were parasitized by cowbirds, and the vireo population was near extinction (Holmes, 1993). When a cowbird trapping program reduced parasitism to near zero, the vireo population increased tenfold. Cowbird populations are being controlled by trapping at Camp Pendleton as well as in the breeding grounds of several endangered songbirds, including the Kirtland’s warbler (Den- droica kirtlandii) in northern Michigan and the black-capped vireo (Vireo atricapillus) in central Texas (Holmes, 1993). American goldfinches (Spinus tristis) are regularly para- sitized by cowbirds, but cowbirds do not survive the nestling period because the granivorous diet of the goldfinch provides inadequate protein (Middleton, 1991). It is rare among birds for the diet of nestlings to be composed mainly of seeds, because seeds are relatively low in protein. The only known parasitic mammals are vampire bats, which feed on fresh blood of sleeping or resting birds and mammals, including humans (Fig. 13.7). Their teeth are sharp, so that the incision is virtually painless and the victim is not awakened or disturbed as blood is “lapped up” rather than “sucked out.” The saliva may contain an anticoagulant, so that blood may continue to flow from the wound for sev- eral hours. The bitten animal may contract virally caused diseases such as rabies, or secondary infections may develop at the site of the wound. Male Asian elephants with longer tusks have been found to have fewer internal parasites (Bagla, 1997). Males carrying genes for resistance to parasites are healthier and in a better Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 382 Chapter Thirteen FIGURE 13.8 A black rat snake (Elaphe obsoleta) homes in on a clutch of northern cardinal eggs. Snakes strongly prefer to forage along forest edges. Eggs and nestlings are normally only a minor part of the snake’s diet. condition to develop secondary sexual characteristics. These better-fit males are then more likely to be chosen by females as mates. Since ivory hunters are likely to poach the best males because of their larger tusks, it is feared that poaching may weaken the elephant gene pool by removing the most fit males and their parasite-resistant genes from the population. Parasitism of reintroduced and captive endangered species by external (ticks, mites, lice, fleas) and internal (nematodes, trematodes, cestodes) parasites may be a critical danger to their well-being and reestablishment (Phillips and Scheck, 1991). Potential parasites need to be considered when designing and implementing restoration projects. ■ PREDATION Predation is an interaction in which one species—the predator—benefits from killing and eating a second species—the prey. Predators and prey coevolve, with preda- tors becoming specialized to capture their prey, and prey species becoming adapted to evade their predators. Each vertebrate class has a large number of predaceous species. Sharks feed on other fishes and marine mammals. Largemouth bass (Micropterus salmoides) feed primarily on smaller fishes. Amphibians and reptiles feed on a wide variety of inver- tebrates and vertebrates, with the choice of food being primar- ily determined by the size of the mouth-opening—amphibians and reptiles are gape-limited predators. Amphibians feed pri- marily on invertebrates, although some larger forms such as bullfrogs (Rana catesbeiana) will eat almost any suitably sized animal that moves within striking range. Many aquatic tur- tles feed on invertebrates, as well as on small fish and amphibians. Snapping turtles (Chelydridae) are known to consume amphibians, snakes, small turtles, birds, and small mammals. Most marine turtles are omnivorous. Juvenile green turtles (Chelonia mydas), however, are more carnivorous than adults, which subsist mainly on plants. Most lizards feed on invertebrates, although some, such as the Gila mon- ster (Heloderma suspectum) and the Komodo dragon (Varanus komodoensis), include mammals in their diet. Crocodilians prey on fishes, reptiles, and birds and on mammals as large as antelopes. All snakes are predaceous, feeding on prey rang- ing from larger invertebrates, birds, and bird eggs (Fig. 13.8) to mammals. Carnivores, in general, have a more difficult time obtain- ing food than herbivores. Once a carnivore captures its prey, however, the meal is far higher in nutrition because of its pro- tein and fat content. Thus, meat eaters spend considerably less time eating than plant eaters (Fig. 13.9). In addition, the larger the herbivore, the more time it needs each day to obtain sufficient food. Many birds and mammals are insectivorous; others feed on a wide variety of fishes, amphibians, reptiles, birds, and mammals. Hawks, eagles, ospreys, and owls feed on fishes, lizards, snakes, other birds, and mammals up to the size of skunks, monkeys, and sloths. Most predatory birds consume their smaller prey whole, later regurgitating the indigestible hair, bones, feathers, scales, or insect parts as pellets (Fig. 13.10). Predatory mammals include such groups as bears, raccoons, cats, wolves, foxes, and weasels. Black bears (Ursus americanus) and raccoons (Procyon lotor), for example, are major predators on American alligator (Alligator mississippiensis) eggs and young (Hunt and Ogden, 1991). Predators in certain regions have preferred prey (cougar–deer; wolf–moose; fox–rabbit), but most are oppor- tunistic and will kill a variety of prey. They frequently cap- ture older, weaker, debilitated animals, thus acting as a selective agent promoting the genes of those prey animals able to evade capture. Predators may differentially consume individuals based on age or sex within populations of prey species and thus may have subtle effects on prey-population dynamics. On an island off the coast of western Australia, adult house mice (Mus musculus) foraged primarily in dense cover; juveniles, especially females, used areas of open vegetation more than adults and were potentially most at risk of predation (Fig. 13.11a) (Dickman et al., 1991). Barn owls (Tyto alba) took a greater number of young female house mice than any other size or sex class. Correlations between the hourly number of hunting owls and the overall hourly capture rates of mice were significant for juvenile female (r=;0.84, p<0.001), almost significant for juvenile males (r=;0.57, p ~ 0.05), and not significant for adults (males: r=:0.10; females: r=;0.51) (Fig. 13.11b). These data strongly support the hypothesis that juvenile mice, especially females, that use Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Interspecific Interactions 383 100 90 80 70 60 50 40 30 20 10 0 Percentage of time spent feeding Body weight (lbs.) Herbivores 100 90 80 70 60 50 40 30 20 10 0 Percentage of time spent feeding Body weight (lbs.) Carnivores Elephant 5,750 Rhino 3,000 Gazelle 125 Monkey 17 Hunting dog 50 Lion 400 Cheetah 300 Polar bear 1,200 FIGURE 13.9 Although carnivores must work harder than herbivores to find a meal, a carnivore’s meal is higher in nutrition than an herbivore’s. Thus, carnivores spend much less of their time eating than herbivores. In addition, the larger the herbivore, the more time it needs each day simply to stay fed. Source: Data from Shipman, “What Does it Take to be a Meateater?” in Discover Magazine, September, 1988. more open vegetation than adults face a higher risk of pre- dation from hunting owls. Some predators and their prey have developed complex interrelationships. For example, moose (Alces alces) colonized Isle Royale in Lake Superior, probably swimming from nearby Ontario in the early part of the 20th century (Mech, 1966) (Fig. 13.12). With no effective predators and an abun- dant food supply, the population grew to very high levels by the late 1920s. Murie (1934) estimated 1,000–3,000 moose present in 1929 and 1930. Significant mortalities from mal- nutrition apparently reduced the population to several hun- dred animals by the mid-1930s (Hickie, 1936). The population again increased, until direct mortality from mal- nutrition was observed in the late 1940s. In 1947, a popula- tion of 600 moose was estimated by aerial strip count (Krefting, 1951). Mech (1966) estimated the 1960 popula- tion at 600 animals. The moose population apparently increased during the 1960s (1,300 to 1,600 from 1968–1970) and leveled off, or perhaps even declined, from 1970 to 1974. Mid-winter aerial censuses in 1972 and 1974 produced esti- mates of 818±SE 234 and 875±SE 260 moose, respec- tively (Peterson, 1977). During the winter of 1948–49, timber wolves (Canis lupus) managed to cross the ice from the mainland of Ontario and became established on the island. Their population increased and fluctuated between 20 and 50 animals during FIGURE 13.10 A life-size regurgitated pellet from a short-eared owl (Asio flammeus). The pellet contains the remains of a small rodent. Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 384 Chapter Thirteen the period 1960–1980. Thus, predator and prey had reached a dynamic equilibrium—a stabilization of numbers such that each species could survive without having a detrimental impact on the other. Sufficient resources were available to support the moose population, which was maintained at healthy levels by selective culling of old and weak individu- als by the wolves. In 1958, wildlife biologist Durward Allen began tracking the changing population numbers in what has become the longest-studied system of natural predator–prey dynamics in existence. After the wolf population on Isle Royale reached a peak of 50 animals in 1980, it experienced a decline in the early 1980s, from which it still has not recovered (Fig. 13.12). Only four pups were born, to the same female in one wolf pack, between 1991 and 1993 (Mlot, 1993). As of August 1993, the other two packs were down to just a pair of wolves Night Hour of the day Nos. of observations Nos. of captures 12 10 8 6 4 2 0 40 30 20 10 0 12 16 20 24 4 8 Juveniles Adults Mus males Tyto alba 30 20 10 0 Juveniles Adults Mus females (b) (a) Adults Juveniles Females Males Hour of the day Percentage active in open vegetation 70 60 50 40 30 20 10 0 40 30 20 10 0 12 16 20 24 4 8 FIGURE 13.11 (a) Hourly number of captures of Mus musculus in open vegeta- tion, expressed as percentages of the total numbers of captures in different sex and size categories. (top) Females. (bottom) Males. Results for three periods of 24 hours are combined. (b) Comparison of hourly numbers of captures of Mus musculus by sex and size, and numbers of observations of Tyto alba. Results for three periods of 24 hours are combined. each. The moose population, which has steadily increased, reached a record high of about 1,900 animals in 1993. The decline of the wolves was probably the result of two factors: an encounter with canine parvovirus in 1981, and low genetic variability (Mlot, 1993). Because the start of the wolf’s decline coincided with a 1981 parvovirus outbreak in nearby Houghton, Michigan, it is thought that the virus could have been carried to Isle Royale on the hiking boots of visitors to the U.S. national park on the island. Restriction enzyme analysis of the wolves’ mitochondrial DNA revealed that they were all descended from a single female and had only about half the genetic variability of mainland wolves (Mlot, 1993). Whenever a small number of individuals manage to cross an already existing barrier and found a new geographi- cally isolated colony, they generally carry with them in their own genotypes only a small percentage of the total genetic [...]... crops and ornamental plantings The white-tailed deer (Odocoileus virginianus) in parts of the eastern United States is an excellent example of a species whose population has grown beyond the carrying capacity of its range Linzey: Vertebrate Biology 388 13 Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Chapter Thirteen BIO-NOTE 13. 2 Seal Die-Offs and Global Warming Human predation... the first known instance in which natural selection brings FIGURE 13. 13 The solitary grizzly bear (Ursus arctos) is classified as an omnivore, but in coastal regions of the bears’ range, salmon become an important component of the diet Linzey: Vertebrate Biology 386 13 Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Chapter Thirteen about a change in body dimensions through growth... “reed” in the marsh Linzey: Vertebrate Biology 13 Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Interspecific Interactions 387 FIGURE 13. 16 Musk oxen (Ovibos moschatus) forming a defensive circle with the females and young in the center Predation pressure can favor the evolution of social life when members of the group are safer than solitary animals FIGURE 13. 17 of ruffed grouse.. .Linzey: Vertebrate Biology 13 Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Interspecific Interactions FIGURE 13. 12 2,000 60 Moose 1,800 1,600 1,400 40 1,200 1,000 30 Moose Wolves 50 800 20 600 10 Wolves 400 200 0 0 1955 1960 1965 1970 1975 1980... trees (Stix, 1995) (Fig 13. 17) The leaves are hard to digest and provide one of the least nutritious diets of any mammal Eucalyptus trees growing in poor soil produce more toxins than trees in good soil Thus, the trees have evolved leaves that are foul-tasting and toxic, but koalas have evolved complex digestive systems to deal with the poisons FIGURE 13. 15 FIGURE 13. 14 The fire-bellied toad (Bombinator... Schneider, S H 1989 The changing climate Scientific American 261(3):70–79 White, R M 1990 The great climate debate Scientific American 263(1):36–43 Linzey: Vertebrate Biology 13 Interspecific Interactions Text © The McGraw−Hill Companies, 2003 Interspecific Interactions Vertebrate Internet Visit the zoology website at http://www.mhhe.com to find live Internet links for each of the references listed below 1... predator (see Cycles, Chapter 10) Some predators, such as bears (Fig 13. 13), lynx, cougars, owls, and snakes, hunt singly Others, such as wolves and lions, usually hunt in groups Female lions normally make the kill, after which food is shared with the rest of the pride, consisting of several males and the young Grasshopper mice (Onychomys spp.), whose primary diet consists of invertebrates and small... fishing seasons Size limits as well as the numbers and kinds (e.g., bucks, does) that can be harvested legally are written into law Age limits are set for hunters and fishermen, and licenses (in-state, out-of-state) are required As a result of these measures, fish hatcheries and game farms have been established to propagate certain species for stocking in order to increase populations of prey for sports... might prey on them The coral snake (Micruris fulvius) of the southern United States is one example The poison-dart frogs of South America are brilliantly patterned with reds, blues, yellows, and blacks The fire-bellied toad (Bombinator igneus) assumes a unique “warning” position when threatened (Fig 13. 14) It exposes its bright red or yellow belly coloration in an attempt to discourage a potential predator... global warming What effects is global warming having on vertebrate populations? Supplemental Reading Ausubel, J H 1991 A second look at the impacts of climate change American Scientist 79:210–220 Byers, J A 1997 American Pronghorn: Social Adaptations and the Ghosts of Predators Past Chicago: The University of Chicago Press Dietz, R., M.-P Heide-Jorgensen, and T Harkonen 1989 Mass deaths of harbor seals . variety of vertebrates and invertebrates. Turtles often deposit their Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 378 Chapter Thirteen TABLE 13. 1 Summary. depend on bacteria and Linzey: Vertebrate Biology 13. Interspecific Interactions Text © The McGraw−Hill Companies, 2003 380 Chapter Thirteen FIGURE 13. 5 Yellow-billed and red-billed oxpeckers (Buphagus. animals during FIGURE 13. 10 A life-size regurgitated pellet from a short-eared owl (Asio flammeus). The pellet contains the remains of a small rodent. Linzey: Vertebrate Biology 13. Interspecific