Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 CHAPTER 10 Population Dynamics ■ INTRODUCTION Animal populations, which are dynamic and constantly changing, depend on successful reproduction to maintain their existence. Other important factors in maintaining viable populations include an adequate food supply, sufficient home sites, and the effects of dispersal, immigration, emigration, climate, predation, disease, and parasites. The impact of some of these factors is density-dependent—that is, the effect varies according to the population density; for others, the impact is density-independent—that is, unrelated to population size. ■ POPULATION DENSITY Population density is an important variable that can influence the level of competition for scarce resources. Every habitat has a theoretical maximum number of individuals of a given species that it can support for an extended period of time. This level is known as the carrying capacity (Fig. 10.1a) and is determined by environmental resistance factors acting on the reproductive (biotic) potential of a population. It is pri- marily determined by the availability of food and shelter. Vertebrates exhibit three basic types of population growth. Once many species reach the environmental carrying capacity of their range, they maintain relatively stable populations (Fig. 10.1b). This is especially true of species inhabiting some trop- ical regions where temperature and rainfall show little vari- ability. Some species that normally maintain relatively stable populations experience sharp population increases at irregular intervals. Such irruptions, which cause the population to exceed its carrying capacity, may be the result of such transient factors as a reduction in predators, an increase in food, a favor- able change in the weather, or any combination of these. Still other species experience sharp increases in their population sizes at regular intervals, followed by crashes. Species exhibit- ing regular cyclic population increases usually do so either every 3 to 4 years or approximately every 10 years. Reproductive (Biotic) Potential The maximum number of young that a population can produce under ideal conditions during a particular time period is referred to as the reproductive (biotic) poten- tial of that population. In a healthy, natural population, the birth rate will equal, if not exceed, the death rate, but due to environmentally limiting factors, the reproductive potential is rarely, if ever, reached. Dispersal, immigra- tion, and emigration may affect the reproductive poten- tial to a limited degree. Most populations will level off after the population reaches a certain size (the carrying capacity). The point at which population growth levels off varies with the species, the habitat, and the climate. A natural population will con- tinue to show fluctuations (seasonal, annual), but they will generally not be far removed from the average carrying capacity (Fig. 10.1c). Each individual can affect the reproductive potential of its species in one or more of the following ways: 1. By producing more offspring at a time. 2. By having a longer reproductive life, so that it repro- duces more often during its life span. 3. By reproducing earlier in life. The shorter the genera- tion time of a species (that is, the younger its members when they first reproduce), the higher its reproductive potential (Fig. 10.2). Reproductive rates vary widely among the vertebrates. Some fishes such as sturgeon and cod may produce several million eggs annually, whereas many mammals normally give birth to only a single young. Factors such as climate and pre- dation of eggs and/or young have undoubtedly been factors in the evolution of egg production. Numerous hypotheses have been proposed to explain clutch size in birds. These were summarized by Lack (1954), who presented arguments for and against each hypothesis. Among the principal hypotheses are the following: 1. Females produce as many eggs as they are physiologi- cally capable of producing. Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 Population Dynamics 325 Environmental resistance Biotic (reproductive) potential Carrying capacity (a) Time Number of individuals Irruptive Cyclic Stable (b) Time Number of individuals (c) Year Number of breeding pairs 400 300 200 100 0 1940 1950 1960 (a) The theoretical number of individuals of a given species that can be supported for an extended period of time in a habitat is known as the carrying capacity. It is determined by environmental resistance factors (pri- marily food and shelter) acting on the reproductive (biotic) potential of the population. (b) Some populations remain relatively stable after reaching the carrying capacity of their range; some experience regular cyclic pop- ulation increases; and others experience sharp population increases (irruptions) at irregular intervals. (c) A stable population is illustrated by the number of breeding pairs of gray herons (Ardea cinerea) in northwestern England. After recovering from the severe winter of 1947, this population showed little fluctuation over a 15-year period. Source: (c) Data from D. Lack, Population Studies in Birds, 1966, Claren- don Press, New York. FIGURE 10.1 Time (years) Brood size (b) = 2 Age at first reproduction = 1 year P opu l a ti on s i ze 10 8 6 4 2 0 12345 2 years 3 years 4 years Also curve for: Brood size = 4 Age at first reproduction = 4 Population growth is dramatically affected by the age at which females first reproduce. In each of these examples, females produce two off- spring per year, but the age at which females first reproduce differs for each curve (first reproduction at 1, 2, 3, or 4 years of age). Changing the age of first reproduction from 4 to 3 years has the same effect as doubling the brood size from two to four. Source: Data from Cole, Quarterly Review of Biology, 29:103, 1954. FIGURE 10.2 2. Females produce as many eggs as they can successfully incubate. 3. Females produce approximately the number of eggs and young that the parent(s) can satisfactorily feed and care for. Whereas each of these hypotheses holds true for many species, many exceptions exist. For example, many birds will lay additional eggs in their nests if one or more of the orig- inal eggs is removed. This fact has been of extreme impor- tance in the attempt to increase the population of endangered whooping cranes (Grus americana). Females normally pro- duce two eggs. When biologists remove one egg for artifical incubation in order to increase the size of captive flocks, the female usually will produce and incubate a third egg. Whereas many birds apparently produce as many eggs as they can satisfactorily incubate, there are other species that seemingly could incubate more than the number of eggs they produce in the average clutch. Critics of the third hypothe- sis point out that precocial birds do not need to expend time and energy feeding their offspring. In studies where clutch size was adjusted experimentally during incubation, larger clutches were associated with signif- icantly lower percentage hatching success in 11 of 19 studies; longer incubation periods in 8 of 10 studies; greater loss of adult body condition in 2 of 5 studies; and higher adult energy expenditures in 8 of 9 studies (Thomson et al., 1998). Since incubation does involve metabolic costs and since the demands of incubation increase sufficiently with clutch size to affect Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 326 Chapter Ten breeding performance, Thomson et al. (1998) proposed that optimal clutch size in birds may in part be shaped by the number of eggs that the parents can afford to incubate. Among mammals, small prey species such as mice, voles, rabbits, and ground squirrels usually produce several litters annually, each of which consists of several young. Many of these species make up the primary consumer level in a food web or food pyramid; they are subsequently consumed by secondary and tertiary consumers (Fig. 10.3). Bailey (1924) recorded a meadow vole that produced 17 litters within 12 months. Larger species, such as most ungulates, breed only once a year and produce a single offspring. Although smaller species generally produce greater numbers of young annually than larger species, longevity is also a factor. Many small mammals have a life expectancy of approximately 1 year. However, most bats, although small, are long-lived—up to at least 34 years in Myotis lucifugus (Keen and Hitchcock, 1980; Tuttle, pers. comm., 1992). With the exception of lasi- urine bats, most North American species produce a single young annually. Many predators, such as mustelids, canids, and felids, produce only one or two litters annually. The ratio of adults to juveniles varies during the year. Juveniles form a larger proportion of the population during and immediately after the breeding season in temperate regions. By fall and early winter, many juveniles have either matured and become part of the adult population or have been lost. Most temperate populations, therefore, reach their largest size in late fall and early winter. Loss of individuals during the harsher conditions of winter usually leads to low population levels in late winter, just prior to the breeding season of many species. In years when the climate is favor- able and food is plentiful, many species may breed well into the fall, resulting in larger populations the next year. Environmental Resistance Although populations have the biotic potential to increase, a variety of factors act to limit the number of young actu- ally produced or that survive. These factors represent the environmental resistance. Climate (including rainfall, flood- ing, drought, and temperature) is a primary controlling fac- tor. Other controls are exerted by intraspecific aggression, inadequate supply of den sites, predation, disease, and par- Northern Harrier Upland plover Garter snake Crow Cutworm Meadow frog Grasshopper Grassland Badger Coyote Weasel Prairie vole Pocket gopher sparrow A food web for a prairie grassland in the midwestern United States. Arrows flow from the grassland (producer) to various levels of consumers. FIGURE 10.3 Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 Population Dynamics 327 asites. Resistance factors can be grouped into two categories: density-dependent and density-independent. Density-Dependent Factors Density-dependent factors are those whose effects vary directly with the density of the population. For example, as population density increases, suitable home sites and food may become scarcer per individual. As the rate of individual contacts increases, intraspecific aggression may increase; females may stop breeding; the rate at which nestling young may be killed and/or cannibalized by their parents may increase; and the rate at which juveniles are forced to disperse may be greater than what occurred at lower densities. Parasites can increase in response to population size of the host, and diseases can spread much more rapidly. For example, when waterfowl congregate in dense flocks, the incidence of infection and the chances of an epizootic are increased (Fig. 10.4). Approximately 600 Mediterranean monk seals (Monachus monachus) remain in the wild, mostly in groups of about 20. From May to August, 1997, a catastrophic epizootic struck the largest social group (Osterhaus, 1997; Harwood, 1998). Of 270 seals living in a pair of caves on West Africa’s Mau- ritanian coast, only about 70 survived the disease. Osterhaus (1997) reported that most of the seals examined harbored a dolphin morbillivirus, a virus similar to the one that causes distemper in dogs. Hernandez et al. (1998), however, carried out histopathological examination of lung and other tissues from 14 fresh carcasses and found no indication of typical morbillivirus lesions. There was no evidence of primary viral damage or secondary opportunistic infections in lung tissue, which are hallmarks of morbillivirus infections in other aquatic mammal species. The terminally ill seals exhibited clinical signs of lethargy, motor incoordination, and paraly- sis in the water—symptoms consistent with drowning caused by paralysis due to poisoning. Hernandez et al. (1998), who identified three species of toxic dinoflagellates in eight water samples collected from near the colony during the mortality event, suggested that poisoning by paralytic algal toxins may have been the cause of death. Optimal densities may vary seasonally in temperate areas. For example, the lower flow of many streams during summer determines the annual carrying capacity for species like trout (Salmo). The winter food supply may determine the annual carrying capacity for many species, even though more animals can be supported during the summer months. In ungulates, food limitation as a cause of density-dependent population regulation has been shown for roe deer (Capreo- lus), wild reindeer (Rangifer), kangaroos (Macropus), wilde- beests (Connochaetes), and white-eared kobs (Kobus) (reviewed by Skogland, 1990). One effect of high population density in herbivores is overgrazing. Skogland (1990) reported increased tooth wear and lowered body size and fat reserves in wild reindeer (Rangifer tarandus). Skogland (1990) stated: During late winter foraging, lichen mats in the Loiseleria- Arctostaphylion plant alliance become the only available vegetation type due to snow cover [Skogland, 1978]. As the unrooted lichens are grazed off, the animals substi- tute easily digestible lichens in their diet by the dead parts of grasses, dwarf shrubs, and also mosses, with insufficient nutrient content [Skogland, 1984a]. Increased use of crustaceous lichens with encrusted small rock particles as well as soil particles and detritus in the ingested diet accelerated molar wear. This lowers chew- ing efficiency and increases the passage time of larger plant particles into the digestive system whose ability to process energy is slowed down [Skogland, 1988]. Although adult female survival rate was not affected, a sig- nificant negative correlation existed between population den- sity and juvenile winter survival rate. Calves normally were not able to compete successfully with conspecifics of higher rank. Neonatal survival was directly related to maternal con- dition during the last part of gestation and the calving sea- son (Skogland, 1984b). Male common toads (Bufo bufo) tend to call at low den- sities, but are more likely to remain silent at high densities (Hoglund and Robertson, 1988). Male wood frog (Rana syl- vatica) density has a significant effect on the behavior of searching male wood frogs at breeding ponds (Woolbright FIGURE 10.4 A concentration of snow and blue geese. When waterfowl congregate in dense flocks, the incidence of infection and the chances of an epi- zootic such as fowl cholera are increased. Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 328 Chapter Ten et al., 1990). When the male population density is low, males are more likely to be stationary. As male density increases, more males actively search for females. High density reduces growth rates in amphibians, thus lengthening exposure to predators and possible unfavorable environmental conditions (e.g., Petranka and Sih, 1986; Wilbur, 1987, 1988). Van Buskirk and Smith (1991) recorded significantly reduced survival and growth rates and an increase in the skewness of the size distributions of individuals with increasing density in blue-spotted salamanders (Ambystoma laterale) in Michigan. Individuals in high-density populations showed an increased skewness in body size, with only a few salamanders becoming large and most remaining small. This tendency did not occur in populations with lower densities. Some species seem to have an inherent self-regulating population control mechanism. This is especially true in ter- ritorial species in which individuals space themselves so that they have an adequate supply of food and shelter. In other species, when the population increases to a certain size, food and home sites become scarcer, intraspecific aggression increases, and breeding decreases or ceases. Many, but not all, members of the population may emigrate from the area. The best known example is the lemming (Lemmus) of Norway. As many members leave the area, more home sites and food become available for those left behind. Intraspecific aggres- sion falls, individuals become better nourished, breeding resumes, and the population begins growing again. Some species exceed the carrying capacity of their range. Because of all the environmental factors acting to control population increase, this is rare for a natural population. It is most common in those populations that are managed by humans, such as herds of deer and elk that are confined to military reservations, parks, and refuges. In addition, herds of elephants whose ancient migration routes and feeding areas are being encroached on by an expanding human population are, through no fault of their own, exceeding the carrying capacity of their dwindling range. In their attempts to locate food, they frequently trample crops and break down fences. In some areas, predator control measures are undertaken in efforts to increase the numbers of another species, usually a game species. Predators often cull sick, lame, injured, and old individuals from a population. When the predator con- trol measure is implemented, the protected species often increases and may exceed the carrying capacity of its range. To prevent overpopulation, the levels of many game species are controlled by federal and state agencies. These agencies set “limits” on the number of individuals of each sex of a given species that can be killed during certain seasons of the year. For- merly, many people were subsistance hunters and utilized most parts of an animal that they killed. Today, some hunters still fall into this category, but most hunters are looking for trophy ani- mals (biggest rack of antlers, etc.). They attempt to kill the largest, healthiest male specimens in order to mount their heads. Only in recent years have regulatory agencies promoted efforts to cull females from the population in order to balance the sex ratio and manage reproductive rates. In deer and many other species, one male will breed with multiple females; thus, pop- ulations can be more efficiently managed by culling some females rather than by focusing exclusively on males. A coyote-proof enclosure was erected encompassing 391 hectares (ha) of pasture on the Welder Wildlife Foundation Refuge in Texas in 1972 (Teer et al., 1991). The immediate response was an increased size of the deer (Odocoileus virgini- anus texanus) herd (Fig. 10.5). Fawn survival was 30 percent Year Inside Deer per sq/km 2 90 85 80 75 70 65 60 55 50 45 40 35 30 25 20 15 10 5 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 Outside FIGURE 10.5 White-tailed deer (Odocoileus virginianus texanus) population estimates inside and outside the coyote-proof pasture from 1972 until 1990 at the Welder Wildlife Foundation Refuge in Texas. Source: Data from J. G. Teer, et al., “Deer and Coyotes: The Welder Experiments” in Transactions of the 56th North American Wildlife and Natural Resources Conference 550–560, 1991. Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 Population Dynamics 329 TABLE 10.1 Number of Predators Removed from Kaibab Deer Habitat Dates Mountain Lions Coyotes Wolves Bobcats 1906–1923. U.S. Bur. of Biol. Survey 674 3,000 11 120 1929–1939. Private hunters and trappers 142 4,488 20 743 for fur, sport and lion bounty 1940–1947. USFWS 36 1,401 0 396 1948–1963. USFWS 18 733 0 282 1964–1976. Private hunters and trappers for fur and sport. 13 No records 0 No records Lion bounty ended 1970 From C. Y. McCulloch, in Southwestern Naturalist, 31(2):217, 1986. Copyright © The Southwestern Naturalist. Reprinted by permission. higher inside the enclosure than outside, where coyotes (Canis latrans) were uncontrolled. After several years, the high number of deer caused forage to become scarce, and deer began to die. Studies showed that mortality was caused pri- marily by lack of adequate food. Parasite loads also had increased. The deer herd reached a low point in 1980, after which it began to increase as food supplies returned to nor- mal. Beginning in 1982, coyotes were once again present within the enclosure, and predation prevented the herd from increasing as it had during the years of predator control. A classic example of a species exceeding the carrying capacity of its range involved the Kaibab mule deer (Odocoileus hemionus) in northern Arizona. In 1906, President Theodore Roosevelt set aside approximately 750,000 acres as a game refuge. At that time, an estimated 4,000 deer inhabited the area. Not only was hunting prohibited, but a predator con- trol program was begun. Within the next 10 years, 600 moun- tain lions were killed. The small wolf population living on the area was almost exterminated by 1926, and it was completely eliminated by 1939. By 1939, more than 7,000 coyotes had been killed (Table 10.1). The winter food supply was the lim- iting factor that determined the annual carrying capacity, which was estimated to be about 30,000 animals. By 1920, however, an estimated 100,000 deer were present on the refuge. During the next two winters, 60 percent of the pop- ulation died of starvation. An estimated 75 percent of the fawn crop was lost during the winter of 1924–25. The numbers continued to decrease due to the depleted range. By 1939, the population had declined to 10,000 animals. However, publicly funded coyote control (trapping, shooting, and poisoning) continued in the area from 1940 until May 1963, resulting in phenomenally high deer densities in the early 1950s (McCulloch, 1986). Presumably due to the high density and inadequate food supply, deer were in poor physical condi- tion and reproduction was low. McCulloch (1986) noted that absolute comparisons of herd size estimates could not be made for the different eras such as 1906–1940 vs. 1950–1961 vs. 1972–1979 because the deer inventory methods varied and were not compatible. Private sport hunting and fur trapping continued after 1963. Mountain lions were designated as game animals in 1971, and now can be taken normally only during designated hunting seasons by sport hunters. As of 1977, an estimated 40 adult mountain lions inhabited the Kaibab (McCulloch, 1986). During the period 1972–1979, the deer population experienced a decline of 9 percent per year (Barlow and McCulloch, 1984). Barlow and McCulloch (1984) stated: “Reasons for the decrease in deer abundance from 1972 to 1979 are not yet known. Climatic factors and increased natural pre- dation are both suspected. We know, however, that the decline has not continued. Pellet counts indicate that the number of deer in Kaibab has increased dramatically since 1979, and now may have exceeded the 1972 population size.” Thus, high lev- els of reproduction and deer in good physical condition have been achieved without predator control programs. As of 1996, an estimated 30,000 deer were living on the refuge. In many areas of the world, increasing wildlife popula- tions are creating problems. The spread of communicable diseases, such as rabies, has been slowed by reducing the pop- ulations of striped skunks, raccoons, and foxes (Bickle et al., 1991). Various control methods involving shooting, trapping, and poisoning have been used. More recently, fertility- inhibiting implants and contraceptive vaccines are being tested for birth control purposes (Moore et al., 1997). Nor- plant implants containing levonorgestrel, a synthetic proges- tin, have proved to be effective fertility inhibitors in several species, including Norway rats (Rattus norvegicus), rabbits (Oryctolagus cuniculus), striped skunks (Mephitis), and humans (Homo sapiens) (Phillips et al., 1987; Brache et al., 1990; Bickle et al., 1991). A single administration of immunocontraceptive vaccine was effective for more than 3 years in gray seals (Hali- choerus grypus) (Brown et al., 1996). A vaccine made from pig ovaries has been used successfully as a contraceptive to control wild horse populations on Assateague Island in Maryland and white-tailed deer on Long Island (Kemp, 1988; Daley, 1997). The vaccine is made of minced pig ovaries that are distilled until only the membrane of the eggs (zona pellucida) is left. This is then mixed with a substance that helps stimulate the immune system. When the mixture is injected, it causes the horse’s body to form antibodies that bind to the outside of the egg when the female ovulates, blocking the sperm receptor Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 330 Chapter Ten sites there and preventing fertilization (Daley, 1997). In lab- oratory tests, the vaccinations have proven to be 90 percent effective and reversible. Fertility returns within a year. BIO-NOTE 10.1 Elephant Birth Control Programs Female African elephants usually are in heat just 2 days of every 17 weeks. In an attempt to control the expand- ing elephant population in South Africa’s Kruger National Park, testing began on two forms of contracep- tion in 1996. The first method involved injecting specially-designed estrogen implants into 31 non- pregnant females. The implant is designed to slowly release hormones into the bloodstream in much the same manner as the contraceptive pills used by women. In 6 months, no cow became pregnant. However, the contra- ceptive caused the females to be permanently in heat, which in turn caused the bulls to be in a perpetual state of sexual excitement. These unintended side effects resulted in a breakdown of the close-knit elephant societies and social responsibilities, including the loss of several baby elephants because their mothers were permanently dis- tracted by as many as eight sexually excited males at one time. Although unwanted pregnancies were prevented, the social cost was too high, and this population control pro- gram was discontinued in April 1997. The second method is based on creating an immunological response: a vaccine made from the outer coating of egg cells taken from pigs produces antigens that prevent elephant eggs from recognizing elephant sperm. Initial data from 21 elephant cows has shown the vaccine to be only about 60 percent effective, a problem the researchers predict they can overcome by giving booster inoculations every 10 months. Daley, 1997 Old World rabbits (Oryctolagus cuniculus) were intro- duced successfully to Australia by British settlers in 1859, and to New Zealand a few years later (Grzimek, 1990). The rab- bits reproduced until they numbered in the hundreds of mil- lions, causing an ecological disaster in the southern half of Australia (see Fig. 3.34). Unchecked, the burgeoning rabbit population creates deserts by devouring plants, shrubs, and seedlings. The widespread destruction of vegetation seriously harmed the sheep-raising industry. A number of native Aus- tralian marsupial species have been endangered or totally eliminated through competition with, or by having their habitats destroyed by, the Old World rabbit. Competition with rabbits for burrows has caused the extinction of one species of bilbie, or rabbit-eared bandicoot (Macrotis leucura), and has caused a second species (Macrotis lagotis) to retreat to northern Australia, where it is listed as endangered. Other marsupials adversely affected by rabbits include mulgaras (Dasycercus cristicauda), hairy-nosed wombats (Lasiorhinus latifrons), long-nosed potaroos (Potorous tridactylus), and banded hare wallabys (Lagostrophus fasciatus). Livestock, including introduced sheep and cattle, struggle to compete with the rabbits for pasture. In the early 1950s, Australian government scientists released myxomatosis, a rabbit-killing virus (Kaiser, 1995; Adler, 1996a; Drollette, 1996; Seife, 1996). Although quite successful at first, myxomatosis gradually became less effec- tive, particularly in Australia’s dry rangelands. In 1991, researchers began testing a calicivirus known as rabbit hem- orrhagic disease (RHD) virus. It kills quickly and fairly pain- lessly by causing blood clots in the lungs, heart, and kidneys. In March 1995, following laboratory testing, it was injected into rabbits quarantined on Wardang Island in Spencer Gulf, South Australia. By late September, however, the virus had evaded containment (possibly by flying insects) and spread to the mainland, killing rabbits hundreds of kilometers inland. It appears to kill 80 to 95 percent of the adult rab- bits it encounters. In September 1996, the Australian gov- ernment announced a nationwide campaign to reduce the annual $472-million damage that rabbits cause to agriculture. The lethal rabbit virus was to be released at 280 sites. The expectation is that, after the calicivirus kills most of the rab- bits, it will remain in the reduced population and act as a long-term regulator of the rabbit population. The virus appears to be working exactly as animal con- trol and health officials had hoped (Drollette, 1997). The wild rabbit population has dropped by 95 percent in some regions, and native fauna and flora are already staging a comeback. Opponents fear that the virus could jump the species barrier (Anonymous, 1996). For this reason, the New Zealand Department of Agriculture decided not to intro- duce the virus pending further study (Duston, 1997). How- ever, in August 1997, officials confirmed that several dead rabbits near Cromwell in New Zealand tested positive for the rabbit calicivirus (Pennisi, 1997d). It is suspected that the virus may have been released intentionally. The virus quickly spread across hundreds of miles, making containment and eradication impossible. Density-Independent Factors Climatic factors such as rainfall, flooding, drought, and tem- perature often play a major role in limiting population growth. Fires and volcanic eruptions also affect populations without regard to their density. Most species in temperate areas are seasonal breeders, with temperature being a major factor affecting reproduction. They produce their young during the time of year that is most favorable for their survival. Most fishes, amphibians, and reptiles breed in late winter or spring. Birds breed and raise their young during the warmer months of the year. Most mammals produce their young during the same optimum period. Most bats breed in the fall, but because of delayed fertilization (see Chapter 9), the ova are not fertilized until late winter or early spring, and young are born shortly thereafter. Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 Population Dynamics 331 Months Fawning Shrubland Chaparral Deer per square mile 100 90 80 70 60 50 40 30 20 10 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov De c FIGURE 10.6 Comparison of mule deer (Odocoileus hemionus) population density through the year on poor range (chaparral) and good range (shrubland) in California. Females living in shrubland produced an average of 1.65 fawns annually, whereas does in chaparral habitat averaged 0.77 fawns annually. Over a 4-year period, shrubland does will produce an average of 6.48 fawns, whereas does in chaparral habitat will produce an average of only 3.08 fawns. Source: Data from R. D. Taber, Transactions of the 21st North American Wildlife Conference, 1956. Temperature controls the food supply for many species. A late spring freeze that kills flying insects or forces them to become dormant can have disastrous effects on insectivorous birds such as swallows and purple martins (Progne subis), as well as on bats. A freeze that kills the buds of oak, hickory, and other mast-bearing trees can create hardship for many animals in late summer, fall, and winter. For example, turkeys, squirrels, deer, bears, and others depend on acorns, hickory nuts, and other mast for their late summer food supply. Mass emigrations of some forms such as gray squirrels (Sciurus car- olinensis) have been reported during years of poor food sup- ply (Seton, 1920; Flyger, 1969; Gurnell,1987). During such mass movements, more individuals are susceptible to preda- tion, and many more than normal are struck and killed by vehicles; natural mortality probably also increases. Some species, such as black bears, often leave the protective con- fines of parks and refuges in search of food. Many are shot as nuisance bears when they wander into civilization; others become victims of hunters or motor vehicles. Members of a species living in an optimal habitat gener- ally produce more young than members of the same species liv- ing in a poor habitat. A study of mule deer (Odocoileus hemionus) in California revealed that does in good shrubland habitat produced an average of 1.65 fawns annually, whereas does in poor chaparral habitat averaged 0.77 fawns each (Taber, 1956) (Fig. 10.6). At this rate over a 4-year period, shrubland does will produce an average of 6.48 fawns, whereas does in chaparral habitat will produce only an average of 3.08 fawns. The breeding season following a poor food year also usually results in fewer young being born. Litter and clutch sizes will be smaller in many species. Depending on the severity of the food shortage, female white-tailed deer (Odocoileus virginianus), for example, may resorb a develop- ing fetus or give birth to no more than one young. Herd sizes obviously will decrease as the average production per female decreases. Rainfall, or the lack thereof, can drastically affect the breeding of certain groups, especially amphibians and water- fowl. If breeding ponds and pools dry up before the larvae and tadpoles can successfully metamorphose, annual recruit- ment may approach zero. Many nesting waterfowl are much more susceptible to predators during periods of drought. Extensive periods of rainfall and flooding also can be disas- trous for many species. The deaths of 158 manatees along Florida’s Gulf Coast between Naples and Fort Myers during a 3-month period in the spring of 1996 was caused by red tide algae. A red tide is a natural algal (Gymnodinium breve) bloom that sporadi- cally occurs along the coast and produces brevitoxin, a pow- erful neurotoxin. Unseasonably cold weather farther north brought a large concentration of manatees to Florida’s Gulf Coast, and a strong northwest wind blew a potent strain of the red tide algae deep into manatee feeding areas (Fig. 10.7). Manatees swam in contaminated water, drank it, and ate sea grass infected with it. When the toxin level got high enough, it attacked the manatees’ nervous system. One of the first nerve centers to be incapacitated was the one that regulates FIGURE 10.7 During the winter months, manatees (Trichechus manatus) congregate in the Crystal River in Florida, a sanctuary of warm water with an abun- dance of water hyacinth. Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 332 Chapter Ten the diaphragm—the major muscle used by mammals for breathing. Many manatees suffocated. Levels of brevitoxin 50 to 100 times normal were found in tissues from the lungs, stomachs, kidneys, and livers (Holden, 1996b). The result was the greatest number of manatee deaths from a single event since record keeping began in 1974. This deadly red tide, along with deaths from other natural causes, cold weather stress, boats on Florida’s waterways, and other unde- termined factors caused 415 manatee deaths in 1996, more than twice as many as the previous record of 206 deaths in 1990 (Anonymous, 1997d). The total Florida manatee pop- ulation in 1996 was 2,639. Cycles Populations of some species such as lemmings and voles show rhythmic fluctuations (Fig. 10.8). Their populations increase for several years and then fall dramatically. This cycle is repeated with some regularity. Three- or 4-year cycles are characteristic of certain species inhabiting tundra and northern boreal forests, such as lemmings (Lemmus and Dicrostonyx), voles (Microtus), ptarmigan (Lagopus), and spruce grouse (Dendragopus), as well as some of the birds and mammals that prey on these species. Some species inhabiting the northern coniferous forests, such as lynx (Lynx canadensis), hares (Lepus americanus), and ruffed grouse (Bonasa umbellus), have a longer 10-year cycle. Due to the intricacies of most food webs, anything affect- ing one species also will affect one or more additional species. When a prey species is abundant, its numberswill be reflected in increasing numbers of the predatory species (Fig. 10.9). Better-nourished females will be able to produce and suc- cessfully care for a larger number of offspring than if they Year 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 New York Percent of stems cut 100 80 60 40 20 Wisconsin Ohio FIGURE 10.8 Comparison of cyclic population fluctuations of the meadow vole (Microtus penn- sylvanicus) in Wisconsin, Ohio, and New York. Source: Data from U.S. Fish and Wildlife Service, 1971. BIO-NOTE 10.2 Invasion of the Brown Tree Snakes The U.S. territory of Guam is being overrun by brown tree snakes (Boiga irregularis), a nocturnal, tree-climbing, bird-eating, egg-gobbling, mildly poisonous reptile that can reach 3 m in length. Brown tree snakes, which origi- nally found their way to Guam some 50 years ago, encountered no natural predators and an abundant food supply. The population of these snakes has soared to an estimated 2,000,000 or more—about 10,000 per 1.6 km 2 . The snakes hang like vines from trees, fences, and power poles. Power outages caused by electricity arcing across snakes spanning power lines have become a frequent prob- lem. These snakes have eliminated Guam’s native lizards and 9 of 18 species of Guam’s native forest birds; 6 of the remaining species are endangered, and the other 3 are rare. Research is under way to control the snake popula- tion by using a strain of virus that will kill the snakes without affecting other animal life. Extensive efforts are being taken to prevent this snake from invading Hawaii, which is home to 40 percent of the nation’s endangered birds (many of which are already threatened by introduced wildlife). Snake-sniffing beagles and their handlers closely inspect every commercial and military flight from Guam. Douglas, 1997 Allen, 1998 Fritts and Rodda, 1999 were malnourished and/or emaciated (Madsen and Shine, 1992). In addition, many predators will turn their efforts to a secondary prey if their primary prey becomes scarce. Erlinge Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 Population Dynamics 333 et al. (1991) suggested that predation has a significant influ- ence on the pattern of change in a population. In ecosystems dominated by predators specializing on a single species, a cyclic pattern is promoted, whereas in ecosystems dominated by switching “generalist” predators, cyclicity is limited. Numerous studies of snowshoe (varying) hares (Lepus americanus) and a variety of predators have shown significant predator responses to hare cycles (Brand et al., 1976; Brand and Keith, 1979; Powell, 1980; Todd et al., 1981; Thompson and Colgan, 1987) (see Chapter 13). For example, snowshoe hares are the primary prey of many fisher (Martes americana) populations. Bulmer (1974, 1975) examined fur sale records in Canada and concluded that population fluctuations of fish- ers were linked to hare cycles. However, a study of fishers in Minnesota during eight winters when the snowshoe hare pop- ulation declined revealed that fishers consumed less hare as the hare population declined (33% of the diet during 1977–79, but only 3% in 1984). Consumption of small mammals (deer mice, Peromyscus; voles, Microtus, Clethrionomys; lemmings, Synaptomys; shrews, Blarina, Sorex; and moles, Condylura), however, increased from 4 to 5 percent during 1977–79, to 19 percent of the weight of the stomach contents in 1984. Fat deposits and reproduction (proportion of pregnant females, mean number of corpora lutea, and proportion of juveniles in the fisher harvest) by the fishers did not decrease during the period of the study (Kuehn, 1989). MacLulich (1937) presented the original data on cyclic fluctuations of snowshoe hare and Canadian lynx (Lynx canadensis) populations obtained from records of pelts received by the Hudson Bay Company and covering the period from 1845 to 1935 (Fig. 10.10). These data show that these cycles have been going on for as long as records have been kept in North America. It now serves as a classic study of how the cyclic fluctuations of one species (prey) appar- ently affect another species (predator). More recent studies have shown, however, that lynx are not the primary cause of periodic drops in hare populations, although they may be a contributing factor in the decline. Furthermore, Stenseth et al. (1999) found that the dynamics of lynx populations could be grouped according to three geographical regions of Canada that differed in climate and proposed that external factors such as weather influence lynx population density. In reference to snowshoe hares, Lack (1954) stated: “It is suggested that the basic cause of the cycles is the domi- nant rodent [snowshoe hare] interacting with its vegetable food to produce a predator-prey oscillation. When the pri- mary consumers decline in numbers, their bird and mammal predators become short of food, prey upon and cause the decrease of the gallinaceous birds of the same region, and themselves die of starvation and/or emigrate.” Keith (1974) and Keith and Windberg (1978) proposed an essentially identical theory to explain the 10-year snowshoe hare and grouse cycles. A similar theory was also proposed to explain the 3- to 4-year vole–predator–small game cycle in Sweden (Hornfeldt, 1978). Hares normally feed on the bark and twigs of birch, poplar, alder, and black spruce (Fig. 10.11). As hare popula- tions increase, food becomes scarcer, and the hares are forced to feed on the young shoots of these plants, which contain large amounts of toxins (see Chapter 13). The plant toxins act as antifeedants, resulting in a loss of weight and a decline in health in the hares, which causes them to be more sus- ceptible to predation (Joggia et al., 1989; Reichardt et al., 1990a, b). Thus, it appears that the chemical defenses of cer- tain plants serve as a density-dependent means of regulating hare populations, at least indirectly. While hare populations are low, the vegetation recovers, stimulating a resurgence of hare populations and initiating another cycle. It may well be a combination of limited food resources, climatic conditions, and predation—rather than any single phenomenon alone— that explains cycles in hare populations. Some researchers feel that some cycles can be explained by another type of nutrient recovery, namely, seed produc- tion (Pitelka, 1964). Many northern plants have seed cycles of approximately 3 1/2 years. These plants require this time to build up sufficient nutrient material to produce seeds. Year 1978 (a) 1980 1982 1984 1986 1988 1990 1992 Mean clutch size Field vole abundance 7 50 40 30 20 10 0 6 5 4 3 Clutch Field vole abundance 01020304050 (b) Mean clutch size 7 6 5 4 3 r = 0.87, p < 0.001 Voles (a) Average annual clutch sizes of barn owls (Tyto alba) show a cyclic pattern clearly in synchrony with the field vole (Microtus agrestis) cycle near Esk, Scotland. (b) Average barn owl clutch sizes in the Esk study area were closely correlated with spring field vole abundance. Data from Taylor, Barn Owls, 1994, Cambridge University Press. FIGURE 10.9 [...].. .Linzey: Vertebrate Biology 334 10 Population Dynamics Text © The McGraw−Hill Companies, 2003 Chapter Ten FIGURE 10. 10 (a) 140 Number (thousands) 120 Hare 100 80 Lynx 60 40 20 1845 1855 1865 1875 1885 1895 Years 1905 1915 1925 1935 (b) Population cycles for the snowshoe hare (Lepus americanus) and its major predator, the Canadian lynx (Lynx canadensis) The 9- to 1 0- year cycles are based... communities with few predators (Hansson and Henttonen, 1988) High predation pressure normally prevents small rodents from population cycling by Linzey: Vertebrate Biology 10 Population Dynamics Text © The McGraw−Hill Companies, 2003 Population Dynamics FIGURE 10. 11 Snowshoe hare (Lepus americanus) browsing intensively on an early successional shrub As the density of hare populations increases, trees... weather followed by returns to more normal conditions Source: Data from Miller, Resource Conservation and Management, 1990, Wadsworth, Inc., Belmont, CA Linzey: Vertebrate Biology 336 10 Population Dynamics Text © The McGraw−Hill Companies, 2003 Chapter Ten Review Questions 1 What defines the carrying capacity for a particular environment? How are carrying capacities for game species regulated by... environment In addition, some species may possess an inherent self-regulation (biological clock) that triggers the cyclic events Cyclic trends in local populations are poorly documented primarily because intensive, long-term data for such populations are generally lacking 16,000 12,000 8,000 4,000 0 1850 1860 1870 1880 1890 1900 1 910 Year A 60-year record of raccoon pelts taken in the same general area... stress, this chemical control system may cease functioning FIGURE 10. 12 Irruptions Enormous numbers of animals sometimes occur in a given area for brief periods of time because of certain environmental and climatic conditions Abnormally high numbers of a given species are known as irruptions and are of limited duration (Figs 10. 1b and 10. 12) Conditions leading to irruptions may involve a combination... have increased the carrying capacities for certain regions 4 Differentiate between density-dependent and density-independent factors Give examples of limiting factors that come into play when a population of mammals reaches very high density 5 List some modern techniques that are being used to control exploding vertebrate populations 6 The release of the rabbit hemorrhagic disease virus in Australia... 1978 A mid-continental irruption of Canada lynx, 1962–1963 Prairie Naturalist 10: 71–80 Morris, D W., Z Abramsky, B J Fox, and M R Willig 1989 Patterns in the Structure of Mammalian Communities Lubbock: Texas Tech University Press Slobodkin, L B 1980 Growth and Regulation of Animal Populations New York: Dover Publications Thompson, H V., and C M King (eds.) 1994 The European Rabbit: History and Biology. .. bacterium Pasturella tularensis, was found among these animals during the subsequent decline and may have been a (density-dependent) factor in the population decline Another factor in the decline of high populations may be the exhaustion of the adrenal gland (see the Endocrine System section in Chapter 9) brought on by stress caused by the high level of intraspecific interaction (Christian, 1950, 1959, 1963;... montane vole (Microtus montanus) This spectacular irruption occurred in 1906–1908 in Nevada and California (Piper, 1909) In some areas, estimated population density exceeded 25,000 voles/ha Approximately 10, 000 ha 24,000 20,000 Number of raccoons taken keeping their densities low, especially during winter and early spring (Hansson, 1979; Erlinge et al., 1983; Erlinge, 1987) Although many possible explanations,... of a Successful Colonizer New York: Oxford University Press Wildlife Conservation May–June 1996 issue Entire issue devoted to cats—bobcats, lynx, ocelots, jaguars, cougars, tigers, lions, cheetahs, etc Vertebrate Internet Visit the zoology website at http://www.mhhe.com to find live Internet links for each of the references listed below 1 Terrestrial Mammals of the Arctic Information from a text on Arctic . in the years indicated. FIGURE 10. 10 Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 Population Dynamics 335 FIGURE 10. 11 Snowshoe hare (Lepus americanus). and the chances of an epi- zootic such as fowl cholera are increased. Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 328 Chapter Ten et al., 1990) sperm receptor Linzey: Vertebrate Biology 10. Population Dynamics Text © The McGraw−Hill Companies, 2003 330 Chapter Ten sites there and preventing fertilization (Daley, 1997). In lab- oratory tests,