

Passenger Pigeons and Their Extinction

Written by

Bruce A. Wright

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PUBLISHED BY:

Bruce Wright on Smashwords

Passenger Pigeons and Their Extinction

Copyright © 2013 by Bruce A. Wright

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TABLE OF CONTENTS

Introduction...3

Columbids...4

Distribution...4

Feathers, flight and migration...5

Social behavior...8

Reproduction, nests, eggs and chicks...8

Population size...10

Food, feeding ecology and landscape ecology...11

Mortality factors and extinction...13

Loss of habitat...13

Starvation...13

Competition...13

Predation ...14

Hunting...15

Inbreeding suppression...16

Contaminants...16

An experimental disease model...16

Abstract...17

Introduction...17

Methods...18

Results...19

Discussion...20

Passenger pigeon proxy...22

So, was it disease?...23

Timing of spread of trichomoniasis...25

Conclusions...26

Columbid conservation...27

Reoccurring exposure to T. gallinae...27

Globalization and the spread of diseases...28

South American eared dove extinction experiment...28

Global warming, climate change and Columbids...28

Acknowledgements...29

References...29

Glossary...34

Index...39

About the author...42

When I was in high school, I practiced falconry. It would take me nearly 40 years later that I figured out what caused the death of my red-tailed hawk. The same disease that killed my hawk was the primary cause for the extinction of passenger pigeons.

Bruce Wright 2010

In the autumn of 1813, I left my house at Henderson, on the banks of the Ohio, on my way to Louisville. In passing over the Barrens a few miles beyond Hardensburgh, I observed the pigeons flying from northeast to southwest, in greater numbers than I thought I had ever seen them before, and feeling an inclination to count the flocks that might pass within the reach of my eye in one hour, I dismounted, seated myself on an eminence and began to mark with my pencil, making a dot for every flock that passed. In a short time, finding the task which I had undertaken impracticable, as the birds poured in countless multitudes, I rose, and counting the dots then put down, found that one hundred and sixty-three had been made in twenty-one minutes. I traveled on, and still met more the further I proceeded. The air was literally filled with pigeons; the light

of noonday was obscured as by an eclipse; the dung fell in spots, not unlike melting flakes of snow; and the continued buzz of wings had a tendency to lull my senses to repose.

John James Audubon, Ornithological Biography, I (1833)

I always thought there was more to explaining the extinction of passenger pigeons than hunting or loss of habitat. I thought disease could have been important.

Richard Kocan (2005)

INTRODUCTION

No other human-caused extinction event has been as spectacular and as pervasive in the literature as that of the passenger pigeon (Ectopistes migratorius). However, documentation of this event relies on personal journals, newspaper and magazine articles, and a few volumes that summarize some of the events after the passenger pigeons were extinct. The prevalent message from most of the articles is that passenger pigeons, once the most abundant bird on the planet, went extinct because humans pressed forward with their desire to conquer all that was before them, in this case, the New World, and without considering the consequences. Passenger pigeons were a keystone species is what is now known as the eastern United States and portions of eastern Canada and Mexico; they drove the ecosystem, were pursued by a huge suite of predators, including Native Americans, and were of such numbers, 3-5 billion birds, they were a dominating force which must have manipulated their ecosystem with a randomness as variable as their vast and sky-blackening migrations (see Wilson 1812). Their migrations of millions of birds were necessary as they pursued berries, and fall crops of mast, mostly beechnuts (Fagus grandifolia) and acorns (Quercus spp.). Passenger pigeons were defined by their movements throughout the eastern section of North America; they spent much of their time in search of patches of mast.

Observers of the demise of passenger pigeons noted loss of habitat and over-harvest (hunting) as readily identified factors leading to their extinction. Audubon (1844) mentioned starvation and predation as possible factors. Less obvious population factors are contaminants, competition, and disease. I found evidence from reports that cast some doubt on all these factors as causes of the extinction of passenger pigeons, except disease for which I found no contradictory evidence. I think that an introduced disease caused the extinction of passenger pigeons, even if other factors exacerbated the population crash on various scales. In this book I will present an overview of what we know about passenger pigeons, and I will consider possible consequences resulting in the extinction of these interesting birds. I will provide evidence and present a disease model that helps explain how disease was the preeminent cause that led to the rapid and complete elimination of passenger pigeons in the short 30 year period at the end of the 19th century.

COLUMBIDS

Pigeons and doves, including passenger pigeons, are classified in the Columbiformes Order and the Columbidae Family, but they are often referred to as columbids. Worldwide there are 308 species in the order Columbiformes, and in North America there are 14 species and 6 genera. The columbid species most commonly seen around human habitation and in cities is usually the rock dove ( _Columba livia_ _)_ , also called the rock pigeon, domestic pigeon or feral pigeon. I will discuss this species throughout the book as it relates to the passenger pigeon. The columbids are stout-bodied birds with short necks and short slender bills with a fleshy cere. The North America native living columbids are the morning dove (Zenaida macroura), white-winged dove (Zenaida asiatica), white-tipped dove (Leptotila verreauxi), Key West quail dove (Geotrygon chrysia), Inca dove (Columbina inca), ruddy ground-dove (Columbina talpacoti), common ground-dove (Columbina passerina), band-tailed pigeons (Columba fasciata), red-billed pigeon (Columba flavirostris) and white-crowned pigeon (Columba leucocephala). The introduced species are rock dove, Eurasian collared-dove (Streptopelia decaocto), ringed turtle-dove (Streptopelia risoria) and spotted dove (Streptopelia chinensis) (Sibley 2000). All the North American dove and pigeons have strong flight, useful for escaping predators, but the passenger pigeon was among the strongest fliers.

DISTRIBUTION

The passenger pigeon occurred generally east of the Rocky Mountains and north to about the 53 degrees latitude and to southern Texas. There were some sightings as far north as Yukon Territory in Canada and west to Nevada (Schorger 1955, Townsend 1932). However, misidentifications could have easily explained the most westerly observations where band-tailed pigeons and morning dove occur. Band-tailed pigeons generally occur west of the Rocky Mountains and inhabit a niche that has similar characteristics to that of the passenger pigeon. The significance of this and the relationship between passenger pigeons and band-tailed pigeons will be discussed later in the book.

Passenger pigeon breeding range was primarily the eastern deciduous forests where nesting trees and mast were readily available. However, pairs and small groups nested throughout their range (Townsend 1932) indicating passenger pigeons were not dependent upon mass, high-density nesting situations. This is an important to know because some passenger pigeons authors conclude that demise of passenger pigeons was a result of disturbance of mass nestings.

Passenger pigeons generally migrated north in the summer and early fall after nesting season and south during the colder months. Severe winters may have been responsible for the few observations of passenger pigeons in northern Mexico, the Caribbean and Cuba.

Passenger pigeon distribution may have been greater prior to the arrival of people to North America. As far back as 100,000 years ago, as revealed from fossil records, passenger pigeons inhabited North America and occurred as far west as California (Chandler 1982, Harris 1992, Howard 1937, 1971, Majors 1993). The changes in their distribution and relationship to other columbids (e.g. band-tailed pigeons) prior to 1600 are not understood.

FEATHERS, FLIGHT AND MIGRATION

G enerally, birds migrate to find food and water, a safe place to nest and avoid predation. Many species will migrate to far northern areas where the severe winters have reduced the predator population. Passenger pigeons likely benefited by flying north by leaving many of their less swift predators to the south, but they also benefited by finding food resources, in the form of mast, that were again available when the snow melted. This hypothesis is supported because they continued to migrate north, presumably in search of food, after nesting season and before the fall migration south. Passenger pigeons had evolved into one of the great migrating species, as this section will reveal.

Passenger pigeons look much like a large mourning dove; they have a long pointed tail about 8 inches long (20 cm) with a total body length of about 16 inches (40cm) (Ridgway 1916) and weigh about 11 ounces (300 grams) (Eaton 1910). Adult males are more colorful than the females and they had iridescent feathers on the back and sides of their neck. Their throat to lower belly colors changed from pinkish to tan to white while their back and tail were dark. The wings were long and pointed at about 8 inches (20 cm) each and were spotted much like seen on mourning dove (Whitman 1919).

The feathers and wings of passenger pigeons, as with most birds, allow birds the ability to fly. The advantages are obvious; birds can travel great distance with greater efficiency over walking and swimming, so they can more easily locate food, good habitat, and avoid predation. The passenger pigeon was well suited for flight and especially long-distance migrations.

Feathers wear out and old feathers must periodically be replaced with new feathers. This is referred to as the molt. Some birds, such as waterfowl, can find food and refugia on lakes, rivers and oceans, so they aren't dependent upon flight for their survival. Waterfowl generally molt all the flight feathers in a short time frame during which they are flightless. Passenger pigeons, and most bird species, cannot afford to lose their ability to fly, even for a short period. They would likely starve and/or be taken by predators. The birds that must maintain their flight abilities molt over an extended period, usually losing one or two flight feathers (primaries and/or secondaries) on each wing at a time. Some larger bird species, such as eagles, take two years to molt their primary flight feathers; passenger pigeons molted their feathers every year (see Forbush 1927, Pyle 1997) and they retained their flight abilities during the molt.

Flight requires lift and for birds lift is achieved via a foil. The cross-section of a bird's wing reveals the air foil with convex upper and concave lower parts of the wing. As a bird moves through the air, the air moves faster over the upper part of the wing creating a lower pressure than the under (concave) part of the wing. This creates lift. The lift can be increased if the angle of attack of the wing (foil) or speed is increased. Resistance or drag increases with increased speed, angle of attack or turbulence. Passenger pigeons weighed only about 250-350 grams (9-12 ounces) (Eaton 1910, Foster 1772) making them light and small enough to promote fast and efficient flight. The optimum angle of attack is about 3-5 degrees; a greater angle of attack can cause turbulence and stalling resulting in loss of lift. Turbulence can be reduced by being streamlined, and passenger pigeons are very streamlined or aerodynamic. This is a simplistic description of flight; more complex explanations of aerodynamics are needed to understand powered flight, takeoffs, landing, and gliding, use of thermals and moving air, flying through downdrafts and in formation. But when one looks at a passenger pigeon one can detect they are aerodynamic and fast, efficient fliers, and probably more so than any of the other columbids. Morning dove level flight has been measured at about 55 miles/hr (90km/hr) (Bastin 1952). Passenger pigeons likely exceeded these speeds and flew over 60 miles/hr (100km/hr) (Schorger 1955) and regularly flew more than 100 miles (160 km) per day (see Wilson 1812). Passenger pigeons did not emit the whistling sound heard when mourning dove fly, but during their mass migrations their great numbers created sounds similar to wind through a vessel's rigging and especially when landing (Audubon 1831, see also Pokagon 1895). As passenger pigeons landed they sometimes made a clapping sound and the females sometimes emitted a soft clucking sound.

Passenger pigeons walked like the more familiar rock dove we see in towns and cities today; they are not well adapted to walk long distances (see Bryant 1913, Craig 1911 and Whitman 1919). After landing, passenger pigeons might have walked short distances to feed and drink. However, they used their quick and maneuverable flight to avoid predators and travel great distances to find the food and water.

The eastern North American forests are a mosaic of patches of mast-producing trees. Predation upon the mast is controlled by trees periodically producing more seeds than the seed predators can consume. Some of the most important predators are invertebrates (such as weevils). Trees were successful in increasing their overall productivity by periodically overwhelming the invertebrate predators with more seed than could be infected and eaten (Minckler and Janes 1965 and Silvertown 1980). Passenger pigeons had evolved to utilize these patches of super-abundant food; they were among the best of flyers and well suited to locate and consume dense patches of mast.

The predominant mast-producing trees, especially beech, chestnut and oak, produced high-density mast in what is perceived by passenger pigeons as random and non-predictable patches in a landscape matrix of hardwood and pine forests. Accordingly, passenger pigeon mast hunting strategy depended upon somewhat random and nomadic search patterns. These nomadic migrations generally resulted in most passenger pigeon population to the central sections of its range to nest. After breeding season, in late summer and fall, passenger pigeons used more northern sections of their range where there was an abundance of seeds, berries and grapes. The migrations then led south to the wintering range. The vast numbers of passenger pigeons forced the nomadic movements; once a patch of mast was discovered it was quickly consumed and the birds had to locate the next patch of abundant food. Later in the book I will discuss later how this hop-scotch pattern of migration resulted in mixing and exposure to thousands to millions of individual birds and increased their risk of transmission of diseases.

Timing of the migration was likely driven by changes in day length and storm events. North migrations from wintering regions in the south probably began in January to February and passenger pigeons were arriving on their breeding grounds from February through April (Schorger 1955). Post-breeding migrations were generally north and began in May (see Atkinson 1905 and Cooke 1888). August through October was the time period for the passenger pigeon fall migration to the south, but the exact time may have been determined by snowfall covering their food as much as the shortening length of the day (see Scherer 1939, Schorger 1955).

Passenger pigeon nomadic and somewhat random migration patterns resulted in their occasionally migrating across the Great Lakes, following shorelines and other topographical features. However, they usually crossed at narrow points (Mitchell 1935). The migrations sometimes numbered in the millions and could blacken the sky and the take days to pass, but the flocks may have been a converging of smaller groups that later broke up into smaller groups. Topography may have been important for developing the huge migrating flocks.

Individuals within a population have individual behaviors; this variability allows for the population to survive change and factors that may otherwise diminish their numbers and/or cause extinctions. I will discuss in the chapter on nesting that most passenger pigeons nested in large colonies that numbered sometimes in the hundreds of millions, but sometimes they nested in small isolated groups. There are obvious advantages and disadvantageous to these nesting strategies I will discuss later, but individual behaviors were also seen in the way passenger pigeons migrated and flew. Some birds flew close to the ground. This was probably advantageous when flying into a head wind, but people learned some of the low-flying birds could be snatched right out of the air with a net or knocked down with a pole, an obvious problem for those birds.

Flocks sometimes appeared as a broad front; these were usually birds that were feeding. As they progressed across the landscape, the areas where they had alit and fed were devoid of mast, so the individual competition for food probably demanded they fly in a broad front instead of in a column. When seen in long and winding columns (Pokagon 1895), passenger pigeons were more likely traveling longer distances, and sometimes layers of migrating birds filled the sky. These were the migrations that Audubon (1832) and others reported that resulted in blackening the sky and reducing the sun's light to a level more like 1/2 hour after sunset. These great flocks must have been an amazing sight; to most people they probably appeared boundless.

SOCIAL AND OTHER BEHAVIORS

Passenger pigeons drank like other columbids drink; they suck some water in their bills and swallow, not needing to toss their heads back as seen with some bird species. They would sometimes land on lakes or ponds, as if emulating a duck, and drink while sitting, except their wings would be held open (Linkletter 1920). Then, with a quick beat of their wings the birds would fly off. Drinking from the center, as opposed to a shore, of a lake could have been a predator-avoidance strategy, or the lakeshore may have already been occupied by hoards of other passenger pigeons. Kalm (1911) and Pokagon (1895) noted that passenger pigeons sometimes sought and drank brackish water, perhaps to replace needed minerals. Passenger pigeons bathed similar to other columbids, but likely sharing the bathing water with many other passenger pigeons. Sharing watering holes, and with such great numbers of birds, may have been important for transmission of diseases, something I will discuss later in the book.

Communal feeding was the norm, and flocks of thousands of birds would hop-scotch across the landscape searching for mast, landing, and feeding as other flocks passed overhead also searching for food. When more desirable food was located, passenger pigeons would regurgitate the food already in their crops and eat the more desirable food (Mershon 1907, Whitman 1919). The regurgitated food, if consumed by other pigeons, would have been a mechanism for transmission of disease.

Passenger pigeons were capable of a variety of vocalizations, but their vast numbers, wildly beating wings and vocalizations were reported to create a roar as if a storm were approaching (see Behr 1911, Craig 1911, 1913). Passenger pigeons were among the most gregarious of birds, sharing this quality with the Australian flock pigeon (Phaps histrionica) and South American eared dove (Zenaida auriculata) (Bucher 1982) which I will discuss later as a model for future disease spread. Flights of these other species can also be quite noisy.

If roost sites were used for extended periods, the amount of droppings could grow to be many inches (centimeters) thick (Zeisberger 1910) and kill some plants and trees. The feces could be source for spreading disease. The dung may have been an important resource for some invertebrates.

REPRODUCTION, NESTS, EGGS and CHICKS

Passenger pigeons nested in the eastern deciduous forests, usually beech forests where the mast was revealed with the melting snow in spring. Some sites were used repeatedly, but this must have been due to a combination of factors, such as available food and reduced predation, that allowed for good nesting successes (see Bishop 1886, Thompson 1921). Passenger pigeons often nested (or roosted) in very high densities, sometimes breaking branches due to the weight of so many birds. Reports of birds falling from the trees may have been confused with birds dying of disease (discussed later) and birds falling to the ground when a branch broke under their weight. Healthy passenger pigeons would have easily recovered and flew to another branch.

Passenger pigeons bred in their first year and likely attempted to breed annually. Both parents were needed to raise the single chick, and passenger pigeons were monogamous (Blockstein and Westmoreland 1993), but we don't know if passenger pigeon pairs mated for life. Craig (1911) describes, before copulation, passenger pigeons display with a brief nuptial flight and continue displaying on a branch, which includes some soft sounds. Mutual preening and billing were part of the pre-nuptial behaviors (see Scherer 1939). When ready, the male mounted the female and copulated.

During the nuptial activities the pair built their nest (see Herman 1948), usually in early April, and this would occur at the same time throughout a colony. The synchrony of breeding and nesting was astounding (see Pokagon 1895) where birds are so preoccupied with the drive to reproduce they could be gathered by hand from the ground and in midair. The nest, a simple affair usually in the crotch of a tree's branches, was usually constructed in 2-3 days, but sometimes as long as 6 days (Herman 1948) and the single white egg was laid on the day after the nest construction ended. Band-tailed pigeons, the other North American mast-consuming pigeon, also lay a single egg (Blockstein and Westmoreland 1993). Hundreds of nests could be constructed in a single tree by hundreds of pairs of passenger pigeons (Bryant 1913). The nests were constructed of about 100 small twigs and were about 6 inches (15 cm) across and 2 1/2 inches (6 cm) high (Gibbs 1894, Thoreau 1905). The nest was frail enough the egg and chick could be seen through the nest from below (Wilson 1812), although this may have allowed feces and parasites to drop through and maintain better nest sanitation. Despite their flimsy construction, the used nests often remained in the trees for years. There is no evidence that passenger pigeons produced a second clutch, although some post-nesting flocks were comprised wholly of juvenile birds. This suggests double-clutching could have occurred (see Dury 1910, Gibbs 1894, Goodwin 1983, Schorger 1955, Thompson 1921, Wilson 1812), but probably reflects on the different timing of the adults and young abandoned the nest.

Observers and consumers of passenger pigeons were drawn to the nesting colonies that were usually long and narrow and may have covered thousands of acres (ha) and included millions of birds (see Roney 1879, Schorger 1937). But passenger pigeons also nested in small groups and pairs independent of the giant nesting colonies, an indication of the variability within the population.

Incubation of the egg began immediately upon being laid. The male and female took turns incubating and within 13 days the egg hatched. The newly-hatched young were similar to other columbids, altricial, naked but for a little down (see Clark 1918, Townsend 1932), not able to walk and totally dependent upon their parents for food, warmth and protection. Growth of the young pigeons was very fast (Pace et al. 1952, Hegde 1972) as they were fed pigeon milk, or crop milk, a nutritious curdlike secretion (see Desmeth 1980 and Patel 1936). The young would insert its bill deep into the adults' mouth and crop to get its meal of crop milk.

About 13 to 15 days after hatching the adults abandoned the nest. Within 14 days of hatching the chick was fat and weighed as much as the adults (see French 1919). Within a few days they could fly and the young birds began searching the woods for mast, often in flocks made up entirely of young of the year (Wilson 1812).

POPULATION SIZE

It's not easy to determine the numbers of animals in a population. Complete counts require the enumeration of every individual in a population. The numbers of ducks on a lake might be easier to count than most populations, unless some of the ducks are divers. Counting highly migratory species, such as passenger pigeons is problematic. It's highly unlikely the estimates of passenger pigeon numbers is within even 20% of their actual numbers; their numbers were most likely underestimated.

Another way to enumerate wildlife populations is to use an incomplete count or index and extrapolate those numbers to an entire population. For example, a biologist could determine an approximate number of clams in a bay by laying out randomly placed quadrats, counting the number of clams in each quadrate and extrapolating for the entire area. Assumptions must be made when using this technique. An important assumption, which applies to highly migratory species, is that no target animals are leaving or entering the count area. That's an easy assumption to make when counting clams in a bay, but counting passenger pigeons in an area would be very difficult. Ecologists may use one or many techniques to determine population numbers such as strip or transect censuses, roadside counts, flushing counts and use a variety of indices of relative numbers. For example, some passenger pigeon observers noted relative changes in numbers of nesting birds or nests. This technique yielded very useful data, and may indicate if the population was increasing or decreasing.

Ecologists may employ a number of other more technical methods to count wildlife and then use mathematical equations to determine the populations. The Lincoln-Petersen Estimate (Lincoln 1930, Petersen 1896) requires animals be captured, marked and released back in to the population and the ratio of marked to unmarked animals be determined. Several assumptions must be met for this method to work; the mortality of marked and unmarked animals is the same, marked animals don't lose their identifying marks, both marked and unmarked animals are recaptured at the same rate and it is a closed system with no new recruitment and migrations. It would be difficult to meet these assumptions with passenger pigeons, even today. The Jolly-Seber method (Jolly 1963, Seber 1973) allows for an open system, animals can enter and leave the population, but the difficulty comes when keeping track of individuals over an extended period, and with 3-5 billion individuals, this method would be impossible to deploy.

The observers of the massive passenger pigeon populations employed a method similar to what today is described as the minimum number alive (MNA) method (see Krebs 1966) where the number of animals are enumerated over a period of time and then estimated over the entire population. For example, Krebs used remotely operated cameras to determine the size of a population of meadow mice (Microtus spp.), and he determined the number of mice correlated to the number of runways (paths) in the study area. Knowing this, one could count the number of runways, use these numbers as an index of microtine abundance, and correlate the indices to predator abundance (see Wright 1979), seed abundance, genetic variability, etc.

Wilson (1812) employed the MNA method, although his techniques were crude by today's standards, when he counted a portion of the passenger pigeons in a massive flight in Kentucky. Wilson estimated the area of the migration as a rate with a width of 1 mile (1.6km), rate of passing pigeons of 1 mile (1.6 km) per minute, for about 5 hours and assumed three pigeon per square yard (meter). His calculation of 2.2 billion birds is consistent with Audubon's (1831) calculation of a flight having 1.1 billions pigeons and King (1866) whose 14 hour flight was later calculated by Schorger (1955) at 3.7 billion passenger pigeons. These estimates were minimum number of alive birds. Unfortunately, these calculations do not meet one of the basic assumptions of enumerating animal populations, that of a closed system. There could have been 20 concurrent migrations of passenger pigeons; we have no way of knowing. Accordingly, the population estimates of 3-5 billion bird estimates, which depended upon the data and methods described above, are more likely than not to be underestimates.

Another technique for estimating wildlife populations is the Frequency of Capture Method (Eberhardt 1969) in which one enumerates each animal in a population each time it is captured during a period of time and the data are graphed giving an estimate of the number of animals not trapped and an estimated total population. A related technique, DeLury Method, plot the number of animals removed from a population (killed) relative to the hunting effort (DeLury 1954). One could have used the number of pigeons delivered to market, for which there are some historical data, as related to hunting effort. Unfortunately, several assumption are not satisfied; the hunting effort was not consistent and increased as the number of pigeons dropped, the demand increased and hunting effort increased.

The descriptions of the vast numbers of birds are as meaningful as the estimated numbers; millions upon millions (Wood 1865), darkened the sky (Wilson 1812), countless (Biggar 1922). I have seen millions upon millions of birds coming and going at seabird colonies, and they didn't 'blacken the sky,' so by my estimate the number of passenger pigeons was not simply a number such as 3 billion or 5 billion, but a population unsurpassed today in which intermingling and contact, both directly and indirectly, set the passenger pigeon up as a perfect candidate for the spread of a pathogenic disease. I will discuss more about this in the Experimental Disease Model chapter.

FOOD, FEEDING ECOLOGY and LANDSCAPE ECOLOGY

Passenger pigeons likely used a wide variety of available habitat, but they were dependent upon forests for the majority of their food resources, and nesting and roosting sites. The deciduous forests provided the bulk of the mast and their primary food sources, but swamps, alders (Alnus spp.) and pines (Pinus spp.) provided important and often used safe rooting sites (Schorger 1955) particularly in winter. Within their landscape, the matrix, or predominate habitat component, was forested land. The patches included open meadows and agricultural areas, both of which were used for foraging, but the pigeons returned to the forests to roost.

Mast production likely evolved to overwhelm seed predators and allow for enough seed for new tree growth. However, environmental conditions, such as wet or dry periods, controlled the timing and patchiness of the mast. Passenger pigeons may have been aware of these environmental cues, or they more likely wandered over vast tracts of landscape in search of mast and other cohorts that had already found abundant food patches. Roosting sites were likely used as information centers; birds that had been unsuccessful would follow birds heading out from a roost, in a more direct flight which could reveal good foraging areas (Bucher 1992).

Even within the forests, geographic and geological variability controlled sun exposure (south-facing slopes), water drainage, soil types, etc. which provided habitat types that favored some tree species over others. Passenger pigeons likely learned to search habitat types relative to the season to increase their success of finding productive food patches. Sometimes the patches located contained other types of food important to passenger pigeons.

Mast was favored all year, but was particularly important during the fall, and included acorns, beechnuts and chestnuts (Castanea dentata). Tree, bush and grass seeds, grains and wild rice (Zinzania aquatica) were also consumed (Mitchell 1935). Blueberries (Vaccinium spp.) and other berries (see Dury 1910, Kalm 1911, Macoun and Macoun 1909, Wheaton 1874, Wilson 1934), earthworms (Bendire 1892), caterpillars (Peabody 1841) and snails (Kalm 1911,

Knapp 1874, Pokagon 1895) and other invertebrates were also important food items. Some of these items were collected from the trees, much as band-tailed pigeons sometimes forage for acorns today, but most were collected from the ground (see Bryant 1913).

Passenger pigeons learned to forage from agricultural fields where they ate buckwheat (Fagopyrum spp.), wheat (Triticum spp.), barley (Hordeum vulgare), rye (Hordeum sp.), oats (Avena spp.), and corn (Zea mays). The pigeons even learned to forage in the fields after they were planted which could result in a damaged crop and reduced production for farmers.

Birds don't have teeth but if they eat hard foods such as mast and seeds they need to grind these foods before being digested. Birds eat gravel which, in the ventriculus or gizzard, a muscular organ, grinds hard foods using the gravel to aid in the grinding process. Passenger pigeons likely found much of their gravel along streams, rivers and lakes; they needed to visit these sites regularly to replace supplies for their ventriculus.

Competition for mast in large foraging flocks of thousands to millions of passenger pigeons must have been intense. The birds were likely in a race to fill their crops as fast as possible after which they would seek protection in the trees. Columbids generally have large crops which provide the advantage of reducing the time exposed to predation during foraging and increasing the time in the relative protection of roosting trees. The passenger pigeon crop could be filled so that it approached the size of an orange or at least 2 1/2 inches (6cm) in diameter (Dury 1910). Another advantage of a large crop is it allowed passenger pigeons to forage far from their nest and return with enough food to provide for themselves and their chick.

During the competitive foraging bouts, passenger pigeons were thorough in their search for mast, overturning leaves and foliage and snow, if present (see Wheaton 1882 and Pokagon 1895). Other seed and mast consumers such as squirrels must have suffered food shortages after the passing of feeding passenger pigeons. Passenger pigeons may have even returned to productive foraging area year after year or in the spring following a productive fall (Kalm 1911, Schorger 1955). Imagine what the local seed and mast-eating wildlife would have suffered with the return of the huge flocks of passenger pigeons.

MORTALITY FACTORS AND EXTINCTION

Passenger pigeons could live to be 17-29 years in captivity (see Deane 1911, Shufeldt 1915), but they likely lived only 12-14 years in the wild. This is impressive considering the suite of predators pursuing passenger pigeons, and their relatively migratory and energy-intense lifestyle demands. Keep in mind passenger pigeons' long lives as we now explore possible factors that may have resulted in individuals dying and their ultimate extinction.

I don't dispute the argument most often presented, passenger pigeons died and became extinct due to humans. I do dispute most of the hypotheses for passenger pigeons' extinction and provide evidence that explains the initial population decline and the ultimate extinction of even isolated groups of passenger pigeons (see Blockstein and Tordoff 1985, Bucher 1992). I present the evidence below.

Was it habitat loss?

It is reasonable that passenger pigeon populations might have declined due to loss of habitat resulting in loss of nesting habitat, roosting trees, refugia from predators and weather, and food from mast (acorns, beechnuts, chestnuts, and other berries and seeds). However, the hypothesis that a simple reduction of a percentage of trees might result in the extinction seems unfounded since vast areas of mast producing plants and nesting trees still existed throughout the passenger pigeons' range through the late 1800s (French 1919, Blockstein and Tordoff 1985). Forbush (1917) describes the vast tracts of trees and coppice mast that would, "...furnish great armies of pigeons with food....we cannot attribute their extermination to the destruction of the forest." Reduction of the forests, however, would have had an effect on passenger pigeons; there is an overwhelming amount of literature of species' declines and extinctions brought about by habitat destruction. When a species suffers diminished available and suitable habitat they have few options, unless they can move to suitable habitat. Passenger pigeons were among the best at relocating to suitable habitat, and even years after they disappeared forever, there were still vast tracts of suitable habitat (see Blockstein and Tordoff 1985, Forbush 1927, Schorger 1955).

Was it food?

During the passenger pigeon's greatest decline, between 1870 and 1890, adequate forest areas and mast-producing trees still existed in their eastern range (Blockstein and Tordoff 1985). The early timber industry focused on conifers, and the areas that were cleared for farming still provided food for pigeons. Passenger pigeons regularly raided grain fields and used the remaining forests. The production of grains (corn and wheat) and the mast from the remaining forests could have supported a large passenger pigeon population; food was not the limiting factor.

Was it competition?

Neumann (1985) argues that the passenger pigeon population was in competition with Native Americans for mast and that the pigeon numbers increased when Native Americans populations decreased. This is inconsistent with early accounts by John Josselyn, in his "Two Voyages to New England" published in 1672 (Forbush 1917), and ship master Jaques Cartier reported in 1534 (Biggar 1922, Fischer 1913). They described the vast numbers of the pigeons at a time when Native American populations were still high. Furthermore, the reduction of Native American populations and competition would have helped bolster the passenger pigeon food base and population, which didn't happen.

Was it Predation?

Audubon (1844) reported hearing and observing wolves, foxes, lynxes, cougars, bears, raccoons, opossums, skunks, eagles, hawks of different species, and vultures feeding on passenger pigeons. The number of individual predators and predator species preying upon passenger pigeons must have been great, and Boutin (1992) believed predation was a limiting factor but no greater than hunting. Passenger pigeons were capable of predator avoidance; they could fly fast and far. When most vulnerable, during nesting, their great numbers overwhelmed the predation effect (Blockstein and Tordoff 1985).

Passenger pigeons displayed many behaviors to avoid being preyed upon. Staying in large flocks reduced the chances any one bird would be taken by a predator. This strategy likely also confused and distracted predators thus reducing the predator's effectiveness. Passenger pigeons had sentinels which kept watch over foraging flocks (Bethune 1902, Pokagon 1895) and would alert the feeding pigeons. This technique is seen in many other flocking bird species today.

As the rate of passenger pigeon population decline increased; the predator field remained relatively abundant, thereby exerting a greater relative toll on the remaining passenger pigeon population—a concept referred to as depensation (rather than compensation). Such a mechanism can be sensitive to the degree of prey aggregation and other related factors. It is possible that passenger pigeons became trapped by a (relatively) increasing predator field as they contended with epidemic disease, habitat loss, hunting, and other hypothesized factors. The interaction and combination of these effects might have caused the disappearance of the last surviving wild birds (Blockstein and Tordoff 1985). The predation effect might have been magnified in areas where passenger pigeons sought refuge from human predation.

Fischer (1913) and Wright (1913) noted (around 1870) that after the passenger pigeons left their roosts to forage for the day, large quantities of dead birds were discovered on the ground and subsequently collected. This behavior of dropping from the trees and being available for collection was observed for band-tailed pigeons by me at the Las Padres National Forest study site. Fischer (1913) believed the passenger pigeons died due to the vast numbers of birds inflicting injuries to their own kind. I believe this indicates an explanation other than human predation to explain the sick and dying birds falling from the trees; I believe the increased number of birds (passenger pigeons and band-tailed pigeons) found dead on the ground at roosting sites was caused by mortality from T. gallinae infection.

Deaths from predation may have been substantial, but also only a small percentage of the population. More passenger pigeons likely died from weather-related deaths each year. Some passenger pigeon migration events took the birds across open water such as the Great Lakes where birds were sometimes lost in storms or fog. (see McDougall 1905, Mershon 1907, Schorger 1955, Wilson 1934). Predation from raptors may have declined as the predatory birds consumed infected sick and dead passenger pigeons and were infected and died from T. gallinae infection (frounce) themselves. Research on changes in predatory birds' populations during the mid and late 1800s may reveal the concurrent decline in raptors.

Was it hunting?

When common property is exploited competitively, and there is unlimited or open access to the property, the resource can be reduced quickly, even to the point of extinction (Conrad 1999). Open access has been described by Gordon (1954) and Smith (1969) for common property fisheries; by Wilen (1976) for North Pacific fur seals; and by Bjørndal and Conrad (1987) for North Sea herring. In these cases, competition for a common property resource supersedes conservation incentives because others will harvest what is conserved for conservation maintenance. Passenger pigeons were common property, and they were harvested at the highest level the infrastructure could accommodate, and may even have been a sustainable level. As passenger pigeon numbers decreased and/or demand increased, pigeons became more valuable and commanded higher prices. But was this increasing level of harvest enough to cause the observed declines?

Forbush (1917) described the take of passenger pigeons to be in the millions of birds; nets were strung among the trees and pigeons were taken like fish from the sea. The pigeons nested in mass which was attractive to commercial hunting operators. Wilson (1812) described a mass nesting migration in Wisconsin that contained about 2,200,000,000 birds; Schorger (1937) described nesting colonies exceeding 135,000,000 birds and covering at least 850 square miles (2,200 square km); Wilson (1812) reported harvests of 1,200,000 birds; and Fischer (1913) calculated the average annual harvest for the years 1866-1876 including pigeons used to feed the hunting camps, "Natives," and farmers was 12,000,000 birds. These are large numerical harvests but less that 0.5% of the total estimated passenger pigeon population. There were billions of passenger pigeons, which probably could produce an annual sustainable yield in the hundreds of millions, even considering the effects of natural predation. If passenger pigeons did typically depend on aggregation behaviors, however, efficient hunting might have caused strong effects at low population levels. That is to say, their distributional range would simply collapse as the remaining individuals continued to aggregate, thus providing continuous easy capture at very low population levels.

Nest abandonment was thought to be an important result of the hunting pressure, and Blockstein and Tordoff (1985) theorize the mass nesting were essential and were compromised by human (Native and non-native Americans) hunting activities. Brewster (1889) described pre-nesting birds moving through areas he expected them to nest, and concluded the hunting and human activities forced the passenger pigeons north without attempting to nest. A period of nearly 30 years passed without mass-nesting being identified, and yet the passenger pigeon still persisted. My conclusion is not that the birds stopped nesting and slipped into extinction, but they were nesting where and how they would avoid persecution, either in smaller groups and/or in undeveloped areas. Humans didn't directly kill them all; humans didn't have the means to ferret out every passenger pigeon west of the Rockies.

Halliday (1980) hypothesized that once the passenger pigeon numbers dropped to a threshold their population was doomed. Bucher (1992) thought food-finding ability diminished with the population decline; fewer passenger pigeons results in less communication of patches of forage. Conrad (2005) based his open access model on this "minimum viable population level." This hypothesis indicated a critical mass or number of birds would be necessary for reproductive success. However, passenger pigeons were also seen nesting in smaller groups and in pairs (Audubon 1831, 1844, Bendire 1892); these were birds that avoided the attention of the market hunters and could have perpetuated the species. Passenger pigeons even readily reproduced in captivity (Craig 1913). I find no substantial evidence to support the minimum viable population level hypothesis, and although I believe that the magnitude of hunting take was insufficient to cause extinction in passenger pigeons, I do not entirely discount hunting as a contributing factor.

Was it inbreeding suppression?

Passenger pigeons were reportedly successful in breeding and raising young in captivity (Deane 1881, 1896a, 1896b, Forbush 1917). These birds later died from what was reported as inbreeding, but no experimental data was presented to support this conclusion. The deaths of the captive birds closely tracked the wild population. The last captive passenger pigeon died at the Cincinnati Zoo on September 1, 1914, and the last reported wild passenger pigeon was shot in Quebec, Canada on September 23, 1907.

Was it contaminants?

Industrial contamination was high in particular localized areas in the United States during the late 1800s, and other contaminants were used away from urban centers. One of these, strychnine, was used in a non-discriminating manner to reduce wolf populations. Non-target species also succumbed by feeding at strychnine poisoned prey stations, including eagles, bears, coyotes, and foxes. Passenger pigeons did not fall prey to strychnine. However, burning sulfur pots were sometimes placed among trees with roosting pigeons. The pigeons would succumb to the sulfur fumes and fall from the trees. Use of this technique was limited, and the take was correspondingly small (Mershon 1907).

AN EXPERIMENTAL DISEASE MODEL

Bucher (1992) presents a comprehensive review of the factors that might have led to the extinction of passenger pigeons; he systematically excludes climate change, predation (humans and animals), competition (domestic animals), and inbreeding as the cause(s). I generally agree with these conclusions, but his conclusion that habitat alteration caused the extinction of passenger pigeons conflicts with the conclusions of several other authors (Blockstein and Tordoff 1985, Forbush 1917, French 1919, Schorger 1955). Bucher (1992) did consider disease, but he should have noted that the loss of habitat, though not enough to cause starvation or life-threatening food shortages, may have resulted in increasing passenger pigeon densities at the remaining patches of mast-producing habitat. I saw a similar phenomenon when band-tailed pigeons were forced to use patches with abundant acorns caused by a general failure of the mast crop in California in 2003-2004. In both situations, the passenger pigeons and band-tailed pigeons were concentrated in the remaining 'good mast' areas, which increased their susceptibility to disease as described in the disease spread and mortality formula below.

Bucher (1992) indicated other diseases and specifically referenced Newcastle's disease, a contagious and deadly bird disease, may have been responsible for passenger pigeons' extinction. Other diseases including avian pox, avian cholera, aspergillosis, ornithosis, tuberculosis were also candidates for infecting and killing passenger pigeons (Trainer 1969). I considered these and other diseases in my analysis, including avian malaria and avian pox (These were responsible for extensive mortality and probably extinctions in Hawaiian honeycreepers when mosquitoes were introduced into Maui.), but trichomoniasis seemed the most likely candidate because of the potential mode of re-infection of passenger pigeons by rock doves, and that trichomoniasis' better fit based on the infection model of band-tailed pigeons. Below I present a disease model and supporting documentation I believe best explains the extinction of passenger pigeons.

Passenger pigeons were not the only disease-naive species in North America when Europeans first arrived. The Americas were already inhabited and fully occupied with many Natives from the Athabaskans to Yupiks, and they were not prepared to deal with the diseases brought to the Americas: flu, measles, smallpox, diphtheria, cholera, and others. The Native people of the America's were systematically infected and nearly made extinct because they were naive to these new diseases. The means for harboring and transporting these diseases was Europeans. The means for harboring and transporting the disease that wiped out passenger pigeons was another pigeon, the rock dove.

But this story has not run its course. After presenting the disease model and explaining how I believe trichomoniasis caused the extinction of passenger pigeons, I will describe how Trichomoniasis is continuing to take its toll on other columbid species. Scientists are tasked with making predictions, and I'll make some predictions about additional columbid population declines and/or extinctions.

Model Title: A pathogen carried by rock doves caused massive mortality of band-tailed pigeons; did it also cause the extinction of passenger pigeons?

Abstract

Large numbers of band-tailed pigeons died suddenly in California's Las Padres National Forest in late winter of 2003. Trichomoniasis (Trichomonas gallinae) was the proximate cause. Rock doves might infect wild band-tailed pigeon populations with T. gallinae regularly. Furthermore, high assumed transmission rates related to band-tailed pigeon's aggregation behaviors probably allows T. gallinae to spread rapidly through this columbid's populations resulting in high mortality. This assumption of high transmission rates should also generally apply to passenger pigeons, which once ranged throughout eastern North America from the Gulf of Mexico to Canada, which also exhibited strong aggregation behaviors, and which are now extinct. Many North and South American dove and wild pigeon species and populations might be at risk of infection with T. gallinae. If this disease explanation withholds scrutiny, wildlife managers should consider developing policies that would reduce or eliminate feral rock dove populations and improve disease control measures by rock dove hobbyists.

Introduction

Trichomoniasis is caused by Trichomonas gallinae, a single-celled protozoan, also known as canker in doves and pigeons and as frounce in birds of prey. T. gallinae was identified first in Europe in 1878 and named in 1938 by Robert Stabler, a Colorado researcher. T. gallinae is a parasite of the upper digestive tract of many avian species causing yellowish 'plaques' in the mouth and esophagus. T. gallinae caused disease in rock doves (Old World feral pigeons), and the disease was likely introduced to North America with rock doves as early as the 1600s by European colonists (USGS 1988).

Passenger pigeons were the most abundant bird on Earth in 1800 (Blockstein and Tordoff 1985), but they were extinct by 1910 (Forbush 1913), and I suggest T. gallinae might have been the primary proximate cause. Since the T. gallinae was not described until 1938, the exact date of disease introduction is unknown. Even today exotic and introduced diseases go undetected (Daszak et al. 2000), so it is expected that T. gallinae would have gone undetected in passenger pigeons. T. gallinae was a new species to the Americas, and passenger pigeons, band-tailed pigeons, mourning doves, and other bird species lacked immunity to this disease.

Large numbers of wild band-tailed pigeons were observed in a Las Padres National Forest study area during the winter of 2003, but later in the winter dead band-tailed pigeon carcasses began accumulating on the ground in large numbers and floating down canyon streams. The study area was surveyed and dead birds were collected. Based on analyses of collected pigeons I attribute this major band-tailed pigeon mortality to T. gallinae (Ben J. Gonzales, D.V.M., M.P.V.M., Associate Wildlife Veterinarian, California Department of Fish and Game, 1701 Nimbus Road Suite D, Rancho Cordova, California 95670, (916) 358-1464, e-mail: bgonzale@dfg.ca.gov, necropsy report No. 16-04). Extrapolations of the survey numbers indicate that disease is a serious threat to North America's band-tailed pigeon populations.

Here I also present a disease model as a thought-experiment to understand the effect of T. gallinae on band-tailed pigeons, and discuss the implications of observed band-tailed pigeon mortality for understanding passenger pigeon extinction as well as potential risks to other pigeon populations. I review and compare the various other factors that might have influenced the decline of passenger pigeons and make recommendations for protecting other vulnerable pigeon and dove populations.

Methods

Large numbers of wild, apparently healthy, band-tailed pigeons were observed and noted in Las Padres National Forest just south of Monterey Bay, California during the fall and winter of 2003. Many areas were surveyed within the northern section of the Las Padres National Forest, and the Ambrosia Canyon drainage was selected as a primary study area. Pigeons were counted as they flew between feeding and roosting areas. They were especially numerous in some mountain passes. The survey was expanded beyond the Ambrosia Canyon and adjacent study areas to determine the extent of the population. During January-April 2004, band-tailed pigeons began dying and carcasses were observed throughout the study area. Eighteen 2 km-long transects were distributed throughout the Ambrosia Canyon drainage. Some of the survey transects used existing trails, but to get a better understanding of the density and distribution of pigeon carcasses some transects were run 90 degrees from the beginning and ends of trail transects. The steep terrain and extensive poison oak (Toxicodendron diversilobum) prevented use of random transect surveys. All band-tailed pigeon carcasses within 3 meters of either side of each transect were counted. In March 2004, Eurasian wild boar (Sus scrofa) entered the study area and ate many of the dead pigeons. The survey ended when I noticed this scavenging.

I present the following formulation as a simple thought-experiment that accounts for the basic characteristics of disease spread (Equation 1)

 Equation 1

where R is the number of pigeons infected during a given day in a susceptible population, P is the probability of transmission between two individuals that encounter each other, C is the daily rate of contact of individual birds with a given infected bird and this incorporates the rate of mixing, I is the disease incubation rate in days, and D is the duration of infection in days before the infected pigeon is no longer infectious (due to death or recovery of the infected individual). This infection rate was then applied to a hypothetical C. fasciata population assuming different mortality rates of infected individuals (Equation 2)

 Equation 2

where N is the number of individuals. I used this model to visualize graphically the potential dynamics of T. gallinae in a band-tailed pigeon population and to explore the sensitivity of the rate of infection and population decline to the various characteristics of this disease in this population.

Results

Many of the December 2003 morning band-tailed pigeon counts exceeded 1,000 birds per hour flying through mountain passes from roosting areas to feeding areas. Band-tailed pigeons were abundant, and they were almost constantly flushed from roosting trees as surveyors walked through the forest. It was impossible to avoid flushing band-tailed pigeons from their roosts every few minutes.

The large number of birds appeared to indicate an abundant band-tailed pigeon population. However, the 2003/2004 acorn mast for the Central California region was poor except for some patches. One of the areas with abundant acorn mast was the Las Padres National Forest study area (personal communication, Jeff Cann, California Department of Fish and Game, e-mail: JCann@dfg.ca.gov). The relative abundance of acorns in Las Padres National Forest during this season seemed to have increased the band-tailed pigeon density in the study area above normal levels, perhaps facilitating the observed disease epidemic.

During January 2004 band-tailed pigeons began dying and carcasses were observed throughout the study area. The mean number of band-tailed pigeon carcasses per transect (± standard deviation) was 103 ± 26, or 8,583 dead pigeons per square km in the Ambrosia Canyon drainage. The die-off appeared to occur from late winter through spring, as old and new pigeon carcasses were found in various stages of decay throughout that time. Some scavenging by predators occurred; bobcat (Felis rufus) spoor was found near partially eaten pigeons, and red-tailed hawks (Buteo jamaicensis) were seen in the study area on three occasions. In March 2004 Eurasian wild boar entered the study area and ate the dead pigeons. I noted that feather piles marked where the pigeons had fallen and were eaten by the wild boar.

Specimens of dead band-tailed pigeons were analyzed for cause of death by Wildlife Investigations Laboratory, Wildlife Programs Branch, Wildlife and Inland Fisheries Division, California Department of Fish and Game. The report is shown below.

"EXTERNAL - Birds appear emaciated. No lesions seen externally.

INTERNAL - Bird 1. entire respiratory and gastrointestinal tract clean with no lesions except for inside oral cavity. Heavy, pseudomembranous plaque accumulation approximately 2 cm diameter rostral to glottis on tongue. Part of plaque overhung epiglottis, partially occluding airway. Two entire acorns present in proventiculus, one fragmented acorn in ventriculus.

Bird 2 – Examination of entire respiratory tract normal, as well as upper gastrointestinal tract negative for lesions. Proventiculus and ventriculus empty of food items. Ventriculus lined with yellow-white, caseous plaques.

SPECIMENS TAKEN & RESULTS - Specimens of caseous plaques taken for microscopic evaluation. These samples were unproductive, most likely because birds had been frozen. Examination of plaques for trichomonads is most productive when specimens are collected from live, sick birds or freshly dead birds.

DIAGNOSIS - Avian trichomoniasis (canker) due to Trichomonas gallinae infection. The caseous plaques are formed as part of the intense inflammatory response to infection with T. gallinae. Relatively small lesions may result in mortality if they obstruct either the respiratory tract or gastrointestinal tract. The ventricular lesions in pigeon 2 were unusual in that most lesions are seen in the pharynx and upper gastrointestinal or respiratory tract." (Ben J. Gonzales, D.V.M., M.P.V.M., Associate Wildlife Veterinarian, California Department of Fish and Game, 1701 Nimbus Road Suite D, Rancho Cordova, California 95670, (916) 358-1464, e-mail: bgonzale@dfg.ca.gov, necropsy report No. 16-04).

In this disease spread formulation (Equation 1), the cumulative R, the total number of birds infected over time, is exponential, exceeding 50 million individuals by 33 days (Figure 1) if we assume that P = 0.1, C = 50, I = 4, and D = 8. If all infected individuals died 8 days after infection, a population of 50 million individuals would suddenly crash to extinction between 30 and 40 days after introduction of the disease by a single individual, assuming that all individuals keep aggregating (Figure 1) and no birds develop immunities to the disease. These hypothetical modeling results were most sensitive to the rate of contact between birds (C) and the probability of transmission (P) (Figure 2), both of which are influenced by the aggregation behaviors and the types of contact among pigeons.

Discussion

Band-tailed pigeons preferred the forested areas within the study area. Forested areas comprise about 30% of the Las Padres National Forest, or 2,125 square kilometers. If the pigeon die-off observed in the study area was evenly distributed across the forested areas of Las Padres National Forest, a questionable assumption, and if the example modeling assumptions are accurate, a total of over 18,000,000 band-tailed pigeons would have died there during the late winter and spring of 2004. I assume that the disease landscape of pigeons is heterogeneous (i.e., there are disease refugia), and that the example modeling assumptions are reasonable rather than accurate, but I suggest that the mass-mortality observations described herein and the modeling thought-experiment indicates the real potential for catastrophic population decline in pigeons due to the epidemic spread of the protozoan Trichomonas gallinae. I also suggest that this might have been the driving cause of passenger pigeon extinction. I suggest that this real possibility is well worth closer examination given the continued emergence of avian disease epidemics and the implications for both human and non-human populations and ecosystems.

Several conditions make band-tailed pigeons susceptible to the spread of T. gallinae infection: they are gregarious (i.e., they aggregate, even as population numbers decline), they share feeding and drinking areas where the disease can be transmitted, they use billing during courtship, and they feed their young in a manner that promotes spread of the disease. The model presented here helps to visualize how these social and behavioral characteristics result in rapid transmission of T. gallinae throughout a population. Additional information to consider in the model is background infection and prevalence of carriers of the disease during non-epizootic years. I did not collect data on year-to-year prevalence of T. gallinae in band-tailed pigeons. However, the model reflects the observed high mortality rate in the study area and indicates a highly contagious and virulent form of T. gallinae which seems an unlikely candidate for background infection.

Band-tailed pigeons provide a disease transmission network as they travel, feed, water, roost, and breed communally. Although their communal strategies may reduce individual exposure to predation and aid their search for food and refuge, the network of individuals allows numerous transmission opportunities, much more in fact than would be expected from simple sexual contact often described in susceptible/infective/removed (SIR) models, which solve for and explain disease transmission in networks of individuals (Diekmann and Heesterbeek 2000, Newman 2002). Thus, the SIR model as currently formulated does not account for all the characteristics contributing to spread of T. gallinae in band-tailed pigeons.

To understand the predicted high rate of transmission of T. gallinae in band-tailed pigeons we must understand how the risk factors relate to band-tailed pigeon natural history, behaviors, and population density.

I estimated band-tailed pigeon populations by counting birds as they moved from night roosting sites to feeding areas. They can be counted easily as they pass through mountain passes in the morning. The pigeons fed and watered in communal situations, covering the same ground as others. While feeding and watering the birds mixed and came in direct and indirect contact with hundreds to thousands of birds daily. These birds are highly gregarious and contact among individuals in the group was high. Accordingly, the rate of contact and mixing (C) was high in the model.

Infected pigeons develop large yellow waxy highly-infectious plaques, parts of which sometimes break off and drop to the ground or in the water if they are drinking. Apparent healthy carriers of the pathogenic strain(s) can shed trichomonads into the drinking water. These may have been attractive to other pigeons and eaten, a behavior observed in some doves and pigeons. Indirect infection could have occurred when plaques and other discharges were dispersed on food and water during communal feeding and watering (USGS 1988). Such conditions might have increased P, the probability of transmission, in addition to C—the rate of contact.

During courtship, adult pigeons bill each other, and the adults feed their offspring 'pigeon milk' from their throat—a mixture of salts, fats, and proteins (Blockstein and Tordoff 1985). In an experiment conducted by Kocan and Amend (1972), the incubation rate (I) was very high in mourning dove after inoculation with a virulent form of T. gallinae. Nearly 1/3 of the individuals had signs of trichomoniasis after only three weeks of being infected. The probability of transmission (P) during billing and feeding of chicks would have been very high (see also Deane 1881, Deane 1896b, Peeters 1962). Infection is likely highest during courtship billing and nearly inescapable between young and infected adults due to the manner of food transfer. However, the band-tailed pigeons I studied were infected and died outside of the nesting period; communal feeding and drinking might have been the main mode of infection.

In the disease spread and mortality formulae (Equations 1 and 2), D is the duration of infection before the infected pigeon is no longer infectious (due to death or recovery and is no longer a carrier). Virulent forms of T. gallinae can cause 100% mortality in some columbids. Stabler and Braun (1975 and 1979) found that for band-tailed pigeons the time of death from inoculation by a virulent form of T. gallinae is long enough for the diseased bird to infect many others, 5.7 to 7.1 days after exposure. Mourning doves have a similar duration of infection when infected with a virulent form of T. gallinae (Haugen and Keeler 1952, Greiner and Baxter 1974, Stabler and Braun 1975, and USGS 1988). Once the disease enters the band-tailed pigeon population the spread of the disease is rapid and widespread. The rate of transmission (R) of T. gallinae in the band-tailed pigeon population is high because it is a function of the high probability of transmission (P) and the high rate of contact (C). I didn't collect survivors or otherwise note if any of the infected band-tailed pigeons survived and became carries. It is possible that there were no survivors of the population I observed, but I do not know.

Band-tailed pigeons are found in two regions of western North America, the coastal population occurs from British Columbia south to southern California, and the interior population is located in Utah, Colorado, Arizona, and New Mexico south to Mexico. In 1992 the coastal population was estimated at 2.4-3.1 million birds (USFWS 1996). Mass die-offs are not uncommon and, when identified, are caused by T. gallinae infection. Following my survey of the Las Padres National Forest study area, the number of pigeons sighted flying through the forest dropped considerably. Some birds might have moved out of the area, but the evidence indicates the population was reduced considerably by disease. This simplistic model and extrapolation indicates that 18,000,000 band-tailed pigeons could have died in the forested areas of the Las Padres National Forest during the season. This estimate far exceeds the total USFWS (1996) population estimate for that area. This could be explained if the total band-tailed pigeon population is greater than estimated by the USFWS or if my mortality estimates are too high.

Passenger pigeon proxy

Band-tailed pigeons can be used as a proxy for testing the hypothesis that trichomoniasis caused the rapid decline of passenger pigeons. Band-tailed pigeons and passenger pigeons share several characteristics that make both species susceptible to the spread of T. gallinae infection. Both species are gregarious, share feeding and drinking areas where the disease can be transmitted, use billing during courtship, and feed their young in a manner that promotes spread of the disease. Both species have social and behavioral characteristics that T. gallinae exploit for rapid transmission throughout the pigeon population, and both species were/are disease-naïve to T. gallinae infection.

Passenger pigeons provided an excellent 'landscape' for the transmission of a contagious disease (Bucher 1992). In the simple disease spread and mortality formula for describing the rate of transmission of T. gallinae to passenger pigeons (Equation 1), the factors promoting rapid spread of T. gallinae to passenger pigeons far exceeds that of band-tailed pigeons.

Passenger pigeon flocks were hundreds of miles long and contained billions of birds (Audubon 1831, Wilson 1812). A single file line of them arranged from head to tail would have stretched around the earth at the equator 22.6 times (Cokinos 2000). They were so numerous, some nesting sites covered many thousands of acres and the birds were so congested in these areas that hundreds of nests could be counted in a single tree. A Wisconsin nesting site was reported as covering nearly 2,200 square kilometers, and the number of birds nesting there was estimated to be at least 135,000,000 (Schorger 1937). The pigeons fed and watered in communal situations, covering the same ground as hundreds, thousands, or millions of birds flew from one patch of food to another, and each time passing over and beyond the rest of the flock that had already passed and was feeding or watering. In this hop-scotch pattern the birds mixed and came in direct and indirect contact with thousands to millions of birds daily. These birds were highly gregarious and contact among individuals in the group was high.

Indirect infection occurred when plaques and other discharges were dispersed on food and water during communal feeding and watering (USGS 1988). Large numbers and high density of the passenger pigeons (C in the formula, or rate of contact) meant high probability of transmission. The probability of transmission (P) during billing and feeding of chicks would have been 100% based on experiments with other columbids (see Deane 1881, Deane 1896b, Peeters 1962). Rate of transmission is not equivalent to rate of new cases of disease because any previously infected individual may be immune to disease (canker/mortality). The newly hatched squab however, which is susceptible to infection by all strains will probably die if the parent is carrying a pathogenic strain of T. gallinae. So, squab mortality should be much greater than adult mortality unless there are relatively few exposed adults prior to rapid transmission, which may have been the case with the disease-naive passenger pigeon population.

So, was it disease?

Risk factors for host species are complex (Daszak et al. 2000), but high population density and gregarious and reproductive behaviors irrefutably increase the risk for passenger pigeons, band-tailed pigeons, mourning dove, and other columbids to the spread of disease. Koopman et al. (1991) and Koopman and Longini (1994) describe the disease risk factors in their contagious virulent disease models and Newman (2002) supports the notion that disease spread increases with increases in the mixing rate and rate of exposure. Epidemics among wildlife populations can be triggered by, and are enhanced with, increased contact among individuals (Hess 1996). Passenger pigeons and band-tailed pigeons had/have high mixing and contact rates. The continued spread of the disease until extinction hinges on the assumption of a continued cooperative behavior of passenger pigeons, which would prevent density dependent abatement of the epidemic. This is what happened to northern cod: their proclivity to aggregate led to unabated high fishing rates (because catch per unit effort continued to be high even when the population was crashing) (Bjørndal and Conrad 1987), but in the case of cod, fishing mortality replaced disease mortality seen with passenger pigeons.

Hess (1996) found that metapopulation models predict that highly contagious diseases increase the probability of extinction. The disease risk factors found in columbids promote the spread of disease. The high mortality and risk of extinction of columbids and especially passenger pigeons from trichomoniasis is a function of the disease's virulence. T. gallinae is an invasive species for which American columbids were ill-prepared, they had no immunity for this disease, and it was virulent. Extinction of a host appears, at first flush, to lead to the extinction of the parasite, in this case T. gallinae. However, long-term survival of the parasite can be realized through transmission (Tompkins et al. 2002), including to other species. T. gallinae is a disease of many bird species easily jumping back and forth making the more susceptible species vulnerable to extinction. This transmission and extinction process might take many years as the disease runs its course (Tompkins and Wilson 1998). This ability to jump species and to re-infect species is a characteristic promoting species' extinctions. This is accomplished by having a population with no prior experience with the pathogen, and the parasite is maintained and disseminated (reintroduced) by a carrier species (Hanson 1969) in this case the common pigeon. T. gallinae in passenger pigeons can, by this definition, also be considered a population-independent disease, which, according to Hanson (1969) doom a species to extinction. Based on these rules of disease engagement, passenger pigeons had little hope of surviving virulent forms of T. gallinae, and band-tailed pigeons (and other columbids) may well follow passenger pigeons to extinction.

The mode of disease spread by an invasive species is familiar among birds, mammals and invertebrates. Vilcinskas et al. (2013) describe how invasive harlequin ladybird beetles (Harmonia axyridis) spreads a 'biological weapon,' in this case another parasite, which is lethal to native ladybird beetle species. Diamond (1997) described how invasive Europeans (humans) successfully overthrew superior numbers of disease-naïve Native Americans.

Hanson (1969) explains that epizootics can result from density-dependent diseases, and these diseases are most rapidly spread in a high-density population. Density-dependent diseases are long-lived in the population (Hanson 1969) or until the species becomes extinct. Hanson (1969) believes population-dependent diseases are more likely to cause drastic population declines. Passenger pigeons were vulnerable to extinction from a virulent density-dependent disease. However, any birds that recovered from a virulent strain or were infected with avirulent strains would be immune, although capable of transmitting the parasite to their squabs. In this case, re-infection with other virulent forms of a disease can complete the extinction process.

Following a mourning dove epidemic in South Carolina, Kocan and Amend (1972) found the population contained few young. This is consistent with Forbush's (1913) observation that the passenger pigeon population after 1878 had few young. Blockstein and Tordoff (1985) thought this was a result of harvesting young pigeons from communal nesting locations, but it was more likely the result of high (near 100%) mortality of young pigeons from infection by a virulent form of T. gallinae.

T. gallinae is responsible for the death of millions of rock doves, thousands of mourning dove and band-tailed pigeons and countless trained raptors (Stabler 1969). Mourning dove have been diagnosed with trichomoniasis in Alabama (Haugen and Keeler 1952), Central California (Rupier and Harmon 1988), Nebraska (Greiner and Baxter 1974), South Carolina (Kocan and Amend 1972), and southeastern United States (USGS 1988). Band-tailed pigeon outbreaks of trichomoniasis have been documented in California, Arizona, and Colorado (Stabler 1950, 1951, Stabler and Braun et al. 1975, USGS 1988). Other columbids having been infected by trichomoniasis include Hawaiian barred dove (Geopelia striata) (Kocan and Banko 1974), Inca dove (Scardafella inca) (Locke and James 1962), and rock doves (Mesa et al. 1961, Stabler 1951, USGS 1988). Other bird groups are also infected by T. gallinae; one of the most notable is raptors. Pokras et al. (1993) reported the disease in owls, and Rosenfield et al. (2002) described the prevalence of trichomoniasis in Cooper's hawks (Accipiter cooperii). In 1966, my red-tailed hawk died from frounce a few weeks after eating a sick pigeon. Reports of this disease causing mortality in raptors have been around for hundreds of years, even prior to the causative organism being identified (USGS 1988). Declines in raptor populations, due to direct effects from trichomoniasis or indirect effects from a loss of an abundant food sources (doves and pigeons), warrants further study. The population declines (and extinctions) from T. gallinae of other species such as Carolina parakeets and ivory-billed woodpeckers also merit a closer look.

Band-tailed pigeons share many of the behaviors and ecological characteristics of passenger pigeons. With the extinction of passenger pigeons, one could expect band-tailed pigeons to be capable of expanding their range into the former passenger pigeon range. This may be prevented because T. gallinae continues to exert a high mortality on band-tailed pigeons.

Timing of spread of trichomoniasis

Contrary to Schorger (1955), the delay of the disease spread to passenger pigeons could be explained by lack of niche overlap until rock doves started to become a common feral species long after their introduction. Perhaps the use of rock dove as decoys when hunting passenger pigeons resulted in inoculation of passenger pigeons with T. gallinae. Once the disease entered the wild passenger pigeon population the spread of the disease would have been rapid and widespread. The rate of transmission (R) of T. gallinae in the passenger pigeon population would have been extreme, as a function of the probability of transmission (P), and the rate of contact (C). Any survivors of the infection, those that were exposed and recovered, would have delayed the extinction, but alas, there were no survivors. This supports the idea that the passenger pigeon population was disease-naive and very susceptible to dying from infection by T. gallinae.

The timing and rate of the decline of passenger pigeons indicates an epidemic disease. French (1919) describes the timing of the passenger pigeons' decline as slow at first but by 1865 to 1886 was remarkable. French's (1919) mention of a fever and rapid decline is consistent with the rapid spread and high mortality associated with a virulent disease that was highly contagious and easily spread. Once a pigeon was infected with trichomoniasis, transmission would have been almost certain from the two behaviors common among pigeons and doves, billing during courtship and feeding young, but likely during their daily communal feeding and watering bouts. Initial timing of infection correlates to exposure of the disease via contact with rock doves.

Even as late as 1871 huge numbers of passenger pigeons occupied communal nesting sites; one in Wisconsin covered 850 square miles (2,002 square kilometers) (Schorger 1937). In 1878 a Michigan communal nesting site covered 200 square miles (518 square kilometers), and Brewster (1889) reported a six square mile (16 square kilometers) nesting in Michigan in 1881. Brewster (1889) interviewed pigeon netters, farmers, lumbermen, and others who reported large flights and nestings in Michigan in 1888. If infected with T. gallinae, this could have been the last great spread of the disease among the remaining birds, and this correlates closely with the timing of passenger pigeons' rapid final population decline.

Conclusions

During the winter and spring of 2003/2004 I noted large numbers of wild band-tailed pigeons in a Las Padres National Forest study area, and later in the winter dead band-tailed pigeons began appearing in large numbers on the ground. The band-tailed pigeons died from T. gallinae. I estimated that in the forested areas of Las Padres National Forest a total of over 18,000,000 band-tailed pigeons died there during the spring of 2004, and indicates disease may be a serious threat to North America's band-tailed pigeon populations.

I present a disease model that describes disease susceptibility of columbids to T. gallinae and supports the hypothesis that rock dove regularly infects wild band-tailed pigeon populations with trichomoniasis resulting in high mortality rates. The model indicates that T. gallinae may have been responsible for the extinction of passenger pigeons. Based on the findings I predict that many of the North and South American dove and wild pigeon populations are at risk to infection and possible extinction.

The common misuse of antibiotics might lead to the development of disease resistance and virulent disease forms (see Christensen et al. 1990 and Wilkinson 1999). Accordingly, reported misuse of antibiotic used to treat T. gallinae in domestic pigeons could result in drug resistance and more virulent forms of the parasite. These forms may be highly virulent to a disease-naive population of other species.

Natural selection should favor evolution toward benign coexistence between a host and parasite. However, benign coexistence with one species may result in a virulent disease to another species.

The increased virulence and extinction of one species, such as the passenger pigeon, is of no consequence to the disease and its chances of survival as long as the disease can survive in another species, such as domestic pigeons.

If trichomoniasis is not brought under control, I predict that many of the North and South American dove and wild pigeon populations are at risk to infection and possible extinction. Protection of the wild pigeon and dove populations would be best accomplished by eliminating misuse of antibiotics in rock dove populations, removal of feral rock dove populations, and monitoring of disease outbreaks in wild native dove and pigeon populations.

Figure 1. Predicted number of band-tailed pigeons (Columba fasciata) infected (red line) and the change in a population of 50 million individuals (blue lines) by Trichomoniasis (Trichomonas gallinae) assuming persistent aggregation behavior in a declining population and assuming 100% and 50% mortality.

COLUMBID

CONSERVATION

Reoccurring exposure to T. gallinae

T. gallinae is still extant, possibly being carried now by dove, raptors, parakeets, and other species, and still being transmitted by common pigeons (rock doves) which are spreading and becoming more common in the in the wild. Exposure of wild pigeons and doves to new strains of T. gallinae will continue as they have direct or indirect contact with domestic and wild common pigeons. A disease reservoir exists in rock doves, and new strains of T. gallinae will develop due to continued mis-application of antibiotics (Stabler and Kitzmiller 1967 and Lumeij and Zwijnenberg 1990). Domestic and feral pigeons play a role by providing a "zoonotic pool" from which T. gallinae can emerge (Daszak, et al. 2000). One mechanism for spread is the release of spares, (extra birds) sickly or otherwise inferior rock doves, used to train hunting dogs. Escaped spares can directly infect birds of prey that may take them, or they may indirectly infect wild pigeons and doves via communal watering and feeding situations (Hanson 1969). Based on this, I recommend population control of wild rock dove populations be initiated and consistently enforced, and that falconers and pigeon fanciers be trained in the use and application of antibiotics and proper disposal of sick birds. Where commercial and social constraints exist that preclude following these recommendations, I predict future outbreaks of disease in wild pigeon and dove populations and the possibility of band-tailed pigeons and other columbids going extinct. Further investigations identifying other species affected by trichomoniasis are warranted.

Globalization and the spread of diseases

Introduced infectious diseases often go undetected for years, and globalization will ensure their spread throughout the world. Few measurable successes have resulted from intervention; and crisis management has prevented measurement of the results (Woodroofe 1999). The loss of biodiversity due to extinction from invasive species can result in a cascade of effects. The extinction of passenger pigeons, with their huge biomass and presumed large effect on North American forest communities, likely altered this ecosystem considerably.

Translocations of species, such as the introduction of common pigeons to the Americas in the 1600s, are finally being viewed as a significant problem (Cunningham 1996). The threat of disease spread goes beyond the effects upon the target species; direct and indirect effects might result in considerable changes to ecosystem structure and function, as well as evolutionary changes. As globalization and human populations increase, nonnative flora and fauna introductions will continue increasing, resulting in biological pollution and accelerated loss of global biodiversity (Daszak et al. 2000). Endangered species may be especially at risk from invasive diseases and parasites (McCallum and Dobson 1995).

South American eared dove extinction experiment

Hanson (1969) and Viggers (1993) describe the possible role of infectious agents for many species and how a disease-naive population could be decimated by a disease introduced with another species (see also Kocan and Kinsley 1970). A natural experiment might be underway, which could help us understand the delay of infection by T. gallinae. Breeding colonies of eared dove in Argentina and Brazil, a native species there, can reach 1-10 million birds, and they are considered a nuisance. Poisons dispersed by air and on land, hunting, and trapping can remove hundreds of thousands of birds but with no noticeable effects on the overall population (Bucher 1992). This lends support that hunting and trapping of the passenger pigeon did not lead to its extinction. The experiment that may be taking place and should be carefully studied is if or when rock doves or another columbid ultimately infect the South American eared dove with T. gallinae. Eared dove are similar to passenger pigeons; they have a high population density, and they share similar disease transmission behaviors (billing and feeding of young).

Global warming, climate change and columbids

Population density is one of the risk factors for spread of disease. The 2003/2004 California acorn crop was patchy. This resulted in patchy high-density band-tailed pigeon populations. I would be remiss to not suggest that global warming and global climate change might be reducing acorn mast production thus directly and indirectly adversely impacting wildlife populations. This might indicate a combined effect of famine, climate variability or even climate change, and disease. Decreased or changed distribution of food might have made the birds more vulnerable to this disease and predators. The effects of global climate change must be considered when trying to understand the dynamics of the spread of disease (Grenfell and Dobson 1995). I don't expect human-caused global climate change will be remedied soon, but we can take steps to protect band-tailed pigeons from extinction and understanding the relationship of spread of diseases to climate change.

ACKNOWLEDGMENTS

I would like to thank Mike Lyons for assistance in collecting the band-tailed pigeon data, especially when the summer temperatures and exposure to ticks and poison oak made data collection unpleasant. I would like to thank Ben J. Gonzales, D.V.M., M.P.V.M., Associate Wildlife Veterinarian, California Department of Fish and Game for analyzing the band-tailed pigeons for cause of death. I thank Richard Kocan for his review and comments. I thank Tom Okey for his assistance on the disease model. Tom's work focuses whole-system trophic models and this was an interesting, if not challenging, exercise for Tom.

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GLOSSARY

Acorns: The fruit (nuts) from oak trees.

Aerodynamics: The dynamics of bodies (such as a bird or airplane) moving through the atmosphere and its ability to stay aloft and avoid or overcome drag and turbulence (resistance).

Anthropomorphic: Attribution of human characteristics or behaviors to animals.

Angle of attack: The angle of a wing as it travels through air.

Apex predator: Predators that are rarely, if ever, preyed upon and are often at the end of long food chains where they have a crucial role in maintaining and determining the health of ecosystems.

Aspergillosis: A yeast that can cause disease in birds and other animals.

Avian malaria: A malaria parasitic disease in birds.

Avian pox: A virus that can cause disease in birds.

Beechnuts: The fruit (nuts) from beech trees.

Billing: The act of mouthing (kissing) among birds often as part of courtship behavior.

Biodiversity: The variety of life in all its forms. The greater the biodiversity in an ecosystem the healthier and more stable the system.

Biomass: The amount or mass (weight) of living material.

Boom and bust: Large fluctuations in a species' population results from reaching carrying capacity and then dropping, usually from starvation, predation or disease, to very low numbers.

Bottom up control: This is when species low on the food web, such as grazers, has a significant influence on the upper levels of the food web.

Canker: A disease referred to as Trichomoniasis and caused by Trichomonas gallinae, a single-celled protozoan, known as canker in doves and pigeons and as frounce in birds of prey. T. gallinae was identified first in Europe in 1878 and named in 1938 by Robert Stabler, a Colorado researcher. T. gallinae is a parasite of the upper digestive tract of many avian species causing yellowish 'plaques' in the mouth and esophagus. T. gallinae caused disease in rock doves (Old World feral pigeons), and the disease was likely introduced to North America with rock doves as early as the 1600s by European colonists.

Carnivores: Species of animals that eat primarily meat.

Carrier: An organism that harbors a disease, usually without symptoms but with the ability to pass the disease to another organism.

Cascading effects: A series of related consequences promulgated by a single action.

CO2: Carbon Dioxide

Columbids (Columbidae and Columbiformes): Taxonomic group(s) for birds that includes dove and pigeons.

Communal feeding: Feeding in close proximity to members of a population and can result in the spread of disease.

Competition: When organisms try to secure resources at the expense of other organisms such as when passenger pigeons competed for a limited supply of mast in a specific area.

Conifers: Cone-bearing plants, usually referring to pine, spruce, cedar, and fir trees.

Contagious: The ability of a disease to infect other members of a population.

Copulation: The act of union of the external sexual organs of two sexually reproducing animals. In the case of birds, this is usually a very quick behavior.

Courtship: The process in which a members of a breeding pair attempt to establish a pair-bond.

Critical mass: This term is often used as it relates to nuclear reactions when a certain mass (weight) of specific material are brought together resulting in an uncontrolled reaction & an explosion. This term, when referring to passenger pigeons, relates to the number of birds necessary for successful reproduction (see mass nesting), but it is an unproven and questionable hypothesis.

Crop milk: The excretions of minerals and lipids produced in the throat and crop of pigeons and used by the chicks for food during the first days after hatching.

Deciduous forests: Forests predominately made up of trees that loose their leaves in the fall.

Dispensation: The level below which a population cannot sustain itself even in the absence of additional loss such as by hunting.

Diphtheria: A disease that can infect birds.

Disease naive: When a species has no experience and resistance to a disease.

Disease reservoir: When an organism can harbor a disease, usually without consequences to that organism, but it can infect other organisms.

Disease transmission in networks: When a disease is transmitted to other organisms in its group.

Drag: The resistance caused when a bird flies through the air or a fish swims through the water. Drag increases with increasing speed and increasing turbulence.

Droppings: Feces.

Drug resistance: This occurs when antibiotics are not properly used and develop strains that can longer be treated by some antibiotics.

Ecosystem: The natural system in which energy and nutrients cycle between plants, animals, and substrate.

Ectopistes migratorius: The scientific name for the passenger pigeon.

Esophagus: The tube that connects the throat to the stomach through which passes air to the lungs and food and water to the stomach.

Extinction: When a species no longer exists. Species can also become extinct in the wild so that their kind only survives in captivity such as in zoos.

Falconers: People who keep and train birds of prey such as eagles, hawks, and falcons.

Feathers: The covering of birds that are used for flight and protection form the elements such as wind and rain.

Feral: A domestic animal that lives in the wild.

Food chain: The predatory relationship between plants and animals. Energy and nutrients are transferred from one organism to another through the food chain.

Food pyramid: Energy and nutrients are used to maintain each subsequent link in the food chain, and the amount of available energy decreases rapidly at every trophic level. Each level supports fewer individuals than the one before. This results in a pyramid where there are many organisms at the bottom (producers) and few at the top (predators).

Food web: A more complex and realistic representation of a food chain that depicts the complexities of predatory relationships between plants and animals.

Frounce: (see canker)

Fusiform: Fish or torpedo-shape, and is very aerodynamic.

Gizzard: A muscular pouch behind the stomach in the alimentary canal of birds containing ingested sand and gravel that aids in the breakdown of seeds before digestion. The gizzard functions somewhat as teeth in mammals.

Global warming: The warming of the earth's oceans and atmosphere can be man-made or natural. The present global warming trend is being caused or enhanced by humans due to the addition of greenhouse gases, such as carbon dioxide, into the atmosphere.

Globalization: How human beings are becoming more intertwined with each other around the world economically, politically, and culturally. Although these links are not new, they are more pervasive than ever before and a result of expanded transportation.

Great Lakes: They are the group of the largest lakes on earth that are on the border of Canada and the United States.

Gregarious: Seeking the company of others.

Habitat loss: The loss due to natural or human-caused activities that destroy or otherwise alter the place where organisms live. Climate change is causing loss of on a grand scale in the oceans and on land.

Herbivores: Plant eaters or grazers.

Highly migratory species: Species that travel unusually great distance in their search of food, safe nesting, etc.

Hot spot: Defined in this text as an area where abundant food is found such as a patch of mast.

Information centers: Birds that use communal roosting and nesting may benefit by learning where to find food by watching and/or following other members of the communal roost.

Interspecific competition: Competition between species as opposed to intraspecific competition which is competition within a species.

Introduced species: A species brought by humans to an environment where it did not previously exist.

Invasive diseases: A non-indigenous disease such as smallpox was to the Americas.

Invasive species: An invasive species is a species that was introduced to a new environment by humans and out-competes the natural flora or fauna and has the potential to cause environmental and economic harm.

Ivory-billed woodpeckers: The largest of the American woodpeckers and thought, until recently, to have gone extinct. Its extinction is not well understood, and, based on the findings of passenger pigeons in this book, disease should be considered.

Jolly-Seber method: A method for determining population size.

Keystone species: A species that has a large effect on the biological community despite its relative biomass. Removal of this keystone species can cause widespread changes to community structure.

Market hunters: People who hunted passenger pigeons for profit.

Mass nesting: When very large numbers of an animal nest in a restricted location and is often used to synchronize nesting timing and to overwhelm predators.

Mast: Acorns, beechnuts, chestnuts that can occur is vast amounts during the fall and winter.

Matrix: In landscape ecology several descriptors of landscapes are matrix, corridors and patches. The matrix is the most common or background habitat type.

Metapopulation: A collection of interacting populations of the same species.

Metapopulation models: Mathematical model of segments of a larger population.

Minimum number alive (MNA) method: The method used to enumerate the number of passenger pigeons observed in mass migration events.

Minimum viable population level: Minimum number of animals needed to sustain a population. This number is at least two for all sexual species, but it may be far more for some species. Some researchers believe that passenger pigeons went extinct when their population dropped below a certain number, perhaps hundreds of millions, although there is no evidence to support this theory.

Migration: When animals move in mass to new locations to find food, avoid predations, secure safe nesting habitat, etc.

Models: Using mathematical formulas based on data, models are used to describe a system or process and make predictions.

Molt: Birds molt, or lose their feathers so that old worn feathers can be replace with new feathers.

Monogamous: Having a single mate.

Mortality factors: For most animals the mortality factors include predation, starvation, disease, loss of habitat, contamination, etc.

Mortality rates: The rate at which organisms die.

Natural selection: Darwin's theory of evolution describes natural selection as only the organisms best adapted to their environment tend to survive and transmit their genetic characteristics to succeeding generations while those less adapted tend to be eliminated.

Nest abandonment: When a bird abandons its nest usually due to some measurable disturbance such as predation, severe weather events or lack of food.

Nestings: Young birds before they leave the nest (fledge).

Newcastle's: A deadly and contagious bird disease.

Niche: This is the position occupied by an organism within an ecosystem which includes how an animal survives, locates food, avoids predation and reproduces.

Niche separation: When animals avoid conflicts and competing with other species using a number of techniques such as different times of the day, different water depths, etc.

Nomadic: In birds refers to a somewhat wandering or random flight pattern or migration.

Nuptial flight: Pre-breeding flight display.

Optimal foraging: The tendacy for predators to locate and use areas of high productivity or hot spots their hunting success.

Parasites: When one organism (the parasite) lives on, off or at the expense of the other (the host), and the parasite benefits but the host does not and may be harmed.

Patches: In landscape ecology several descriptors of landscapes are matrix, corridors and patches. Patches are relatively uncommon in the matrix.

Pigeon fanciers: People who raise and/or breed pigeons.

Pigeon milk: The excretions of minerals and lipids produced in the throat and crop of pigeons and used by the chicks for food during the first days after hatching.

Plaques: Caseous plaques are formed as part of the intense inflammatory response in birds to infection with T. gallinae.

Population-independent disease: When a disease is maintained and disseminated (reintroduced) by a carrier species and can result in the extinction of infected (non-carrier) species.

Post-breeding migrations: Migration of adults or young immediately after nesting season.

Predation: Preying on another organism for food.

Predator field: The group of predators. For passenger pigeons the predator field was large with many species of birds and mammals.

Preening: When a bird cleans, smoothes and cares for its feathers usually using its beak and claws.

Probability of transmission: The level of risk of transmission of a disease.

Protozoan: Single-celled eukaryotic organism including amoebas, ciliates, flagellates, and sporozoans.

Raptors: Birds of prey, hawks, eagles, falcons, owls.

Rate of contact: "C" in the disease spread equation (Equation 1).

Rate of exposure: Disease spread increases with increases in the mixing rate and rate of exposure or rate of contact with infected individuals.

Rate of mixing: Incorporated in "C" in the disease spread equation (Equation 1).

Refugia: A refuge.

Regurgitate: To vomit already consumed food.

Reproductive success: The success of nesting and how many young fledged.

Risk factors: As it applies to passenger pigeons, risk of infection by disease is a function of population density, mixing, disease virulence and mechanisms for spread (billing, communal activities).

Rockies: Rocky Mountains.

Roosting sites: Where birds sit and rest at night when they sleep or during the day after feeding, watering, etc.

Rules of disease engagement: As it applies to passenger pigeons, spread of disease is a function of population density, mixing, disease virulence, mechanisms for spread (billing, communal activities), and a disease reservoir.

Scavenging: Consuming dead animals.

Sentinels: Birds that stand watch and warm their flock's members of approaching danger.

Smallpox: A viral disease in humans.

Spares: Extras, usually sick rock dove that are released to practice shooting skills.

Squabs: Young pigeons usually referred to as birds still in the nest.

Strychnine: A poison used to kill predators such as wolves but can also kill non-target species such as ravens and eagles.

Sulfur pots: Pots of burning sulfur that create thick poisonous smoke used to kill roosting passenger pigeons.

Susceptible/infective/removed (SIR) models: A simple sexual contact model often used to describe disease transmission in networks of individuals.

Sustainable: Capable of being continued or sustained.

Synchrony of breeding: Used by birds in which all the birds in a colony lay their eggs around the same time so as to overwhelm their predators with huge amounts of prey (eggs and chicks).

Transect: A straight line, used by ecologists to collect data.

Trichomonas gallinae: A protozoan disease of birds.

Trichomoniasis: The disease caused by the protozoan, Trichomonas gallinae.

Tuberculosis: A disease found in birds and mammals.

Territory: The part of the home range that is defended against intrusion.

Terrestrial: On land.

Top down control: When species high in the food web, such as predators, has a significant influence on the lower levels of the food web.

Trophic cascade: A chain-reaction within food webs resulting in species composition changes and shifting species dominance and effecting more than one trophic level in a food web.

Turbulence: Disruption of smooth flow of air (or water) past a surface and results in drag.

Ventriculus: The gizzard in birds; a muscular organ that grinds hard foods using the gravel to aid in the grinding process.

Viable population: The segment of a population that continues to reproduce and survive.

Virulent disease models: Mathematical descriptions of infection rate and spread of diseases.

Vocalizations: Birds use their call, or vocalizations, to establish and defend territories and attract mates.

Zoonotic pool: Infections from other species that provide for a potential source of emerging diseases.

INDEX

ABOUT THE AUTHOR

Bruce Wright earned his degree in ecology studying birds of prey at San Diego State University. Bruce is a retired University of Alaska professor where he taught courses about bald eagles, orcas, humpback whales, and brown, black, and polar bears. He was the president of the board of directors of the Bald Eagle Research Institute. When Bruce was a section chief for the National Oceanic and Atmospheric Administration (NOAA) he continued his work with predators in Alaska by managing the Alaska Predator Ecosystem Experiment and the Alaska Shark Assessment Project. Bruce was selected as the chief science advisor to Alaska's Governor Tony Knowles when the governor worked with the Pew Ocean Commission on ocean's issues. Bruce is the executive director of the Conservation Science Institute and Senior Scientist to the Aleutian Pribilof Islands Association. Bruce studied microbiology and diseases in university and worked in a medical laboratory before he switched fields and studied ornithology and became an ecologist. The microbiology, ornithology and ecology backgrounds were all called upon when working on this passenger pigeon book. Learn more about Bruce's work at http://www.environmentalaska.us/.

Other books by Bruce Wright:

I Can't Say (https://www.smashwords.com/books/view/313808)

Alaska Predators; Their Ecology and Conservation (http://www.hancockhouse.com/products/alapre.htm)

## Alaska's Great White Sharks

(http://www.lulu.com/us/en/shop/bruce-wright/alaskas-great-white-sharks/paperback/product-1582380.html)

Bald Eagles in Alaska (http://www.hancockwildlife.org/article.php/Bald-Eagles-In-Alaska-Review)

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