Passenger Pigeons: Stewards of the Hardwood Forests
Introduction
The Passenger Pigeon (Ectopistes migratorius) was the most numerous bird species in North America during the Holocene, comprising 25-40% of the avifauna at the time (9). Its range spanned the Eastern Seaboard from Florida to Quebec in the East and Alberta to Texas in the West (6), wintering in the South (6). Despite the extensive range of the Passenger pigeon they are only known to have bred frequently in an area of 1.2 square kilometers in the north-central hardwood forests situated south of the great lakes, where they would congregate to nest in their billions during spring and summer (6). Phylogenetic analyses place Ectopistes migratorius as a sister taxon to the genus Patagioenas (8, 13), which amongst other species includes the ecologically similar (16, 17) band-tailed pigeon (Patagioenas fasciata). The passenger pigeon is well known compared to other extinct birds as it was studied quite widely by 19th-century naturalists, including the famous American ornithologist John James Audubon, and was included in his masterpiece The Birds of America (9). Even so, many things remain unclear including the famous abundance of the species. The most cited number is 3-5 billion individuals and was an estimate proposed by Schorger author of ‘The Passenger Pigeon: Its Natural History and Extinction’, but it would be more accurate to call it a guess, technological limitations make it impossible to provide even a good ballpark figure. Flock size is also the subject of much debate, they were by all accounts huge with the largest recorded flock being apparently 300 miles long and a mile wide, with an estimated 1-3 billion birds (9)
Much and more has been said about the extinction of the passenger pigeon, but its demise is widely attributed to over-hunting (9, 18), though habitat change (4) and low genetic diversity (11) have also been suggested as contributing factors. Regardless, the extinction was driven by the practices of European colonists and within just a few centuries the most common bird in the region and perhaps the world (9) was no more. The very last surviving individual was famously nicknamed ‘Martha’ and died in captivity at the Cincinnati Zoo in 1914 (9). The passenger pigeon was undoubtedly a keystone species by virtue of its overwhelming abundance and may have shaped its habitat in a plethora of ways, but the exact mechanisms of this are rarely discussed. Perhaps the most significant functions of the passenger pigeon were consuming huge amounts of seeds produced during mast and functioning as either key seed dispersers or predators; Causing large amounts of physical disturbance in forests; producing excessive quantities of excrement to alter the soil chemistry, and contributing to fire regimes.
fig 1. Illustration of a male (below) and female (above) passenger pigeon (Ectopistes migratorious) from James Audobon’s ‘The Birds of America’.
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Seed dispersal and predation
The passenger pigeon was capable of feeding on a wide variety of foods including fruits, crops, and insects (18), but during the Late Holocene the primary food source was mast: nuts which are mass-produced at irregular events known as ‘mastings’. The preferred food source during mastings were beechnuts and acorns (oaknuts). Chestnuts also produce mast in the range of the passenger pigeon, but these were usually only consumed if neither oak nor beech was available (18). A small proportion of the population were crop specialists and fed almost exclusively on maize (Zea mays) grown by the native Americans; after European settlement, the diet probably shifted to a wide array of crops (10). Likely, the landscape most affected by the passenger pigeon was the north-central hardwood forests, the breeding range of the passenger pigeon (6). Breeding sites would follow mast locations, this was an estimated 8% of the breeding area annually and would cover most of the area over the course of 12-13 years (6). Breeding took place during spring and summer and a site would be occupied for about a month (6). The birds could forage in about an 80-160km radius if necessary (18), the amount of mast consumed must have been immense, but was it beneficial or detrimental to the surrounding tree species?
Animals are a common vector of seed dispersion, which aids in reproductive success by enabling offspring to colonize a larger area and not compete directly with the parent tree. Unfortunately, no studies were carried out directly on the role of passenger pigeons as seed dispersers, to replicate the conditions band-tailed pigeons were used as a proxy (16, 17). The study showed that all nuts were destroyed after passing through the digestive tract, and so passenger pigeons could probably not aid in seed dispersal through excretion (16, 17). Other methods of seed dispersal have been suggested, passenger pigeons are known to regurgitate large seeds (18), and in band-tailed pigeons, these were found to remain viable if they were regurgitated within 12 hours of ingestion (16, 17). Similarly, seeds may be present within the crop (An organ for storage of food) of a passenger pigeon when it dies and germinates at the site of death (16, 17). Both these events are low probability, however, due to the sheer amount of pigeons and mast it probably occurred in large numbers.
Despite these mechanisms, the vast majority of ingested seeds were destroyed (16, 17), therefore it must be concluded that the passenger pigeon primarily acted as a seed predator with a detrimental effect on its prey species. Masting is a strategy utilized by some tree species to saturate their prey species by overwhelming them with food availability (16), this is probably what allowed passenger pigeons to thrive in the hardwood forests as they can effectively consume huge amounts of nuts. It is unclear how much of the mast would have been consumed by passenger pigeons, but it would easily have outweighed the pressure placed on the trees by any other seed predator. This pressure may have driven adaptations in the most common masting species or at least benefitted species with pre-existing adaptations that would diminish seed predation. White oak (Quercus alba) germinates in the fall rather than the spring (6), this would seem detrimental as saplings would need to survive winter before attaining much growth, but maybe a payoff for avoiding mass predation during the passenger pigeon breeding season (6). Other species such as the bur oak (Quercus macropana) produce seeds that are altogether too large whilst others like the red oak (Quercus rubra) have somewhere between 13-69% of their seeds too large to be ingested ensuring at least some of their progeny are left untouched (17), to a lesser extent this also applies to black oak (Quercus velutina) and American chestnut (Castanea dentata) (17). American Beech (Fagus grandiflora) is capable of root sprouting as a means of reproduction so is not dependant on seed dispersal (6). For whatever reason, the abundant American Chestnut (Castanea dentata) is less palatable to passenger pigeons and are only widely eaten in the absence of other masting nuts, the cause of this is unclear but it could be an anti-predatory adaptation such as unpleasant taste or the spiny seed capsules (17). Little is known about the effect on non-masting species, but passenger pigeons are known to have fed on 42 different woodland genera (9) and were plentiful during periods in which oak and beech forests were rare (16), likely seed predation pressure was placed on different species at different times.
The question then becomes, if Passenger Pigeons are major seed predators and gather for masting events, why do masting trees dominate the North-Central hardwood forests? Even with the anti-predator adaptations, masting seems poor a strategy against such a plentiful species. The answer is that the masting event attracts the passenger pigeons, which provide other key services to the forest (16).
fig 2. Leaves (left), nuts (right) and nutcases (top right) of the American Chestnut (Castanea dentata). Despite the abundance of the chestnut, the mast of this species is only eaten in the absence of other masting species.
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Canopy disturbance
One of the chief consequences of the huge concentrations of birds is physical damage to vegetation. The massive flocks of passenger pigeons would spend most of the time travelling and foraging but would roost during thunderstorms and at nighttime (6). When roosting they would crowd together on the available vegetation reaching as much as 105,000 birds per hectare weighing a combined 36 metric tons (6). It is reported that this was sufficient to snap many branches under their weight and in some cases bend smaller trees completely to the ground (18). At Breeding sites the pigeon concentrations differed widely (6) owing to variability in the size of these sites (18), even so, large degrees of vegetation disturbance was still reported (18) and populations stayed put for much longer periods than during roosts.
This vegetation disturbance is crucial to the species makeup of a forest, particularly due to canopy disturbance. Damage to the canopy branches allows more light through to the forest floor, these gaps promote the growth of shade-intolerant trees (6). Oaks are notoriously shade-intolerant and require disturbance to grow in forests, likewise, other species like pine (Pinus spp.) and Hemlock (Tsuga canadensis) depend on it and American chestnut appears to benefit from it as well (16). Disturbance-dependent communities seem to dominate in Eastern North America during historical periods (16). Large amounts of vegetation disturbance can even lead to the generation of shrubland, which is a highly biodiverse habitat (14) important to both many species of bird (14) and mammal (15).
Numerous natural processes can cause canopy disturbance including wind and ice storms (6), but passenger pigeons were probably a key to this process as well. Besides anecdotal evidence of damage done by passenger pigeons, we can also observe the growth of shade-intolerant oak trees by examining tree rings, which form annually but will be much wider in periods of rapid growth. As noted, oaks especially have difficulty growing in the absence of direct light (16). A study on white oaks demonstrates that prior to the mid-1600s, rapid bursts of growth occurred on average every 5 years, with the central-northern hardwood forests exhibiting more of these periods, this is in line with the breeding habits of the passenger pigeons (3). In addition to the direct damage to the canopy caused by the passenger pigeon, it probably also compounded with the effect of weather by weakening the structural integrity of trees and branches making them more sensitive to the elements, or vice versa the elements making the trees more sensitive to heavy loads of pigeons (6). As such the detrimental effects caused by seed predation in shade-intolerant species of mast species are probably offset by the immense benefit of consistent canopy disturbance.
fig 3. The white oak (Quercus alba), a common masting species of the North-Central hardwood forests. This species uniquely masts during the autumn, a possible adaptation against the passenger pigeons (Ectopistes migratorious).
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Nutrient Loading
The key functions of the passenger pigeon don’t stop there. When millions of passenger pigeons congregate in a small area, they defecate a lot, especially when you consider breeding sites where the population stays put for about a month. In some cases, fecal matter would accumulate in such high levels that it would cover and kill the forest undergrowth either by blocking out light or poisoning them with uric acid (the bird equivalent of urine) (6). Though this is the most apparent effect it is not the only one, the most profound effect is probably through nutrient loading. Nutrient loading is the deposition of large amounts of nutrients to a system. The nutritional content of pigeon feces is not known, but a study that used common blackbird (Turdus merula) faeces as a proxy estimated that 45kg of Nitrogen, 6.9Kg Phosphorus, and 6.6kg Potassium were deposited per hectare every night during a roost (6), in comparison that’s about 180 times the Nitrogen used in per day per hectare In US agriculture (5). Though this estimate is significantly flawed as passenger pigeons are granivores and blackbirds are insectivores as such the chemistry of the feces would be different (20). If this estimate is even in the ballpark of the true figure the effect on the ecosystem would be profound. Unfortunately, studies of nutrient loading on whole forests, particularly hardwood forests are lacking, large amounts of fertilizer do appear toxic to young oak trees (2) but the effect on fully grown trees and other species is unclear. Perhaps the closest comparison in the modern day is nesting sea bird colonies, these will often congregate on small islands with tiny forests. A Study in Yucatan compared areas with and without nesting sea birds and found that phosphorus and organic carbon levels were much higher at nesting sites, this clearly had an effect on vegetation with a particular tree species, Avicennia germinans, being favored in locations where sea bird colonies were present (1). Similar results were found in the Florida everglades (12). The chief negative pressure on these islands appears to be salinity and not acidity (1). We should be careful about extrapolating too much based on a different biome affected by a different group of birds. It does however illustrate that the nutrient load can change the vegetation structure significantly and it is likely that similar effects were present in the forests of Eastern North America. This aspect of Passenger Pigeon ecology is very understudied and hopefully, future research will shed light on how it has affected the ecosystem.
Fire Regimes
The relationship between passenger pigeons and fire is also an interesting one. The passenger pigeons as mentioned cause large amounts of damage to both the undergrowth via excrement and to branches and trees through physical destruction, as such a large amount of dead plant matter will accumulate on the forest floor which is a good fuel source for wildfires (6). Passenger pigeons could therefore increase the frequency of wildfires. Frequent fires tend to benefit more fire-tolerant species such as the oaks, additionally it can aid in the establishment of species such as the white oak by additionally damaging trees and canopy and allow more light to reach for the forest floor (19). The hardwood forests are not the only forest type in the East that requires frequent fires to thrive, pine barrens and oak savannahs are also heavily dependent on it (7). This applies to animal species too, for example the extinct Bachman’s Warbler (Vermivora bachmanii) is speculated to have been dependent on canes (Arundinaria spp) in the hardwood forests as breeding habitat, canes are fire-dependent and may have suffered in part due to the decline of the passenger pigeon (7). That is not to say that passenger pigeons are the sole or even the main drivers of fires in the region, indeed land use by native-americans and Europeans were probably a bigger factor (7), that said the species probably contributed to the fire regimes during the Holocene.
Fig 4. An illustration of the male (left) and female (right) Bachman’s warbler (Vermivora bachmanii), an extinct species of song bird native to North America. This species was dependent on fire regimes and the extinction of the passenger pigeon (Ectopistes migratorious) may have contributed to its demise.
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Conclusion
The passenger pigeon was undoubtedly a keystone species and an engineer of the Eastern Forests of North America, particularly the North-Central hardwoods in which they would breed every year. It ate the huge amounts of nuts produced by the masting trees and may have driven evolution in the species. Pigeons cleared the canopies and allowed in light to bolster shade-intolerant species. The sheer load of excrement may have changed the very chemistry of the soil and this may have led to fires being more frequent as a result. Yet many of these ideas are based on anecdotal evidence and inferences made from other birds, the problem is that the passenger pigeon is a truly unique species with unique behavior. It, therefore, becomes crucial that we dedicate resources to examine the effects of this lost species so that we may consider the implications on modern American conservation efforts. This need for increased research becomes doubly important when one considers that efforts are already in progress to bring back the passenger pigeon by Revive and Restore, and releasing such a species without a good understanding of its impact on the landscape would be reckless.
Fig 5. Photograph of ‘Martha’ the last known Passenger Pigeon, kept at the Cincinnati Zoo until her death on September 1st, 1914.
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