Feeding Wildlife As a Means of Promoting Animal Welfare

Abstract

Many people propose providing supplemental food to wildlife in order to promote their welfare. However, it is likely that providing supplemental food actually causes wild-animal suffering. While supplemental food has some positive effects, such as improved body condition and nutritional status and lower adult mortality, it also has many negative effects. Some food makes animals sick because it is contaminated or inappropriate for their species. Animals tend to aggregate around sources of food, which makes them vulnerable to disease, predation, and aggression from conspecifics. In the long run, supplemental feeding may also increase population size. At the new, larger population size, animals would no longer benefit from supplemental food; they would need it to prevent a population crash and attendant mortality. Ways to reduce the harm from supplemental feeding when it is necessary are discussed.

Introduction

Humans providing food to wildlife– which is called “supplemental feeding” or “provisioning”– is very common. Wild-animal feeding may benefit humans by increasing populations of hunted species, protecting crops in forestry and agriculture, and allowing humans the ability to photograph or observe wildlife (Dubois, 2014, p. 60). In scientific studies, supplemental feeding may be used to habituate wildlife to humans so they can be observed or to answer ecological questions about what happens when food is not a limiting factor (ibid: 59-60). Feeding may be used to achieve management objectives such as reducing human-wildlife contact, increasing the population of a species that is endangered or desirable to humans (Dubois, 2014, pp. 61 – 62), diverting wildlife from certain areas or food types, and delivering medicine (M. H. Murray, Becker, Hall, & Hernandez, 2016, p. 2). In wildlife tourism, feeding is used to cause wildlife to be predictably viewable at a certain place and time (Dubois, 2014, p. 63).

People may choose to opportunistically feed wildlife they encounter in public places or backyards (Dubois, 2014, p. 65). Humans may experience emotional benefits from feeding wildlife, such as entertainment, a sense of usefulness, aesthetic appreciation, education, being trusted by animals, or simply pleasure from contact with nature (ibid: 59-60). People may feel they have an ethical reason to feed wildlife, such as empathy for wild animals’ suffering, a desire to make up for the harm humans have caused wildlife, or the desire to benefit animals (ibid: 60). By far the most common form of opportunistic feeding is feeding wild birds, such as with a bird feeder or feeding waterfowl (ibid: 65-66). Between one-third and three-fourths of Anglosphere households, depending on the study, sometimes feed wild birds (D. N. Jones & James Reynolds, 2008, p. 2).

Therefore, it is important for wild-animal welfare advocates to know the effects of supplemental feeding on animals. If feeding wild animals is a cost-effective intervention to improve their welfare, we can promote it; conversely, if feeding wild animals is a waste of resources or even harmful to animals, we can oppose it. If certain modifications to feeding can improve animals’ welfare, this may be a cost-effective intervention.

Many wildlife management experts oppose feeding animals because they fear negative consequences to animals and ecosystems. However, there are “few scientifically substantiated reports of negative consequences for the health and viability of provisioned animals” (Orams, 2002, p. 286). Statements that feeding animals is harmful to wildlife are “seldom backed up by research” (ibid: 288). Conversely, other experts argue, “many [unintended effects of provisioning] are complex, take time to manifest and act across trophic levels” (Milner, Van Beest, Schmidt, Brook, & Storaas, 2014, p. 23), which suggests that there may be many unintended consequences we simply don’t know about.

Fecund consumers that mature quickly, such as rodents and songbirds, may respond more quickly to fluctuations in the food base than do ungulates and large carnivores (Barboza, Parker, & Hume, 2008, p. 26). Populations of fecund consumers are likely to be at the carrying capacity before feeding and to rapidly rise to the new carrying capacity once they are supplementally fed. Ungulates and large carnivores benefit from supplemental feeding for a longer period of time. However, deaths from predation may maintain a supply of prey well below food limitation (ibid: 26), particularly in slow-to-mature species, reducing the rate of hunger. In the absence of predation, the food base may be overexploited if the consumer’s production is not tightly linked to food production (ibid: 27). Herbivore populations may increase and crash repeatedly (ibid: 27). High fecundity and rapid maturation in habitats with low or erratic food production can cause a population to run out of food and many animals to starve (ibid: 27).

Wildlife nutrition is notoriously difficult to study, requiring repeated field observations and often captive feeding trials for best results (M. H. Murray et al., 2016, p. 4). The best measurements of nutrition require invasive sampling, and noninvasive sampling has not been shown to correspond with invasive sampling for most animal species (ibid: 4).

Dietary requirements for wild animals are determined through studies of domestic or captive wild animals adjusted for variables such as temperature and movement in the wild (Barboza et al., 2008, p. 15). Food intake may be studied in captive wild animals by measuring how much they eat when provided food ad libitum at a given food quality and temperature (ibid: 53). Many studies assume food is available ad libitum, but this may not be true in certain seasons or due to disturbances like storms (ibid: 53).

Food consumption can be measured directly or indirectly (Barboza et al., 2008, p. 57). Direct methods include observation, telemetry and weighing food before and after the animal consumed it (ibid: 57-60).  Indirect methods include both digestible markers, which are incorporated into tissues, and indigestible markers, which emerge in the feces; both natural and synthetic markers can be used (ibid: 63-64). Fish are typically studied using indirect measures (ibid: 63). The concentration of nutrients in food can be determined by taking representative samples of food consumed (ibid: 60). Measurements of food intake must be made when the animal is in a steady state (ibid: 72). Food consumption is one of the most difficult parameters to measure in wildlife (ibid: 72).

Experiments about supplemental feeding may be unreliable (Oro, Genovart, Tavecchia, Fowler, & Martínez-Abraín, 2013, pp. 9–10):

  • The number of stochastic environmental factors affecting individuals in a population is large and difficult to control (Oro et al., 2013, pp. 9–10).
  • Studies of the same species regularly contradict each other about the effects of feeding on population dynamics (Oro et al., 2013, pp. 9–10).
  • Experiments on feeding when food is abundant may show smaller effects on population dynamics (Oro et al., 2013, p. 10).
  • Experiments involve a subsample of individuals and are often performed at small spatial scales (Oro et al., 2013, p. 10).
  • Experimenters may not control for the fitness of the individual (Oro et al., 2013, p. 10).
  • Both natural and non-natural experiments may be unreliable because it is unclear which animals are actually consuming the food (Robb et al., 2011).
  • Not all studies of supplemental feeding track whether the animals are actually eating the food, which may underestimate the effects of supplemental feeding on population dynamics (Newey, Allison, Thirgood, Smith, & Graham, 2010). When a study of mountain hares compared hares that actually ate the food to hares that did not, hares that ate the food had higher male body mass and survival (ibid),

Natural experiments may be more generalizable (Oro et al., 2013, p. 10).

The majority of supplemental feeding studies focus on animals which weigh less than two kilograms, because their food supply is the most easily manipulated (Boutin, 1990, pp. 203–206). Studies tend to focus on small-bodied herbivores that live in temperate environments (ibid: 216). The cited paper is nearly thirty years old, and while some progress has happened in the past thirty years, small temperate herbivores continue to be overrepresented.

Is Provisioning Effective In Achieving Its Goal?

As populations grow, food becomes limited (Barboza et al., 2008, p. 23). Before populations begin to fall due to lack of food, body condition typically declines, energy and nutrients are less often deposited in fat and lean mass, and body stores of fat or protein may fall below the level needed for breeding (ibid: 24). Declines in body condition of reproductive females may precede declines in population size, especially in species that use seasonal body stores to meet the high demands of pregnancy, egg production, lactation, or incubation (ibid: 25). This suggests that increased population sizes decrease welfare before they regulate the population. Food limitation reduces juvenile survival, decreases growth, and increases mortality, particularly among the young and old, due to their increased susceptibility to weather and disease (ibid: 25). For this reason, there are strong theoretical reasons to believe feeding improves welfare.

Body Condition

In general, provisioning seems to improve body condition.

A review from 1990 found that body weight typically increases when an animal is fed (Boutin, 1990, p. 208). A more recent 2016 review finds ten studies that show a positive effect of feeding on body condition, eight that show a negative effect, and six that show no effect (M. H. Murray et al., 2016, p. 3). Provisioned birds typically have higher body mass, although there are some exceptions (Amrhein, 2014). Urban birds, who are often provisioned, may experience natural selection for lower mass, which creates the illusion that provisioning doesn’t improve their body condition compared to rural birds (ibid).

Studies have suggested that provisioning increases body mass for the following species:

  • Barbary macaques (Borg, Majolo, Qarro, & Semple, 2014; Maréchal, Semple, Majolo, & MacLarnon, 2016).
  • Japanese macaques (Hamada, Watanabe, & Iwamoto, 1996, pp. 321–322)
  • Rats (Banks & Dickman, 2000).
  • Marmots (Woods & Armitage, 2003).
  • Badgers (Kaneko & Maruyama, 2005).
  • Voles (males year-round, females in November through March) (Forbes et al., 2015).
  • Snowshoe hares (males only; one year of two only; 10% heavier, better body condition) (O’Donoghue & Krebs, 1992, p. 634).
  • Red squirrels (male only, second year of feeding only) (Sullivan, 1990, pp. 584–586).
  • Bears (Dunkley & Cattet, 2003, p. 12; Inslerman et al., 2006, pp. 27–29; Massé, Dussault, Dussault, & Ibarzabal, 2014, p. 1232).
  • Deer (15-30% heavier) (Ozoga & Verme, 1982, p. 288).
  • Burrowing owl fledglings (both body mass and structural size) (Wellicome, Todd, Poulin, Holroyd, & Fisher, 2013).
  • Black redstarts (gained instead of lost mass during the nesting season) (Wellicome et al., 2013).
  • Australian magpies (Ishigame, Baxter, & Lisle, 2006, pp. 204–205).
  • Pheasants (maintain fat reserves at winter levels in April while unsupplemented pheasants reduce it by 50%) (Draycott, Hoodless, Ludiman, & Robertson, 1998).
  • Kakapo (Powlesland & Lloyd, 1994, p. 100).
  • Chickadees (0.13 grams heavier) (Margaret Clark Brittingham & Temple, 1988b, p. 584).
  • Crested tits (von Brömssen & Jansson, 1980, p. 175).
  • European starlings (Källander & Karlsson, 1993, p. 1032).
  • Kittiwake chicks (larger; second-born chicks are usually smaller but not if supplementally fed) (V. A. Gill, Hatch, & Lanctot, 2002, p. 10).

It also improved body condition in the following species:

  • Snowshoe hares (during the decline and low phase of their cycle) (Hodges, Stefan, & Gillis, 1999, pp. 3–4).
  • Arctic ground squirrels (Karels, Byrom, Boonstra, & Krebs, 2000).
  • Ungulates (Inslerman et al., 2006, p. 5; Milner et al., 2014).
  • Mule deer (emergency winter feeding) (Baker & Hobbs, 1985, p. 939).
  • Gamebirds (Inslerman et al., 2006, p. 5).
  • Scrub jays (Schoech & Bowman, 2003).
  • Rattlesnakes (including after giving birth) (Taylor, Malawy, Browning, Lemar, & DeNardo, 2005).
  • Damselfish (Booth & Hixon, 1999).

It did not have an effect on the following species:

  • Voles (B. S. Gilbert & Krebs, 1981, p. 330; Haapakoski, Sundell, & Ylönen, 2012).
  • Deer mice (B. S. Gilbert & Krebs, 1981, p. 330).
  • Cotton rats (postpartum) (Doonan & Slade, 1995, p. 819).
  • Newly born snowshoe hares (O’Donoghue & Krebs, 1992).
  • Northern flying squirrels (Ransome & Sullivan, 2004).
  • Elk (fed during winter) (Smith, 2001, p. 176).
  • Elk calves (birth weight only) (Dunkley & Cattet, 2003, p. 12; Smith, Robbins, & Anderson, 1997, p. 35).
  • Magpie nestlings (Hogstedt, 1981, p. 224).
  • Goshawks (Ward & Kennedy, 1996, p. 203).
  • Willow tits (von Brömssen & Jansson, 1980, p. 175).
  • Song sparrows (Peter Arcese & Smith, 1988, p. 216).
  • Alpine accentors (Nakamura, 1995, p. 6).
  • Several species discussed in detail later in this section

There is not a consistent taxonomical trend, and closely related species often have different responses to supplemental feeding.

In part, this may be because “feeding” is not all one thing. For example, the effects of artificial feeding on the condition of deer depends on the density of deer, the severity of the winter, and feeding practices regarding age and sex ratios (Dunkley & Cattet, 2003). Supplemental feeding improves body condition of ungulates proportional to the duration and severity of winter, the quality and quantity of available native forages, the quality and quantity of feed, and how promptly feed was provided (Inslerman et al., 2006, p. 5). Feeding red deer can lead to increased body weights or no significant difference, compared to unfed red deer (Putman & Staines, 2004, pp. 290–291). The effects are believed to depend on complex interactions between sex, age, type of feed, and whether the deer were enclosed or on open range (ibid: 291). Since these factors often vary widely between studies, it is difficult to find a consistent response.

In addition, many studies may not have sample sizes large enough to compensate for the natural variance. For example, there is a lot of variance in goshawk weight, because hatching day is not known precisely, young with inexperienced parents might have a lower growth rate, and birds in large broods may get less food (Ward & Kennedy, 1996, p. 205).

Improved body condition does not necessarily improve an animal’s welfare. The animal may not have been experiencing significant starvation-related stress to begin with. For instance, although control fox pups gained weight more slowly than fed pups, there was no evidence that control foxes were malnourished or starved (Warrick, Scrivner, & O’Farrell, 1999, p. 370). Similarly, no unfed goshawk nestlings were emaciated, showed signs of nutritional stress, or died of starvation (Ward & Kennedy, 1996, p. 205). On the other hand, unfed Australian magpies had higher blood levels of non-esterified fatty acids, which indicate starvation (Ishigame et al., 2006, pp. 204–205).

A larger body mass may indicate that the animal is obese, with associated health problems. Some researchers have expressed concern that the large size of fed Barbary macaques may indicate that they are obese (Borg et al., 2014; Maréchal et al., 2016). At least one out of 21 supplementally fed kakapo may have become obese, although when birds were captured there was no sign of obvious obesity like bumblefoot or lipomas (Powlesland & Lloyd, 1994, pp. 103–104).

There are many reasons why animals’ body condition may not improve if they are supplementally fed, even if they are food-limited. Mareeba rock-wallabies use the energy from food to be more active instead of improving their body condition (Hodgson, Marsh, & Corkeron, 2004). Supplemented wood mice devote the extra energy to improved reproductive output (Díaz & Alonso, 2003, p. 2687). Supplemented female deer may also do so, although the evidence is unclear (Bartoskewitz, Hewitt, Pitts, & Bryant, 2003, p. 1225). Fed fawns have a higher field metabolic rate than unfed fawns, but identical body mass and body fat content (Tarr & Pekins, 2002), which implies that they are burning more energy in some way.

Animals may be able to compensate for the absence of supplemental feeding. For example, bears living in the feeder area gained more mass, but non-feeder bears compensated for short-term differences in spring mass gains with increased foraging later in the year (Partridge, Nolte, Ziegltrum, & Robbins, 2001, p. 198). Thus, supplemental feeding does not appear to produce bears who are larger or in better condition (ibid: 198).

Body mass may increase for some species, just not the species studied. Body mass increased for three of six small mammal species studied when food was added (Meserve, Milstead, & Gutiérrez, 2001, p. 553). One of the species that did not increase was the victim of interference competition by one of the successful species, and the other two were opportunistic species who tend to leave during arid years (ibid: 553). Fed pampean grass mice are heavier and longer and have better winter condition (Cittadino, De Carli, Busch, & Kravetz, 1994, p. 449). However, these results only apply to one of the species, which is larger and competitively dominant; the other species did not respond (ibid: 451). For more information, see the section on non-target species use.

Exclusion may also occur within a species. Male deer who use feed have heavier body mass, with a stronger effect during winter (Bartoskewitz et al., 2003, p. 1224). However, summer feed use increases does’ body mass when they are 2.5 years old, but not at other ages or during winter (ibid: 1224). This may be because bucks exclude does from feeders, although there are other possible explanations (ibid: 1225).

Provisioning may have other negative effects on body condition which outweigh the positive effects of additional food. In particular, increased density may be problematic for many species. Tourist-provisioned stingrays have worse body condition, perhaps because of the stress of group living for the normally solitary stingray (Semeniuk & Rothley, 2008, p. 274). Supplementally fed immature bank voles grew slower and had lower body mass (Löfgren, Hörnfeldt, & Eklund, 1996, p. 389). The growth and body mass of adults did not differ (ibid: 389). The lower body mass was probably due to the increased density and higher contact rates of bank voles on the grid (ibid: 392). Alternately, some studies suggest that bank voles tend to grow more when lower-quality low-energy food is provided, compared to high-quality high-energy food (ibid: 392).

By decreasing mortality, provisioning may allow individuals who otherwise would have died to survive longer, thus causing a lower overall body condition. For example, overwinter feeding was not a strong predictor of spring body mass for blue tits (Kate Elizabeth Plummer, 2011, pp. 82–83). However, blue tits who were less fit survived the winter and were indistinguishable in mass from more fit blue tits (ibid: 82-83), implying a positive effect on less fit blue tits.

Winter food supplementation leads blue tits to produce structurally smaller and lower-weight offspring (K. E. Plummer, Bearhop, Leech, Chamberlain, & Blount, 2013, pp. 2–3). Nestlings of birds fed Vitamin-E-rich food overwinter had the same mass in the early nesting phase but a lower mass later in the nesting process (Kate Elizabeth Plummer, 2011, p. 114). One possible reason is that overwinter feeding misled the parents into believing that food was abundant, causing them to make an unsustainable investment in terms of number of offspring (Kate Elizabeth Plummer, 2011, p. 114; K. E. Plummer et al., 2013, pp. 2–3). Overwinter feeding may also lead to an imbalanced diet or cause lower-quality birds to survive and produce lower-quality offspring (K. E. Plummer et al., 2013, pp. 2–3).

Mortality

Starvation is a common cause of death among animals, which suggests supplemental feeding may improve mortality. In one review, 16 studies showed a positive effect of feeding on survival, 4 showed no effect, and 3 showed a negative effect (M. H. Murray et al., 2016, p. 3). However, this is mostly driven by populations fed for conservation purposes (ibid: 3), which may be particularly likely to be food-limited.

Food supplementation increases survival rate in birds (Boutin, 1990, p. 211; D. N. Jones & James Reynolds, 2008, p. 7; Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 480). Birds fed overwinter have higher chick survival rates, perhaps because the food provides important micronutrients (Robb, McDonald, Chamberlain, Reynolds, et al., 2008). However, it’s important to note that study methodologies typically don’t distinguish between a lower death rate and a lower emigration rate (Amrhein, 2014, p. 30). What looks like higher survival may merely be animals staying near the food. Overwinter feeding may or may not improve survival of mammals (Boutin, 1990, p. 216).

Feeding animals may help them survive in degraded habitats and during periods of natural food shortage (Newsome & Rodger, 2008). Provisioning typically reduces the variance of demographic parameters in response to harsh years (Oro et al., 2013). Thus, anthropogenic food increases a population’s resilience against environmental perturbations and catastrophes, reducing the variance of population growth (ibid: 14). Instead of some years where many animals die and some years where many animals have offspring, provisioned animals have consistent birth and death rates.

Species that have reduced mortality due to supplemental feeding include:

  • Primates (some exceptions due to disease transmission or conflict over food) (Asquith, 1989, p. 148).
  • Bears (fivefold increase in mortality when a dump closes) (Oro et al., 2013, p. 10).
  • Bears (Inslerman et al., 2006, pp. 27–29).
  • Deer (postpartum fawn mortality and adult survival) (Inslerman et al., 2006, p. 5).
  • Mule deer (Peterson & Messmer, 2007).
  • Cottontail rabbits (overwinter; doubled survival rate) (Weidman & Litvaitis, 2011).
  • Northern flying squirrels (posttreatment) (Ransome & Sullivan, 2004).
  • Arctic ground squirrels (adults and juveniles; no change in overwinter survival) (Byrom, Karels, Krebs, & Boonstra, 2000, pp. 1314–1315).
  • Hisipid cotton rats (does not eliminate effect of disturbances such as fire) (Morris, Hostetler, Conner, & Oli, 2011).
  • Mongolian gerbils (colony founders) (Liu, Wang, Wan, & Zhong, 2009).
  • Florida scrub-jays (offspring of provisioned birds) (Schoech et al., 2008).
  • Migratory birds (Inslerman et al., 2006, p. 22)

Species that have unchanged mortality when supplementally fed include:

  • Bighorn sheep (lambs and ewes; with or without parasite treatment) (M. W. Miller et al., 2000, pp. 509–510).
  • Rodents in coastal sand dunes (Koekemoer, 2000).
  • Yukon rodents (exception: juvenile survival in spring) (B. S. Gilbert & Krebs, 1981).
  • Rats (may be emigration rather than death) (Banks & Dickman, 2000).
  • Cotton rats (Doonan & Slade, 1995).
  • Marmots (Woods & Armitage, 2003).
  • Voles (Forbes et al., 2015; Haapakoski et al., 2012).
  • Voles (juveniles) (Schweiger & Boutin, 1995, p. 423).
  • Prairie voles (Cochran & Solomon, 2000).
  • Red squirrels (inconsistent; sometimes adult survival improves) (Sullivan, 1990).
  • Herring gulls (Oro et al., 2013, p. 10).
  • Brown teal ducks (translocated) (Rickett et al., 2013).
  • Chickadees (posttreatment) (Margaret C. Brittingham & Temple, 1992a, p. 192).

Adult survival rates remain stable among a population of seabirds with access to non-commercial fish discarded by fishing boats, but daily feeding rates to chicks increases by 45% (Oro et al., 2013, p. 10). Foxes experience a severe (between 64% and 100%) and rapid reduction in survival when their accidental provisioning is reduced (ibid: 11). This also applies to obligate scavenger birds, with larger effects on specialist species (ibid: 11-12). Opportunistic seabirds who eat fish discarded by fishers have higher survival rates, as do provisioned vultures (ibid: 8).

The probability of a snowshoe hare living for one year in the control area during the decline stage of its population cycle is 0.7% (Krebs et al., 1995, p. 1114). Food addition increases the survival rate to 3.7% and food addition and predator exclusion increase it to 20.8% (ibid: 1114).

Provisioned ungulates have improved survival rates (Milner et al., 2014), typically because of improved juvenile survival and survival during severe winters (ibid: 8). Supplemental feeding consistently improves over-winter survival of ungulates, proportional to the duration and severity of winter, the quality and quantity of available native forages, the quality and quantity of feed, and how promptly feed was provided (Inslerman et al., 2006, p. 5). Elk fed during winter are more likely to survive (Dunkley & Cattet, 2003, pp. 12–13; Smith, 2001, p. 177). However, long, protracted winters still lead to high levels of death among elk (Smith, 2001, p. 177).

Winter mortality rates are higher among unfed deer (Ozoga, 1972, p. 866). Mortality rates among mule deer are highest in the control population and decrease as the feeding level increases (Baker & Hobbs, 1985, p. 940). In a severe winter, it is impossible to reduce total mortality below 20%, even with intense feeding (ibid: 940). This analysis should not be taken to support routine feeding of deer, but instead to support emergency feeding in extreme years (ibid: 940-941).

The Petrel Grade deeryard attracts about 500 deer per year (Ozoga, 1972, p. 861). Over the six years of the study, an average of 42.5 dead deer per year were found, although there was high variance (ibid: 866). 15.83 deer per year were found by highways and railways, so it was not possible to determine whether they consumed supplemental food (ibid: 866). Nineteen per year were found in natural browse areas; of those, the cause of death for 9.69 could not be determined, 4.93 died of predation, 3.81 died of starvation, and 0.56 died of accidents (ibid: 866). 7.67 were found at supplemental feeding sites; of those, the cause of death for 3.3 could not be found, 2.84 died of predation, .83 died of starvation, and .66 died of accidents (ibid: 866).

Overwinter mortality among red deer is primarily explained by late summer rainfall and early winter temperature (Putman & Staines, 2004, p. 292). Other winter weather conditions are also important (ibid: 292). If supplementary feeding is begun early enough to increase autumn body weights, it decreases mortality (ibid: 292). Data on overwinter survival is inconclusive or even contradictory, perhaps because red deer survive most winters well whereas overwinter feeding is primarily important during harsh winters (ibid: 292). It is important that prophylactic feeding begin before deer are malnourished, because irreversible starvation due to protein catabolism begins well before the deer dies, leading to famous cases of deer starving to death surrounded by food (ibid: 294). High mortalities result if food is withdrawn (ibid: 298).

Supplemental feeding may have a positive effect on bird survival. The five-month overwinter survival rate for northern bobwhites was six times higher in feeder areas in one studied winter and two times higher in another studied winter (Townsend et al., 1999). However, in the other winter, the control area had a two times higher survival rate (ibid). Survival rates of chickadees are significantly higher on supplementally fed sites (Margaret Clark Brittingham & Temple, 1988b, p. 584). Supplementally fed chickadees have almost double the overwinter survival rates of unfed chickadees (ibid: 584). The effect was largest when temperatures were severe (ibid: 585). Crow survivorship increases significantly near settlements and campgrounds, rich sources of anthropogenic food, while raven survivorship only mildly increases (Marzluff & Neatherlin, 2006, pp. 306–307). Supplemental food increases overwinter survival of upland game birds; for instance, turkeys without access to feed plots experienced a mortality of 60%, while turkeys with access to feed plots experienced a mortality of only 10% (Inslerman et al., 2006, pp. 15–16).

Feeding willow tits and crested tits causes overwinter survival rates to double (Jansson, Ekman, & von Brömssen, 1981, p. 317). 21% of banded birds in control populations were recovered dead, mostly killed by pygmy owls (ibid: 318). Significantly more tits succumbed to predators in the control population (ibid: 318). There is no evidence that emigration happened; emigration would have caused survival rates to be deceptively high (ibid: 319). However, after food was withdrawn in spring, willow tits had a much higher rate of losses; it is unclear if these are due to death or emigration (ibid: 319).

There are many reasons why feeding may not have a positive effect on mortality rates for some species. For example, feeding low-quality food may cause a deceptively low effect of feeding on mortality rates: fed arctic ground squirrels had unchanged overwinter survival, perhaps because the feed was low-quality (Karels et al., 2000).

Animals may not take advantage of the food. In summer, cotton rat individuals directed most of their additional resources into reproduction, while in winter individuals did not go outside very often because of the harsh winter and thus got little benefit from supplemental food (Doonan & Slade, 1995, p. 824). In one study, feeding did not have an effect on bobwhite mortality, perhaps because almost all the food went to non-target species (Guthery et al., 2004, p. 1251).

If food availability is not a limiting factor for animals, increased supplemental feeding will not change the population. Bald eagle populations are below the carrying capacity, so supplemental food does not increase their survival rates (McCollough, Todd, & Owen, 1994, p. 152). Supplemental feeding does not appear to decrease bobwhite mortality except in certain specific circumstances; if the habitat structure is inappropriate or food is not a limiting factor, there is no effect (Inslerman et al., 2006, p. 16). In addition, bobwhite populations may be limited by insect availability, which is vital for chick survival, in which case no amount of supplemental food will increase survival (ibid: 16). Feeding pheasants does not affect the hens’ survival rate (Hoodless, Draycott, Ludiman, & Robertson, 1999). Hens are most likely to die of fox predation, which is not affected by food availability (ibid).

Supplemental feeding may have an effect on some subgroups but not others. For example, feeding bearded vultures increases the survival rate of non-adults but not of adults, perhaps because adults don’t use the feeding sites because the adults are tied to a territory (Oro, Margalida, Carrete, Heredia, & Donázar, 2008). Female overwinter survival of supplemented wood mice increased but male overwinter survival did not (Díaz & Alonso, 2003, p. 2688). The reason is perhaps that, with supplementation, there was enough food, so the females did not have to compete with males for food (ibid: 2688).

Feeding may have long-term effects different from its short-term effects. Fed adult songbirds were less likely to survive the year after feeding (Peter Arcese & Smith, 1988, p. 128). Feeding may have allowed more birds to survive in the short term, increasing competitive pressure and causing birds to lose their territory (ibid: 133).

Juvenile Mortality

Mortality of juveniles is worth discussing separately, because for many species juveniles may be much more likely to die than adults. Increasing the lifespan of juveniles may allow them to have more positive experiences before death.

Fledging success is the average number of fledglings produced per female bird. While increased juvenile survival increases fledging success, fledging success is also increased if birds lay more eggs or if eggs are less likely to be predated, which wild-animal welfare advocates may not prioritize. Provisioning wild birds may increase fledging success due to more food, but may also generate an ecological trap which lowers populations (Kate Elizabeth Plummer, 2011, p. 22). Most studies show a positive effect of feeding on fledging success (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 478). Supplementary food is likely to increase fledging success in brood reduction species but not in species that adjust clutch size based on food availability (Castro, Brunton, Mason, Ebert, & Griffiths, 2003, p. 278).

In songbirds, food supplementation has indirect effects on nest survival (i.e. the number of nests where all the young die before fledging), possibly because the parents are spending more time guarding the nest and less time finding food, and direct effects on partial clutch loss (Zanette, Clinchy, & Smith, 2006a, pp. 635–637). 15% more fed song sparrow nests produced at least one fledgling (Peter Arcese & Smith, 1988, p. 126). However, this may have been due to larger clutches and higher hatching rate (ibid: 126). Nestlings were lost in twice as many control song sparrow broods as experimental broods, but the difference was not statistically significant (ibid: 127). There was no difference in survival from fledging to independence (ibid: 127).

Crows and ravens fledge more young per pair near settlements and campgrounds, which are excellent sources of anthropogenic food, but jays do not, perhaps because jays are successful both close to and far from settlements and campgrounds (Marzluff & Neatherlin, 2006, p. 306).

Provisioned burrowing owls have more fledglings survive to adulthood; 96% of nestling deaths are a result of starvation (Wellicome et al., 2013). Interestingly, provisioning during the nestling period alone has the same effects as provisioning from before the egg was laid until the birds are fledglings (ibid).

In Mauritius parakeets, supplemental feeding increases fledging success, and the number of fledglings per breeding attempt is significantly higher among supplemented pairs (Tollington et al., 2015).

In kittiwakes, food supplementation increases the number of fledglings (Vincenzi, Hatch, Merkling, & Kitaysky, 2015) and fledging success (V. A. Gill et al., 2002, pp. 8–9). Second-laid chicks survive longer if the parents are fed, but there is no difference for first-laid chicks (V. A. Gill et al., 2002, p. 11).  While kittiwakes supplemented as fledglings die younger (probably because supplementation allows less fit chicks to survive), supplemented nests still produce more breeding adults, because of their higher number of fledglings (Vincenzi et al., 2015). It is still unknown what effect food supplementation has on the long-term reproductive success of kittiwakes (ibid).

The nestlings of food-supplemented magpies were more likely to survive a snowstorm (Dhindsa & Boag, 1990, p. 598) and less likely to die of starvation (ibid: 131-132). Perhaps for this reason, food-supplemented pairs were more likely to produce at least one fledgling, produced more fledglings on average, and produced more fledglings per successful nest, in spite of having a similar clutch size (ibid: 132). Nestling survival rates were significantly higher for fed magpies, with 48% of nests producing at least one fledgling in the unfed group and 88% in the fed group (Hogstedt, 1981, p. 224).

Number of fledglings did not change for fed European starlings (Källander & Karlsson, 1993, p. 1032) or blue tits (Kate Elizabeth Plummer, 2011, p. 134). In one year, the survival rate of treatment and control goshawk nestlings did not significantly differ, but in another year treatment goshawk nestlings had a significantly higher survival rate (Ward & Kennedy, 1996, pp. 203–204). Since most goshawk nestling deaths are due to predation, they may not have been independent; if the nest level is compared, there is no significant difference (ibid: 204).

Starvation was the most important mortality factor in the nesting attempts of one-year-old female alpine accentors (Nakamura, 1995, p. 6). Food supplementation did not reduce rates of starvation (ibid: 6). Starvation typically occurred when there were not enough insects for the birds to eat (ibid: 6). The food may also have been low-quality, as accentors only fed it to their offspring when they couldn’t find other food (ibid: 8). Low-quality food or constraint by something other than feeding may reduce nesting success.

Once food was withdrawn, significantly fewer willow tits fledged per brood in the experimental groups, presumably due to starvation because of the higher willow tit populations caused by excessive food (Jansson et al., 1981, p. 319).  Supplemental feeding of Spanish imperial eagles typically ends when the nestlings fledge (Blanco, 2006, p. 344). Thus, parents may have more fledglings than they are able to take care of, resulting in the death of more fledglings overall as parental work is divided among multiple offspring (ibid: 344). Parents may strive to provision all their offspring at the expense of their own survival or reproductive value (ibid: 345). However, this is quite speculative and further empirical research needs to be done. Both cases suggest a troubling possibility that supplemental feeding may maintain populations above the carrying capacity, causing many deaths once the supplemental feeding is withdrawn.

Winter food supplementation leads blue tits to produce structurally smaller and lower-weight offspring, and thus fledge 8% fewer offspring in spite of their marginal advantage in hatching success (K. E. Plummer et al., 2013, pp. 2–3). Winter-fed parents visited their offspring as often as unfed parents, but seemed to provide fewer and/or lower quality food options (ibid: 4). Winter feeding could have allowed lower-quality parents to survive, caused birds to make unsustainable investments in reproduction in locations that don’t have enough food resources, or led to a nutritionally imbalanced diet (ibid: 4). While Vitamin E supplementation increases the hatching success of blue tits, supplemented birds made an unsustainable investment in hatchling number and wound up fledging fewer nestlings (Kate Elizabeth Plummer, 2011, pp. 113–116).

There have also been some studies of the effect of feeding on juvenile mammals. While the size of successful tropical mice litters did not change, feeding halved the rate of litter failure, leading fed females to produce slightly more pups (Duquette & Millar, 1995, p. 354). While fed and unfed cotton rats have the same postpartum mass, the ratio of postpartum mass to litter mass increases if the cotton rats are fed, which may increase the survival rates of juvenile cotton rats (Doonan & Slade, 1995, p. 823).

Does and bucks have linearly increasing survival with increased feeding, but more intensely fed fawns did not have higher survival rates than less intensely fed fawns (Baker & Hobbs, 1985, p. 940). Fed fawns did have higher survival than unfed fawns (ibid: 940). In another study, provisioning reduced the fawn mortality rate from about one-third to about one-sixth; however, as density increased, fawn mortality rose to 63% (Ozoga & Verme, 1982). Most fawns died within two weeks of birth (ibid: 297). Crowding disrupts maternal behavior, limits fawn-rearing space, or both (ibid: 297-298).

Provisioned arctic fox cubs are less likely to die before weaning, but they are still very likely to die in their first year of life, perhaps because the food was not continued (Angerbjörn, Arvidson, Norén, & Strömgren, 1991). Supplemental feeding significantly increased kit fox survival in one of two years studied; the difference is probably because of the intensification of a coyote control program, which increased the survival rate of control kit foxes (Warrick et al., 1999, p. 570). When supplemental feeding was discontinued, kit fox survivorship reduced to control levels, not below (ibid: 373).

Overprovisioning of dolphins reduces calf survival rates, possibly due to failure of provisioned mothers to nurse their calves enough and to teach calves how to forage (Foroughirad & Mann, 2013, p. 247). While some provisioned bottlenose dolphins do experience higher calf mortality, appropriate provisioning regimes result in higher calf survival rates (Neil & Holmes, 2008). Possible factors to consider include limiting human/animal interaction, limiting provisioning duration to minimize interaction with boats and humans, careful hygiene to prevent disease transmission, and the provision of high-quality fish (ibid: 64-66). Separations between mothers and calves during chases when foraging increase risk of predation on the calf, and increased food intake due to provisioning decreases the risk of malnutrition and starvation (ibid: 65).

Growth Rates

Growth rate typically increases when an animal is fed (Boutin, 1990). Most studies show a positive effect of feeding birds on chick growth rate (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 478).

Species that grow faster if they are fed include:

  • Deer (captive; both adults and calves) (Inslerman et al., 2006, p. 5).
  • Rats (Banks & Dickman, 2000).
  • Magpies (no difference before eight days) (Dhindsa & Boag, 1990).
  • Rattlesnakes (Taylor et al., 2005).
  • Damselfish (captive) (Booth & Hixon, 1999).

Species that experience no change if growth rate if they are fed include:

  • Arctic ground squirrels (juvenile) (Karels et al., 2000).
  • Snowshoe hares (juvenile) (O’Donoghue & Krebs, 1992, pp. 636–637).

Cotton rats grow more quickly if fed in summer, but not if fed in winter, probably because of their season-specific foraging strategies, which involve maximizing growth in summer and minimizing weather and predator exposure in winter (Eifler, Slade, & Doonan, 2003). In spring, males grow faster if fed, but females do not, perhaps because males are better competitors for food (ibid). Pregnant females receiving supplemental food had higher growth rates than unsupplemented females, and dependent pups produced by supplemented mothers had higher growth rates (ibid).

In mice, feeding low-quality oats increased juvenile growth rate, but feeding high-quality sunflower seeds did not (B. S. Gilbert & Krebs, 1981, p. 330). However, this paradoxical result may simply be because many experimental mice may not have been trapped until full-grown (ibid: 330).

Distribution of Food

Studying the distribution of food is important for several reasons. Feed may tend to be consumed by animals that really need it (such as the young and the sick), which would lead to more positive effects than one would naively suppose; conversely, feed may tend to be consumed by older and stronger animals, in which case the effect is more negative. Some researchers find that dominant individuals and their relatives often consume a disproportionate amount of food (Barboza et al., 2008, p. 55).

In many species of birds, young, sick, weak, or otherwise vulnerable animals are more likely to take advantage of supplemental feeding. Young eagles are more likely to use supplemental feeding sites than older eagles are, perhaps because they are less efficient at competing for resources (McCollough et al., 1994, p. 151). Vultures with poor body condition are more likely to visit vulture restaurants (García-Heras, Cortés-Avizanda, & Donázar, 2013). In blue tits, individual variation in food consumption is complex, depending on food availability, population density, social dominance, and natural foraging abilities (Kate Elizabeth Plummer, 2011, p. 131). Female blue tits with lower feather carotenoid concentration (i.e. females with worse diets) and yearlings used provisioned food more, but only in sites provisioned with both fat and Vitamin E instead of just fat (ibid: 131-132). Blue tits that are the least likely to survive overwinter are the most likely to take advantage of feeders (ibid: 132).

In mammals, the situation is more complex. While some mountain hares ate supplemental food and others did not, it was probably unrelated to dominance hierarchies, as there were no age and sex differences in food consumed (Newey et al., 2010, pp. 217–218). In Barbary macaques social rank predicts time spent feeding for juveniles but not for adults (Fa, 2012a, p. 146). Lower-ranking individuals generally have shorter feeding bouts and lower ingestion rates and consume fewer calories (ibid: 146-148). While young and subordinate bears were not more likely to consume supplemental food, adult bears did not exclude young or subordinate bears from eating pellets (Partridge et al., 2001, p. 197).

According to some researchers, subordinate deer are not typically excluded from feeding (Ozoga, 1972, p. 867). Some dominants tolerate considerable crowding, as long as the subordinates are not aggressive (ibid: 867). However, other researchers suggest, if insufficient food is provided to ungulates, adult males will dominate all other animals, and adult females will dominate fawns and yearlings (Inslerman et al., 2006, p. 4). Adult male deer are more likely to use feed than adult female deer, particularly during winter, although there is no difference for juveniles (Bartoskewitz et al., 2003, p. 1222). When bucks are absent, fawns and does eat more food (Grenier, Barrette, & Crête, 1999, p. 331). Bucks generally win conflicts with fawns or does (ibid: 327). There is generally sexual segregation of troughs, with bucks being more likely to eat at some troughs and fawns and does at others (ibid: 332-333). Fawns have better access to food than does, because fawns will take a beating and hold their ground and eventually be tolerated (ibid: 333).

Many deer never visit a feeding station or use the feed (Putman & Staines, 2004, pp. 296–297). Many of those who do visit a feeding station never get a chance to eat anything, and many of those only consume a marginal amount of food (ibid: 297). Deer continue to eat browse even if supplementally fed (Schmitz, 1990, p. 530). This may be because the deer are excluded by larger or more dominant deer (ibid: 530).

Fish tend to be understudied. However, a few Caribbean reef sharks eat the vast majority of the bait, suggesting that dominant sharks tend to consume all the food (Maljković & Côté, 2011, p. 863).

There does not seem to be a consistent gender pattern across species. Female badgers were more likely than males to take advantage of these sources (Kaneko & Maruyama, 2005). Conversely, provisioned male Barbary macaques spend more time feeding than females (Fa, 2012a, p. 146).

Birds with lower levels of neophobia (fear of the new) are more likely to eat at feeders (Herborn et al., 2010/4). It is unclear if neophobic birds will eat at familiar feeders or what the long-term effects of this difference may be.

Anthropogenic food has a particularly large effect when habitat quality is poor or in years with harsh environmental conditions; in highly productive ecosystems, it is mostly used by suboptimal individuals or during times of food shortage (Oro et al., 2013, p. 13). Supplemental food consumption by deer is highest in October and December and when there is inclement weather, and lowest in spring (Ozoga & Verme, 1982, pp. 285–286). Deer gained between 37% and 61% of their diet from the supplement (ibid: 286). Bird feeders are more important to chickadees when ambient temperatures are low, but may be unnecessary in spring (Margaret C. Brittingham & Temple, 1992b, p. 109). However, spring bird feeders may help other species (ibid: 109).

Dependence

Many experts have expressed concern that supplemental feeding of wild animals may cause them to be dependent on humans for food, both because they get less practice in finding food and because there may not be an opportunity to transmit the knowledge of how to find food to another generation (Green & Higginbottom, 2000, p. 188; Higginbottom, 2004, p. 87; Newsome & Rodger, 2013; Orams, 2002; Reese, 2007, p. 41). However, studies suggest that this is not a problem for most forms of feeding (Orams, 2002, pp. 284–285). No study has ever demonstrated dependency in a free-ranging species, although individual animals have become dependent (D. N. Jones & James Reynolds, 2008, p. 267).

Despite common belief, birds do not appear to become dependent on bird feeders, continue to use natural food, and can survive well when feeders are suddenly withdrawn (D. Jones, 2011, pp. 7–8). Birds may become dependent on human-provided food, particularly if feeding causes changes in migration patterns, but some studies suggest mortality rates do not differ between birds who were once fed and are no longer fed and birds who have never been fed (Robb, McDonald, Chamberlain, Reynolds, et al., 2008, p. 481). A similar study has been done on foxes. There is no evidence that fed kit foxes became dependent (Warrick et al., 1999, p. 373). When supplemental feeding was discontinued, kit fox survivorship reduced to control levels, not below (ibid: 373).

The reason that some animals do not become dependent is most likely that they continue to eat natural food, even if supplementally fed. Most provisioned bird species continue to mostly eat natural food (D. N. Jones & James Reynolds, 2008). Natural food dominates the diets of both fed and unfed Australian magpies (O’Leary & Jones, 2006, p. 211). Chickadees generally rely primarily on natural food sources, only occasionally using the feeder, even if the feeder has been provided for 25 years (Margaret C. Brittingham & Temple, 1992a, p. 193). Black-capped chickadees who use winter bird feeders obtain about a fifth of their food requirements from feeders (Margaret C. Brittingham & Temple, 1992b). Song sparrows continue to use natural food even if supplementally fed (Peter Arcese & Smith, 1988, p. 123).

Mammals also choose to consume natural food. Bears who eat food pellets continue to eat grasses, forbs, invertebrates, and other natural foods, even after feeders have been used for several years (Partridge et al., 2001, p. 196). According to hunters who leave out food to increase the bear population, bears typically only use supplemental food when acorns, berries, or other desirable food is not available (Gray, Vaughan, & McMullin, 2004). Provisioned Iberian lynx eat wild rabbits in accordance with their prey’s presence in the population; their consumption of prey did not decrease no matter how long the supplemental feeding happened (López-Bao, Rodríguez, & Palomares, 2010/5). In every documented case of red foxes eating human food, they have also eaten natural food (Reese, 2007, p. 16/17). Scavenged items make up 20-50% of the diet of urban and suburban foxes (ibid: 17). Foxes which beg for food from humans appear to also eat natural food (ibid: 46). However, it is difficult to judge precisely how much human food foxes eat because they are often completely digested with few indigestible remains showing up in scat (ibid: 46). Natural food was found in fifty percent of scats of supplementally fed kit foxes (Warrick et al., 1999, p. 373). Increased availability of food plots does not decrease the percentage of natural forbs in deers’ diets (Hehman & Fulbright, 1997). Mule deer typically switch to native forages as soon as they are available (Inslerman et al., 2006, p. 4). Deer continue to eat browse even if supplementally fed (Schmitz, 1990, p. 530). However, in the case of deer, this may not be due to preference; large feeders may be monopolized by some deer, forcing others to eat browse (ibid: 530).

In a handful of cases, dependence does appear to occur. Stingrays fed by tourists appear to be hungry on days when they are not fed, suggesting that they may be dependent on tourist food (Shackley, 1998, p. 334). This is perhaps because tourist feeding encourages stingrays to aggregate in an unnatural and stressful way (see Other Negative Effects of Aggregation under Health Effects for more). In a handful of cases, deer have been observed coming to rely on the feeding station and no longer foraging themselves (Putman & Staines, 2004, p. 296). This results in lower weights and higher overwinter mortality (ibid: 296). It does not seem clear why deer differ from most animals.

Non-Target Species Use

Non-target species use is the consumption of feed by species other than the species one intended to feed. In some cases, it may be harmless or even desirable, allowing a single feeder to improve conditions for many species of animals. Even if food is consumed by other species, the target species may still benefit: in snowshoe hares, provisioned food appears to go to its intended recipients, even with minimal effort to prevent non-target species use (Wirsing & Murray, 2007). However, in many cases, feeding non-target species may be harmful. It may increase contact between species, including predation (Milner et al., 2014, p. 20). The food may be toxic to non-target species (ibid: 20). Non-target species may not be at risk of starvation, reducing the effectiveness of feeding (ibid: 20). Omnivorous species may consume feed, allowing them to maintain a higher population that leads to more animals dying of predation.

Non-target species use is generally very common, although careful feeder design may ameliorate it. The majority of food produced in food plots intended for game wildlife is consumed by non-game wildlife (Donalty, Henke, & Kerr, 2003). Nontarget species may consume as much as 98% of food at a feeder (Inslerman et al., 2006, p. 28).

Feeding ungulates typically attracts many non-target species (Milner et al., 2014, p. 20). One study found that about half of animals that use bait sites for white-tailed deer are not white-tailed deer (Bowman, Belant, Beyer, & Martel, 2015). Another found that only 8% of visitors to ungulate feeding sites are ungulates; the rest are non-target species (Selva, Berezowska-Cnota, & Elguero-Claramunt, 2014, p. 6). Rodents and lagomorphs consume 56% of the biomass of food plot intended for deer (Donalty et al., 2003). Provisioned food plays only a small role in the diet of red deer in Hungary, in spite of the intensive feeding programs there (Katona, Gál-Bélteki, Terhes, Bartucz, & Szemethy, 2014). However, while this may be because of non-target species use it may also be because the food rots or is trampled into the ground (ibid). Species which commonly visit white-tailed deer feeding sites include passerine birds, mourning doves, and raccoons (Lambert & Demarais, 2001). Exotic ungulates and wild turkey rarely seem to visit white-tailed deer feeding sites, although by the end of the study period exotic ungulates had learned to hop the fence to get food (ibid: 119).

Nontarget species make up 98% of the visitors and 99.6% of the time of feeder use for bobwhite feeders (Guthery et al., 2004, p. 1250). Food spread along fields and intended for the consumption of Northern Bobwhites fed rodents (about half of visitors) and songbirds (about a third of visitors) (Morris, Conner, & Oli, 2010). Remarkably, not a single bobwhite was recorded consuming feed, although this may have been due to quirks of the recording equipment (ibid). When eagles were supplementally fed, they consumed only about 9% of provided carrion (McCollough et al., 1994, p. 151). Crows commonly used eagle feeding sites and may have eaten most of the carrion, but they attracted eagles to the feeding site (ibid: 151). Mammalian scavengers were observed but consumed little food (ibid: 151).

There is a high level of diversity in terms of which birds take provisioned food (Robb et al., 2011), which means it is relatively rare for a home bird feeder to feed only one species of bird. However, non-target species use does not necessarily prevent target species use: for instance, while other species did use song sparrow feeders, they did not prevent song sparrows from eating (Peter Arcese & Smith, 1988, p. 123). Bird feeders may also feed a variety of non-bird species. In Flagstaff, skunks feed at bird-seed feeders at 88% of sites and 68% of nights; next most common are cats (72%/30%) and raccoons (48%/22%) (Theimer, Clayton, Martinez, Peterson, & Bergman, 2015, p. 900). When cat food is added, the number of sites visited by skunks and cats increases by 10%, but raccoons don’t increase at all (ibid: 900). The number of nights visited increases by 27% for skunks, 92% for cats and 70% for raccoons (ibid: 900).

Psychosocial Effects

Individual variance plays a large role in the psychosocial effects of supplemental feeding. For example, there is considerable individual variation in whether supplementing causes bears to be more likely, less likely, or the same amount likely to be nuisances to humans (Steyaert et al., 2014). For this reason, information about psychosocial effects should generally be taken with some skepticism.

Activity Budgets

Supplemental feeding allows animals to spend more time on socializing, resting, and traveling (Orams, 2002). Provisioned animals generally spend less time feeding and moving (Fa, 2012a, p. 145).

Behaviorally, supplementally fed Barbary macaques are indistinguishable from unfed macaques (Fa, 2012a, p. 152). However, provisioned Barbary macaques spend less time foraging (Unwin & Smith, 2010). Supplementally fed Barbary macaques spend 5-7% of their time feeding, while unprovisioned macaques spend half their time feeding (Fa, 2012a, p. 145). There is no difference in time spent allogrooming but provisioned macaques do spend more time resting (ibid: 145). Provisioned Barbary macaques spend more time vigilant (Unwin & Smith, 2010). Disabled baboons with access to anthropogenic food (i.e. through theft or garbage) spend less time feeding than nondisabled baboons, perhaps because they’re choosing to eat high-risk anthropogenic food instead of more difficult to obtain but lower-risk natural food (Beamish & O’Riain, 2014). Thus, in spite of their disability requiring them to spend more time resting and traveling, they spend as much time socializing as nondisabled baboons do (ibid).  Provisioning of primate troops allows them to spend more time on creative and innovative behavior (Asquith, 1989).

Provisioned dolphins do not have a different activity budget, except that they spend less time engaged in calf care (Foroughirad & Mann, 2013, p. 245). The calves of provisioned dolphins spend more time foraging and less time resting, even though their ranges are narrower (ibid: 246). This compensates for the reduction in calf care provided by their mothers.

Provisioned elands spend more time resting, unless there is a food shortage, in which case they continue to forage to meet nutritional needs (Hejcmanová, Vymyslická, Žáčková, & Hejcman, 2013). However, these elands were part of an ex situ conservation program that did not have any predators, and it is unknown how their behavior would change if they had predators (ibid).

Among impalas, provisioning reduced time spent foraging during the dry season, presumably allowing the impalas to increase time spent on rewarding activities such as rest and social behavior (Kurauwone et al., 2013).

Provisioned Mareeba rock-wallabies are more active than unprovisioned rock-wallabies (Hodgson et al., 2004, p. 453). Provisioned individuals spend more time eating, grooming themselves, and performing non-dominant and non-submissive social behaviors such as grooming each other and mutual nose-sniffs (ibid: 453). The increased grooming is probably because they spend more time outside during the daylight, and grooming is a thermoregulatory strategy (ibid: 455).

Provisioned male black redstarts (a species of bird) spent less time foraging and flying and more time preening, singing, and engaged in vigilance, which may represent attempts to find a second mate, given that the abundance of food makes their offspring likely to survive without their help (Cucco & Malacarne, 1997). Provisioned female black redstarts spent more time flying and less time foraging (ibid).

Scrub-jays in suburban environments, who receive supplemental food, spend 11% more time perching and 12% less time foraging than scrub-jays in urban environments (Fleischer, Bowman, & Woolfenden, 2003, p. 519). In spite of this they eat approximately the same amount of food (ibid: 522). Scrub jays fed a high-protein, high-fat diet spent less time foraging and more time engaged in territorial behavior than unfed birds did (Schoech, Bowman, & Reynolds, 2004, p. 569).

Rural (and thus unfed) mute swans spent 48.1% of the daytime eating, while urban swans fed only 4.6% of the time and begged 8.7% of the time (Jozkowicz & Gorska-Klek, 1996). Urban birds spend more time swimming and loafing (28.3% and 36.1%, respectively) than did rural birds (10.2% and 18.4%) (ibid).

Fed hummingbirds perform more dive display bouts, with increased dives per display bout and dives per session (Tamm, 1985, p. 204). Hovering bouts were also more frequent, and both hovering bout duration and hovering time per session increased (ibid: 204). Feeding increased the amount of time hummingbirds spent on their territories, probably due to less foraging pressure (ibid: 205). Dive displays have been traditionally considered to be courtship displays, but some authors consider them to be aggressive, because they occur in interspecific interactions and interactions with other males (ibid: 206).

Fed female song sparrows spent less time off their nests between periods of incubation than did control females (Peter Arcese & Smith, 1988, p. 127). Fed females frequently foraged for short periods and spent much of their off time above the nest, preening and surveying their territory (ibid: 127). Perhaps because of this, rates of cowbird parasitism are strikingly lower in fed birds (ibid: 127).

Provisioned house sparrows spend more time with their mates, reducing rates of extra-pair paternity (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 480).

Seabirds with access to discarded non-commercial fish from fishing trawlers reduce time spent devoted to feeding by 38% (Oro et al., 2013, p. 11). Fed songbirds spend less time foraging (Nagy & Holmes, 2005).

Fed adult female goshawks are seen significantly more often in the nest stand than control adult females (Ward & Kennedy, 1996, pp. 204–205). The presence of the mother at the nest stand deters predators and improves nestling survival (ibid: 206). Fed kittiwakes spend significantly more time guarding their nests, particularly later in the breeding season (V. A. Gill et al., 2002, p. 7). Fed songbirds stay closer to their nests (Nagy & Holmes, 2005). Supplemental feeding increases sentinel behavior in Arabian babblers, which protects them from predators (J. Wright, Maklakov, & Khazin, 2001).

Provisioned birds spend more time singing (Amrhein, 2014, p. 33). Fed songbirds spend more time loafing (Nagy & Holmes, 2005).

Stress

Feeding tends to reduce stress levels in some animals, particularly birds. Fed kittiwakes have lower baseline and stress-induced levels of corticosterone, a stress hormone (Kitaysky et al., 2010). Fed songbirds have lower levels of chronic stress (Zanette et al., 2006a). Feeding lowered both maximum and baseline corticosterone levels, free fatty acid levels (which power the wings), glucose levels (which power the legs), anemia, and the percentage of red blood cells that are immature (ibid: 2475). There was no effect on heterophil to lymphocyte ratio, a commonly used method of measuring immune function in domestic birds, but since this measure has not been validated in wild birds, too much should not be read into it (ibid: 2475-2476). Scrub jays fed a high-protein high-fat diet had lower corticosterone than unfed jays did (Schoech et al., 2004, p. 569). Baseline corticosterone is significantly higher in food-restricted mountain chickadees than in mountain chickadees fed ad libitum (Pravosudov, Kitaysky, Wingfield, & Clayton, 2001, p. 326). There was no statistically significant difference in response to the standardized acute stress of handling and restraint (ibid: 326).

Food-restricted non-molting starlings did not experience any changes in baseline or stress-induced corticosterone or fecal glucocorticoid metabolite levels, suggesting that they did not experience chronic stress due to food restriction (Bauer, Glassman, Cyr, & Romero, 2011, p. 396). However, molting food-restricted starlings showed significant decreases in baseline and stress-induced corticosterone and fecal glucocorticoid metabolites, perhaps indicating a stress response (ibid: 396). (Responses to chronic stress typically differ between molting and non-molting birds (ibid: 391).)This is hard to interpret because in previous studies chronically stressed starlings showed no change in baseline corticosterone, an increase in stress-induced corticosterone, and either no change or an increase in fecal glucocorticoid metabolites (ibid: 396-397). Non-molting birds had an elevated morning heart rate, which may indicate stress, but given the lack of other indicators of stress probably just meant that because their food was restricted later in the day they were eagerly anticipating being allowed to eat again (ibid: 397). Starlings decreased their heart rates when food was removed and increased them when food returned, implying that they were conserving energy and that food removal was not a stressor (ibid: 397). Because periods without food are normal experiences, it is possible that starlings do not find them chronically stressful. This may not be generalizable to birds in the wild as food was ad libitum outside of a four-hour period of food restriction.

Animals generally find high densities fairly stressful. The density of animals around feeding sites is typically higher than it is in more natural situations (for more, see “Aggregation and Disease Transmission”). Four of five studies that measured stress found higher stress levels in provisioned wildlife due to higher densities (M. H. Murray et al., 2016, p. 5). Provisioned ungulates show a higher level of stress (Milner et al., 2014, p. 16). Fed elk have higher levels of fecal glucocorticoids, which are an indicator of stress (Forristal, Creel, Taper, Scurlock, & Cross, 2012). Dispersing feed more broadly did not reduce glucocorticoid levels, possibly because elk still concentrated at the locations with the freshest hay (ibid).

Lower-ranked mountain goats are more likely to win dominance interactions at artificial feeding sites than they are at natural feeding sites, perhaps because the animals were more closely aggregated and thus more likely to be approached from behind (Côté, 2000, p. 952). Given that being of low rank is often a source of chronic stress, this may improve the well-being of low-ranked animals; however, this outcome is very speculative.

Intraspecies aggression

Supplemental feeding may increase the risk of intraspecies aggression because of competition for food (Maréchal et al., 2016, p. 6; Newsome & Rodger, 2008; Orams, 2002).  Increased density of animals can lead to more competitive behavior (Dunkley & Cattet, 2003, p. 13). Fed animals may also be more aggressive to other animals because they have to spend less time foraging (Newsome & Rodger, 2008). Fed animals typically engage in more and more costly territorial displays (Boutin, 1990, p. 206).

Feeding animals may result in natural selection for highly aggressive animals which do well in intraspecific competition for human-provided food (Orams, 2002, p. 286). Highly aggressive animals may cause grave harm to other animals even once the food has been removed.

Mammals

Primates are often more aggressive to each other when provisioned, but it is not clear if that is due to an insufficient amount of food or the animals having to be close to each other (Asquith, 1989, p. 144). Barbary macaques, however, do not have higher rates of scars or injuries when provisioned, implying that they experience less aggression (Maréchal et al., 2016, p. 6; Orams, 2002). While provisioned macaques do experience high levels of stress, this may be because of interaction with tourists, not aggression (Maréchal et al., 2016; Orams, 2002). Provisioned and non-provisioned Barbary macaques show no significant difference in intraspecific aggression (Unwin & Smith, 2010). Barbary macaques typically engage in violence only if they expect to gain energy from it, so provisioning may provide enough food that violence is unnecessary (ibid: 115). Provisioning does cause chimpanzees to be more coercive sexually and rougher with young chimpanzees (Asquith, 1989).

Provisioned ungulates show higher levels of aggression, possibly due to increased density (Milner et al., 2014, p. 16). Provisioning deer significantly increases the rate of interaction between deer (Grenier et al., 1999, p. 327). Deer mostly resolve social strife through dominance hierarchies at feeders (Ozoga & Verme, 1982, p. 295). Conflict was generally resolved through non-contact means (ibid: 295). Social tolerance is common among well-nourished white-tail deer (ibid: 295). However, another study found that 42% of competitive interactions between deer ended in a strike or flail, which may cause injury (Ozoga, 1972, pp. 863–864). In high-density situations adult bucks, particularly yearlings, disrupt normal feeding behavior by vying for dominance (Ozoga & Verme, 1982, p. 296). Even matriarch does had a difficult time maintaining their dominant status in the wake of constant harassment by adult bucks, reducing their ability to eat regularly (ibid: 296-297).

Ungulate aggression increases later in winter (Grenier et al., 1999, p. 331). In one study, two aggressive contacts per hour were noted in February and four in March and April (Ozoga, 1972, p. 864). However, physical contact occurred in 61% of February conflicts, 42% of March conflicts, and 40% of April conflicts (ibid: 864). Hunger in late winter increases competition for food, but due to earlier agonistic conflict, the dominance order has been determined and can be maintained through noncontact interactions (ibid: 864). Adult bucks are the most dominant and does tend to dominate fawns (ibid: 865).

Botos, a solitary species of Amazon river dolphin, are significantly more prone to biting each other when interacting with tourists, presumably because they otherwise would not interact with each other (de Sá Alves, Andriolo, Orams, & de Freitas Azevedo, 2012). The aggression is higher when they are around tourists and not fed (ibid). Provisioned botos form a strict dominance hierarchy, with negative health consequences for the subordinates (ibid). Provisioned botos show a higher level of intraspecific aggression when interacting with humans than do cetaceans who are unhabituated to humans (Scheer, de sá Alves, Ritter, Azevedo, & Andriolo, 2014).

Provisioned Mareeba rock-wallabies perform more aggressive behaviors per hour but do not spend more time performing aggressive behaviors overall (Hodgson et al., 2004)

Feeding red foxes can increase aggressive interactions between foxes, leading to social stress and less group stability (Reese, 2007).

Bears concentrated due to feeding may engage in isolated aggressive behavior to members of their species, including infanticide or cannibalism, but in general do not seem to compete with each other (Inslerman et al., 2006, pp. 27–28).

Birds

Provisioned birds are more territorially aggressive, probably because they have more energy (Amrhein, 2014, p. 33). Provisioned great tits defend their territories more aggressively, whether or not the feeder is in their territory (Ydenberg, 1984, pp. 106–107). Since they have less time pressure from feeding, they can devote more resources to defense (ibid: 106). However, in many bird species, provisioning increases territorial behavior if the resource is in one place, but decreases it if it is spread more widely (Robb, McDonald, Chamberlain, & Bearhop, 2008, pp. 479–480).

Urban mute swans, which are fed by humans, engage in more aggressive behavior than do rural swans (Jozkowicz & Gorska-Klek, 1996).

Feeding Spanish imperial eagles significantly reduces siblicide, the primary cause of death for fledglings, which is usually caused by fighting over food (González, Margalida, Sánchez, & Oria, 2006). However, feeding kittiwakes does not reduce rates of sibling aggression (V. A. Gill et al., 2002, p. 7).

Fish

Provisioned sharks engage in more fights (Clua, Buray, Legendre, Mourier, & Planes, 2010).

Fish fed at a tourism site showed aggression to each other during feedings and had visible scars, potentially because of aggressive behavior during feedings (Brookhouse, Bucher, Rose, Kerr, & Gudge, 2013).

Tourist-provisioned stingrays are more likely to be bitten by members of their own species (Semeniuk & Rothley, 2008, p. 277). The most likely explanation is increased interference competition for food (ibid: 278).

Effects on Offspring

Provisioning causes chimpanzees to be slower to be independent from their parents (Asquith, 1989, p. 145). However, in Japanese macaques, provisioning causes relatives to survive longer, creating a longer matriline (ibid: 145). The presence of additional relatives allows offspring to be independent at an earlier age (ibid: 145).

Bottlenose dolphin calves spend less time in infant position when in the provisioning area compared to when they are not (Mann & Kemps, 2003, p. 302). The calves repeatedly try to get into infant position and do not succeed (ibid: 302). They must sometimes wait half an hour for their mothers to get out of the provisioning area so they may return to infant position (ibid: 302). This is probably because their mothers are busy obtaining fish instead of allowing their calves to nurse or gain contact (ibid: 302). Unlike calves of provisioned females, calves of unprovisioned females are essentially never denied infant position access (ibid: 303). Although it’s unclear what the effect of calves being out of infant position is, some evidence suggests increased provisioning may lower calf body size and increase mortality once a calf has been weaned (ibid: 302).

The offspring of provisioned songbirds have smaller song repertoires, perhaps because their parents have more eggs and devote fewer resources to each egg (Zanette, Clinchy, & Sung, 2009). This reduces the birds’ overall mate quality (ibid).

Effects on Social Structure

Increased food supply may lead to increased aggregation, which has benefits and costs: on one hand, it may lead to decreased vigilance and increased foraging, and on the other hand it may lead to increased aggression and monopolization of food by dominant individuals (Boutin, 1990, pp. 206–208).

Feed grounds lead to unnatural crowding of ungulates and the potential for negative interactions (Inslerman et al., 2006, p. 4). Negative interactions can be minimized by providing unlimited amounts of food to reasonably well-nourished animals (ibid: 4). Artificial feeding disrupts the spatial segregation of deer matrilines by bringing animals from several matrilines together at feeding sites (Blanchong, Scribner, Epperson, & Winterstein, 2006, p. 1038). Genetic analysis finds that artificial feeding leads to unnatural mingling of deer populations (ibid: 1041). In addition to disrupting social structures, this mingling may lead to disease transmission (ibid: 1042).

Feeding has no effect on group size in Barbary macaques (Fa, 2012a, p. 151) or prairie voles (Cochran & Solomon, 2000). Stingrays fed by tourists live in family packs of 12-15 individuals, while unfed stingrays are usually solitary (Shackley, 1998, p. 334). Young stingrays are taught by adults how to behave to get the most food from tourists (ibid: 334).

Fed pheasants have smaller territories and a higher percentage of male birds have territories (Hoodless et al., 1999). The same percentage of males with territories have harems (ibid). Therefore, average harem size is smaller for supplementally fed birds (ibid). There was no indication that females were more evenly distributed among males (ibid).

Provisioning may cause an increase in polygyny in both ungulates (Milner et al., 2014, p. 15) and some birds (Boutin, 1990, p. 208). Since polygyny means most males cannot breed, increased polygyny probably causes wild-animal suffering.

Effects on Foraging

Feeding typically leads to improved foraging. Provisioned birds forage more effectively due to having more energy and less pressure (Kate Elizabeth Plummer, 2011, p. 21). Seabirds with access to discarded non-commercial fish from fishing trawlers reduce foraging range by 50% (Oro et al., 2013, p. 11). Supplemental feeding allows deer to be pickier about what they eat, consuming more nutritious plants, because they don’t experience the pressure of hunger (Brown & Cooper, 2006; Murden & Risenhoover, 1993).

Miscellaneous

Seabirds with access to discarded non-commercial fish from fishing trawlers increase successful copulation by 14% and engage in less interspecific kleptoparasitism (Oro et al., 2013, p. 11).

Provisioned varied tits are less likely to join mixed-species flocks (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 479).

There are no differences in migratory behavior, home range size, or seasonal movements for ungulates (Inslerman et al., 2006, p. 4).

Fed kittiwakes are more likely to receive food from their mates (V. A. Gill et al., 2002, p. 9).

There is no significant difference between philopatry rates in unsupplemented and supplemented prairie vole enclosures, but philopatry increases more over time in unsupplemented enclosures (Cochran & Solomon, 2000). Food supplementation did not lead to an increase in philopatry in a species of mice, perhaps because they already had sufficient food to maintain a high level of philopatry (Teferi & Millar, 1994, p. 117). Provision of food seems to lead to young moving farther away from their home site (ibid: 117-118).

Health Effects

Nutritional Status

42% of studies showed a negative effect of provisioning on nutritional outcomes such as protein or micronutrient deficiencies, while 36% showed a positive effect (M. H. Murray et al., 2016, p. 4). This effect appears to mostly be driven by inappropriate food (ibid: 4-5). Many animals, particularly herbivores, may be fed a diet deficient in protein because people are not aware of their protein needs (ibid: 4-5). Provisioning by tourists or other individual humans is particularly likely to result in animals being fed nutritionally imbalanced food, such as bread and chips in waterfowl and grapes and ground beef in iguanas (ibid: 5). For more on this topic, please see the “Inappropriate Food” section.

Artificial feeding improves the nutritional status of several species, including mule deer (Peterson & Messmer, 2007), many species of birds (Amrhein, 2014, p. 30), macaques (Kurita, 2014, p. 46) and deer (Dunkley & Cattet, 2003, p. 12). In addition, fed magpies consume significantly more food (O’Leary & Jones, 2006, p. 211), which would presumably improve their nutritional status.

The more intensively deer are fed during winter, the higher-quality their diet is (Page & Underwood, 2006, pp. 722–723). Creatinine, which has a direct relationship with muscle mass, is related to lean body weight, and is elevated during nutritional stress and when body fat is low, is lower in fawns who are more intensively fed (ibid: 721). Protein status is also improved for fawns and deer who are more intensely supplementally fed (ibid: 721). A greater proportion of fiber is consumed by deer at unfed or less intensively fed sites (ibid: 721). Level of digestible energy is correlated with intensity of feeding at three of four sites; at the fourth site, deer may have been eating lichen, which has effects on fecal indicators of digestible energy level (ibid: 722).

In blue tits, overwinter feeding was not a strong predictor of the concentrations of carotenoids, an important nutrient, the following spring (Kate Elizabeth Plummer, 2011, pp. 82–83). However, since lower-quality individuals could survive the winter with food supplementation and were not distinguishable from high-quality individuals in carotenoid concentration, we can assume a benefit to low-quality individuals (ibid: 82-83). Nestlings of birds fed Vitamin-E-rich food overwinter did have higher carotenoid levels (ibid: 114-115).

Birds that are fed bird food have overall better health than birds that are not (Wilcoxen et al., 2015). They have an improved heterophil-to-lymphocyte ratio, which indicates that the bird lives in less harsh and more energy-rich conditions (ibid). They have higher levels of subcutaneous fat (ibid). They had greater antioxidant capacity, which influences fertility, growth, immune function, and resistance to aging (ibid). In two studied years the fed birds had a better body condition, improved nutritional condition, and improved immune defense but in one year they did not (ibid). There was no relationship with total plasma protein (which is an index of total protein reserves), haematocrit (which is an indicator of ability to nourish the body with oxygen and of hydration), or reproductive hormones (ibid). After removal of the feeders, birds returned to the status quo, neither more nor less healthy than they were before (ibid).

Provisioned Australian magpies have cholesterol well above the normal range for magpies, although it’s unclear what effects this has on their health (Ishigame et al., 2006, pp. 203–205).

Meadow voles supplemented with high-fat forage had atypically high lipid mass and percent lipid mass and atypically low percent fat-free mass, with no changes in total body mass or fat-free mass (Unangst & Wunder, 2004). This is far above the normal fat range for voles (ibid). It is unclear to me if this is a positive or negative result.

Supplementally fed deer were very healthy, with excellent blood assays and low parasite load (Ozoga & Verme, 1982, p. 295). Supplementally fed fawns had smaller thymus glands than penned fawns, probably indicating a negative energy balance, probably because they preferred natural forage to feeders (ibid: 296). The fawns compensated in winter, when they had to rely on the feeder for food (ibid: 295).

Red-legged partridges fed an energy-rich fiber-poor diet had heavier spleens, lighter gizzards and bursas, shorter long intestines, larger pectoral muscles and higher plasma levels of proteins, glucose, cholesterol, and triglycerides (Millán, Gortazar, & Villafuerte, 2003, p. 85). The effects of heavier spleens and lighter bursas are unclear (ibid: 90). Shorter long intestines and lighter gizzards may reduce survival (ibid: 85). Larger pectoral muscles and higher blood glucose levels may lead to better flying ability (ibid: 90). Plasma proteins, cholesterol, and triglycerides may improve ability to survive starvation (ibid: 90). However, the partridges had a survival rate similar to partridges fed an energy-poor fiber-rich diet (ibid: 87).

Parent birds provisioned with antioxidants have improved antioxidant defenses and lower oxidative stress (Kate Elizabeth Plummer, 2011, p. 22). Males but not females have lower levels of oxidative stress after overwinter Vitamin E supplementation: possibly males used the feeders more, possibly females instead used their Vitamin E to improve egg quality, and possibly the increased attractiveness of supplemented males meant they didn’t have to spend as much time finding food for their young in order to find mates (ibid: 84-85).

Inappropriate Food

Animals may be fed the wrong food or choke on inappropriate food (Green & Higginbottom, 2000, p. 188; Newsome & Rodger, 2008, p. 264, 2013, p. 437). Provisioned food may lack essential nutrients, although few studies have linked this with long-term negative health consequences for animals (Higginbottom, 2004, p. 87). Non-infectious disease occurs when animals are fed foods they can’t digest, that have little nutritional value, or that are spoiled (Dunkley & Cattet, 2003, p. 15).

Bears observed at candy blocks have bad teeth and appear stressed (i.e. moaning and unable to get to their feed when approached by observers) (Inslerman et al., 2006, pp. 29–30). In Japanese macaques, provisioning is correlated with an increased rate of congenital disability, possibly due to the food given (but possibly due to incest or pesticide residue) (Asquith, 1989, p. 147). Provisioning of chimpanzees may have led to protein deficiencies due to excessive consumption of bananas (ibid: 147). Foxes generally eat whole animals, bones and all, which gives them needed calcium and is absent in human-provided meat (Reese, 2007, p. 40).

Many people feed wild waterfowl nutritionally poor food like bread and popcorn (Inslerman et al., 2006, p. 21). While more nutritionally balanced bird food has been developed, there are concerns about bread, the most commonly provided food to birds; it is unknown if bread is helpful, harmful, or neither for birds (D. N. Jones & James Reynolds, 2008, p. 7).

Even seemingly ‘natural’ diets can be inappropriate: for instance, stingrays fed on squid have a significantly different fatty acid composition, which implies their diet is actually highly unnatural (Semeniuk, Speers-Roesch, & Rothley, 2007).

Provisioning by tourists is particularly likely to result in inappropriate food consumption. Anecdotally, a few populations of dolphins, kangaroos, and fish have been fed inappropriate food, which causes them health problems (Orams, 2002, p. 286). Iguanas provisioned by tourists have worse nutritional health (Knapp et al., 2013). Fish fed at a tourism site had high parasite loads, skin lesions, and other signs of ill health; however, these symptoms lessened or disappeared when the tourism operator switched to feeding fish pellets instead of bread (Brookhouse et al., 2013).

One reason provisioning by tourists causes health problems is that tourists are particularly likely to feed animals highly palatable “junk food.” Low-quality food resources that are high in fat or low in protein may impair immune function (Becker, Streicker, & Altizer, 2015). Tourists regularly feed foxes such food, which may cause indigestion, diarrhea, or illness (Reese, 2007, pp. 40–41). For Barbary macaque troops, four percent of provisioned food was unsuitable, while a quarter of tourist-provided food was unsuitable (O’Leary, 1996, p. 183). Unsuitable foods are those which lead to obesity or cavities, such as cake, ice cream, bread, and chips (ibid: 179). Provisioned and natural food is lower-calorie than tourist-provided food (ibid: 184). Tourist-provisioned macaques are noticeably overweight (ibid: 185).

Non-target species use may present problems. For example, non-target animals such as canids and wildfowl eating bear food may find it toxic and possibly fatal (Inslerman et al., 2006, p. 28).

Inappropriate food poses a particular problem for ungulates. Eating large quantities of high-carbohydrate foods, instead of the high-fiber low-carbohydrate woody browse that ungulates typically eat, may lead to rumen acidosis and enterotoxaemia, both of which may result in death (Inslerman et al., 2006, p. 8). Deer switching in winter from roughage to readily fermentable carbohydrate provided by humans may experience rumen overload and rumenitis (Wobeser & Runge, 1975, p. 596). Rumen overload is the term for the acute phase, while rumenitis develops in deer which survive the acute phase  and can cause opportunistic bacterial and fungal infection (ibid: 596). In one study of 108 dead deer, 30 had rumenitis, while five had died of rumen overload or rumenitis (ibid: 597). Rumenitis was associated with a number of other infections (ibid: 597). Of seven deer killed by predators, three may have been unable to flee due to severe rumenitis (ibid: 597-598). Deer with rumenitis were much more likely to have recently consumed grain (ibid: 598). However, experimental mule deer who ate a diet of forage, were starved for five days, and were then fed a supplemental wafer formulated from commercial feeds maintained their body weight and did not experience digestive troubles, diarrhea, lethargy, or bloat (Baker & Hobbs, 1985, p. 938). There were no digestive problems in returning to green grass (ibid: 939). However, both switching to and from the supplemental feed led to soft, consolidated feces for two to three days (ibid: 938-939). The ration provided high levels of energy in easily digested form and sufficient fiber to prevent overeating and acidosis (ibid: 940). This suggests providing appropriately high-fiber feed can eliminate these concerns.

Contamination

Animal feed may be contaminated with substances which harm the animals that eat them. Four of five studies in one review showed a negative effect of contaminants in feed (M. H. Murray et al., 2016, p. 5).

Pesticides may exist on supplemental food. In Japanese macaques, provisioning is correlated with an increased rate of congenital disability, possibly due to pesticide residue (but possibly due to incest or the food given) (Asquith, 1989, p. 147).

Carcasses provided to predators may contain medicine which was used to treat the prey animal while it was alive. Former pet rabbits who had been taking antibiotics when they died were fed to eaglets, which was associated with immunodepression (lowered immune response) and infection by harmful pathogens in the eaglets (Blanco, Lemus, & García-Montijano, 2011). Vultures in India may eat carcasses contaminated with diclofenac, a pharmaceutical used regionally to treat inflammation and fever in livestock (M. Gilbert, Watson, Ahmed, Asim, & Johnson, 2007, pp. 63–64). In vultures, diclofenac consumption causes acute renal failure manifested as visceral gout and responsible for up to 85% of mortality (ibid: 63). Providing uncontaminated carcasses at a vulture restaurant reduces mortality rates from 0.387 birds per day to .072 birds per day (ibid: 73).

Aflatoxin

By far the most-studied contaminant is aflatoxin. Spoiled or rotten feeds may contain poisonous aflatoxins (Inslerman et al., 2006, p. 8). Animals at risk include deer (Brown & Cooper, 2006, p. 521) and migratory birds (Inslerman et al., 2006, p. 22). Corn deliberately left unharvested as a game bird food source may have high levels of aflatoxin (Inslerman et al., 2006, p. 16). Aflatoxicosis affects wild waterfowl, including geese and ducks; infections may occur due to waste food left in fields or due to the use of old corn as bait (Robinson, Ray, Reagor, & Holland, 1982). Birds are not capable of distinguishing contaminated and uncontaminated feed (Inslerman et al., 2006, p. 22) which means human intervention is the only way of ensuring birds eat safe food. Aflatoxin can be produced in feeders, even if the grain itself is aflatoxin-free (Deanna G. Oberheu & Dabbert, 2001, p. 478).

It is difficult to determine how common aflatoxins are in feed. Ten percent of wild turkey feed tests positive for aflatoxins (Schweitzer, Quist, Grimes, & Forest, 2001, p. 658). 17% of bags of birdseed contain a unsafe level of aflatoxin (Henke, Gallardo, Martinez, & Balley, 2001). Less than eight percent of samples of aflatoxin-free corn exposed to various typical environmental conditions developed aflatoxin levels that exceeded a safe limit (C. Thompson & Henke, 2000, p. 176).  Mean aflatoxin levels in feeders are lower than the levels shown to cause mortality or symptoms of aflatoxicosis (Deanna G. Oberheu & Dabbert, 2001, p. 478). However, some individual samples are above that level (ibid: 478). Even at small doses, aflatoxin reduces metabolic efficiency, which can harm animals that rely on metabolic efficiency to survive harsh environments (ibid: 479).

Many species, such as the northern bobwhite, have not been studied to figure out their resistance level (Deanna G. Oberheu & Dabbert, 2001, p. 478). However, wild seeds eaten by northern bobwhites have a higher aflatoxin concentration than supplemental food does, although it is still well below the level hypothesized to cause harm (D. G. Oberheu & Dabbert, 2001). It is possible that other unstudied species have higher levels of aflatoxin resistance.

It is possible for animals to evolve to be resistant to aflatoxin (Pegram, Wyatt, & Marks, 1985), although it is uncertain whether any animals have evolved in this way.

Disease

Supplemental feeding has two contradictory effects on urban animals, and perhaps for animals more generally (Bradley & Altizer, 2007). On one hand, it improves host condition, increases immunity, and decreases pathogen impacts on host survival and reproduction (ibid: 97). On the other hand, it increases pathogen transmission through increasing contact between animals (ibid: 97).

Positive Effects

Energy, protein, and nutrient deficiencies typically decrease immune defence and sometimes lead to immunosuppression (Becker et al., 2015). Fed wildlife may also spend less time foraging and more time on grooming and other defenses against pathogens (ibid). A simple model of provisioning suggests that, for species where provisioning improves immune defense, intermediate levels of provisioning produce the lowest pathogen rates (Becker & Hall, 2014). High levels of provisioning lead to larger host populations and rates of aggregation, which cause the population to have worse disease outcomes than unprovisioned populations (ibid). If provisioning does not improve host condition and immunity, it will worsen pathogen transmission rates (ibid).

Provisioning may also decrease transmission rates by encouraging animals to eat from uninfected food sources or in uninfected places (Becker et al., 2015).

In a handful of species, supplemental feeding has shown a positive effect on parasite prevalence. In wood mice, supplementation decreased prevalence of short-lived parasites but did not affect prevalence of long-lived parasites (Díaz & Alonso, 2003, p. 2688). It is conceivable that the latter is because the experiment was too short to show an effect (ibid: 2688). In the month of April, although not earlier in the spring, fed elk have a lower level of parasites, possibly because of improved nutrition (Hines, Ezenwa, Cross, & Rogerson, 2007, p. 354).

Aggregation and Disease Transmission

Wildlife are attracted to sources of artificial food, which leads to abnormal concentrations of wildlife and closer contact between animals (Becker et al., 2015; Bradley & Altizer, 2007, p. 97; Campbell, Long, & Shriner, 2013; Dunkley & Cattet, 2003, p. 14; Newsome & Rodger, 2008, pp. 262–263). When wildlife interact with each other more often than happens without human intervention, there is a severe risk of increased disease transmission.

Supplemental feeding leads to a variety of risk factors associated with disease transmission, including physical contact between infected and susceptible individuals, exposure to body secretions and aerosol droplets, and contact with contaminated surfaces (Inslerman et al., 2006, p. 5). It also increases disease risk by increasing density and encouraging prolonged and repeated presence at feeding sites (ibid: 5). Animals are attracted to artificial sources of food in higher density than occurs naturally, and competition for food increases contact rates among individuals (Dunkley & Cattet, 2003, p. 14). Stress from crowding reduces immunocompetence in some animals, increasing the likelihood of disease (ibid: 14-15). Provisioning may reduce host movement, leading to year-round pathogen exposure, as well as loss of connectivity with other groups such that pathogens go extinct on short timescales, eventually get reintroduced, and cause large outbreaks (Becker et al., 2015). Increased fecundity and survival of young animals may increase the population of susceptible hosts (ibid). Increased carrying capacity may increase rates of pathogens; however, a meta-analysis suggests it has little effect (ibid).

Backyard bird feeding may lead to disease transmission (D. N. Jones & James Reynolds, 2008; Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 481). Over two years of a study, fed birds were more likely to experience transmissible diseases than unfed birds were (Wilcoxen et al., 2015). After removal of the feeders, birds returned to the status quo, neither more nor less healthy than they were before (ibid).  Feeding ungulates may also increase the rate of disease (Milner et al., 2014, pp. 21–23; Smith, 2001, p. 182)). In particular, deer are not capable of avoiding feces consumption (A. K. Thompson, Samuel, & van Deelen, 2008). Provision of cat food increases contact rates and aggression rates for urban mesocarnivores, potentially leading to injury and increased spread of disease (Theimer et al., 2015, pp. 902–903).

In one meta-analysis, 26 studies showed that feeding increased pathogen prevalence, eight showed no effect, and four showed that it decreased pathogen prevalence (M. H. Murray et al., 2016). Feeding for tourism is the most likely to increase pathogen prevalence, while feeding for conservation is the most likely to decrease pathogen prevalence (ibid: 3). 95% of 29 studies found that provisioning increased pathogen transmission rate (M. H. Murray et al., 2016, p. 6). All ten studies which measured contact rates found that provisioning increased contact rates (ibid: 6).

However, another a meta-analysis found that, while there is significant heterogeneity in infection outcomes, there is no direct effect of provisioning (Becker et al., 2015). That is, while provisioning may affect some populations positively and other populations negatively, overall there is no effect. Pathogen type causes much of the variation, with pathogens spread through close contact or environmental infectious stages having the largest effect (ibid). Intentional feeding leads to more pathogen spread than unintentional feeding does (ibid). It is important to note that not all species increase contact when density increases (Becker et al., 2015), suggesting that there is a good deal of interspecies difference and it may be difficult to generalize about the effects of supplemental feeding on animals.

Specific diseases attributed to artificial feeding include (Dunkley & Cattet, 2003, pp. 15–18):

  1. Bovine tuberculosis in cervids.
  2. Chronic wasting disease in deer.
  3. Bovine brucellosis in elk and bison.
  4. Carbohydrate overload in wild ruminants due to eating highly digestible, low-fiber feed, which leads to a fatal imbalance of the body’s acid-base balance.
  5. Psoroptic mange in elk.
  6. Demodectic mange in white-tailed deer.
  7. Starvation of white-tailed deer when feeding delays migration to winter yards or when feeding is terminated abruptly
  8. Mycoplasmal conjunctivitis in house finches
  9. Salmonellosis in passerine birds due to eating food contaminated with feces
  10. Nutritional deficiencies and metabolic bone disease in birds due to inappropriate food.

#4, #7, and #10 are discussed elsewhere in this paper. I will now explore several well-studied diseases in more detail.

Bovine Tuberculosis

High deer densities at feeding sites lead to increased transmission of bovine tuberculosis among deer (Inslerman et al., 2006, p. 7; R. Miller & Kaneene, 2006, p. 612; R. Miller, Kaneene, Fitzgerald, & Schmitt, 2003; Palmer, Thacker, Waters, Gortázar, & Corner, 2012, p. 3; Schmitt et al., 1997, p. 755). The epicenter of at least one bovine tuberculosis outbreak was the place of highest deer density (Palmer et al., 2012, p. 2). Aggregation of wild boar at artificial feeding and watering sites is associated with an increased prevalence of tuberculosis lesions in both wild boar and red deer (Vicente et al., 2007, p. 458). High bovine tuberculosis rates in one feedground were maintained for decades after the cessation of deer feeding (R. Miller & Kaneene, 2006).

The high transmission rates are caused by direct contact between animals at feeding sites and contaminated food used by large numbers of animals (R. Miller et al., 2003; Vicente et al., 2007, pp. 460–461). At all temperatures, bovine tuberculosis survives on deer feed for up to seven days (Palmer & Whipple, 2006). At 23 degrees celsius, bovine tuberculosis survives for 112 days (ibid). Therefore, food contamination is a likely cause of transmission of bovine tuberculosis among deer (ibid). The bovine tuberculosis bacterium is easily transmitted from deer to deer (Palmer, Whipple, & Waters, 2001, p. 695). After only 69 days of intermingling with infected deer, all deer were infected with the bacterium (ibid: 695). The bacterium was also present in both pelleted feed and hay (ibid: 695).

Brucellosis

Brucellosis is a disease in ungulates which results in miscarriage and nonviable calves (Smith, 2005). Brucellosis is particularly harmful to domestic cattle, to whom elk might transmit it (Smith, 2001, pp. 183–184, 2005). The aggregation of elk at feedgrounds leads to increased transmission of brucellosis (Cross et al., 2010; Smith, 2001, pp. 183–184, 2005). About 30% of fed elk have brucellosis, while almost no unfed elk have brucellosis (Inslerman et al., 2006, p. 6). Hunt areas with supplemental feeding grounds have a higher prevalence of brucellosis (Cross et al., 2010). Brucellosis is generally believed not to be self-sustaining for unfed elk herds (Inslerman et al., 2006, p. 6).

Feedgrounds have a negligible effect on disease transmission for bison, who are already a very gregarious species (Smith, 2005, pp. 10–11).

Brucellosis does not seriously harm ungulate welfare. If anything, it may be useful as a form of contraception. However, it is fairly well-studied, and understanding the dynamics of brucellosis transmission may help us to understand the effects of feeding on disease transmission more generally.

Chronic Wasting Disease

While the exact mechanism of transmitting chronic wasting disease is unknown, it is believed that heavy concentration of ungulates at feed sites increases transmission risk (Inslerman et al., 2006, p. 8). Elk feedgrounds provide an excellent location for the transmission of chronic wasting disease, due to animal crowding and amount of feces on feed sites (Smith, 2005, pp. 16–17).

Conjunctivitis

Congregation at bird feeders caused a conjunctivitis epidemic among house finches (A. A. Dhondt, Tessaglia, & Slothower, 1998). Mycoplasmal conjunctivitis spreads more among finches in seasons with more heavy reliance on bird feeders (Hartup, Mohammed, Kollias, & Dhondt, 1998). Finches that spend more time on feeders have a higher risk of conjunctivitis (Adelman, Moyers, Farine, & Hawley, 2015). Conjunctivitis virus deposited on bird feeders remains infectious for 24 hours but not for 48 hours or longer (André A. Dhondt, Dhondt, Hawley, & Jennelle, 2007).

Finches with conjunctivitis spend longer at feeders because they are less efficient at getting seeds and have a hard time transferring from one feeder to another, probably because their vision is impaired (Hotchkiss, Davis, Cherry, & Altizer, 2005, p. 6). They may also spend more time at feeders because infection makes them rest more and move less (ibid: 6). Infected finches staying longer at feeders could lead to increased transmission rates (ibid: 6). Male finches prefer to feed near conspecifics with conjunctivitis, because the conspecifics are more lethargic and thus less likely to engage in aggressive behavior (Bouwman & Hawley, 2010). (Female finches show no such pattern (ibid).)

Feeders keep house finches from dying of starvation due to contracting conjunctivitis (Fischer & Miller, 2015). Therefore, they may have a positive effect on the welfare of diseased house finches.

Indirect infection, such as occurs when birds are infected by bird feeders, causes much less severe physical signs than direct infection (Hartup et al., 1998). Indirectly exposed birds are less likely to be seropositive for conjunctivitis, their antibodies decline more rapidly, and within forty days of the experiment no indirectly exposed birds had antibodies to conjunctivitis (ibid). This indicates that the conjunctivitis is relatively mild, with a quick recovery (ibid). It can be conjectured that this reduces mortality risk (ibid). Exposure to infected bird feeders may increase immunity to conjunctivitis (ibid).

House finch conjunctivitis is a model system for studying the ecology of wildlife diseases, in part because infection with conjunctivitis is visible (Hotchkiss et al., 2005, p. 2). The dynamics of conjunctivitis may be generalizable to many other feeding situations.

Parasites

Feeding raccoons with clumped resources leads to no change in ectoparasite levels, but a doubling of endoparasite levels (A. N. Wright & Gompper, 2005, p. 152). Feeding raccoons with dispersed resources causes no change in ectoparasite or endoparasite levels (iid: 152). When clumped resources are provided, 11 parasite species increase and two decrease in prevalence, while when dispersed resources are provided, eight species increase and five decrease (ibid: 153).

From January to March, fed elk have a consistently higher level of parasites (Hines et al., 2007, p. 354).

Increased feeder density for wild boar increases gastrointestinal parasite traits (species richness, infection probability and intensity of infection) (Navarro-Gonzalez et al., 2013). It has no effect on pulmonary parasite traits (ibid). The effect size is fairly small (ibid).

Tourist provisioning has particularly negative effects on animals. Tourist-provisioned Barbary macaques had higher levels of endoparasites, either because they were aggregating near the food or because of contact with human feces due to tourists (Borg et al., 2014, pp. 60–61). Iguanas provisioned by tourists have higher rates of endoparasites than iguanas not provisioned by tourists do, probably due to aggregation (Knapp et al., 2013). Tourist-provisioned stingrays have higher parasite loads (Semeniuk & Rothley, 2008, pp. 276–277). However, this is almost certainly due to the extraordinarily large effects of aggregation on stingray health (see “Other Negative Effects of Aggregation”).

Scabies

Scabies causes 20-30 elk to die each winter on the National Elk Refuge in Wyoming (Smith, 2001, p. 182; Sorensen, van Beest, & Brook, 2014, p. 4). Feedgrounds have an unknown role in the transmission of scabies (Smith, 2005, pp. 20–21). Overcrowded conditions caused by feeding may lead to increased transmission of scabies mites (Sorensen et al., 2014, p. 4).

Other

Birdwatchers report approximately one mortality from disease per 21.5 feeder-years (Margaret Clark Brittingham & Temple, 1988a, p. 197). However, this is almost certainly an underestimate, because some birds’ deaths might not have been detected, and other birds might have been killed by predators but have been unable to escape because they were weakened by disease (ibid: 197). Feeders with more birds were more likely to have a death from disease, which may be because there were more feeder-years at those feeders, and may be because the greater aggregation of birds allowed them to spread diseases more quickly (ibid: 198). Most species found dead or dying and all species associated with a greater risk of mortality feed and roost in large flocks, which increases the risk of disease transmission (ibid: 199). Mortality occurs most frequently at platform feeders, where the food is more likely to be contaminated with feces (ibid: 200). However, regardless of feeder type, seeds that fall to the ground and the surrounding vegetation are likely to both be contaminated with feces (ibid: 200-201). While it is hard to distinguish deaths from disease, starvation, and hypothermia, deaths are unlikely to be from starvation next to a bird feeder, and most birds can survive normal cold temperatures fairly well if they have adequate food (ibid: 201).

Concentrations of birds due to feeding may cause transmission of duck viral enteritis (Inslerman et al., 2006, p. 22). Feeding wild turkeys near domestic turkeys risks spreading mycoplasma from domestic turkeys to wild turkeys (ibid: 16).

Ungulate feedgrounds lead to the transmission of septicemic pasteurellosis and bovine paratuberculosis, both of which are potentially fatal (Smith, 2005, pp. 21–23). Septicemic pasteurellosis may or may not be caused by feeding, because feedground elk are also more intensively monitored for disease (ibid: 183). Skin tumors are common in North American deer (Sorensen et al., 2014, p. 4). Some skin tumors are transmitted by tumor cell suspensions coming into contact with open skin sounds (ibid: 4-5). Since feeding can increase the risk of aggressive behavior, it may also increase skin tumor transmission rates (ibid: 5). Selective hunting may reduce the risk of disease transmission because of supplemental feeding, but the evidence is sparse (ibid: 5).

Banana feeding increases the rate of respiratory illness in chimpanzees, but rates of respiratory illness are quite low (Lonsdorf et al., 2011). Banana feeding is positively correlated with respiratory illness rates in the early dry season (ibid: 31). Chimpanzees may be more likely to get bananas during the dry season, when food is limited (ibid: 32).

When infected with B bronchiseptica, a respiratory disease, food-supplemented voles had a higher infection prevalence and more pathological effects associated with infection (Forbes et al., 2015). Food-supplemented voles had lower survival rates (ibid). Aggregation of voles around feeding stations or direct oral contact with feeding apparatuses may have increased transmission of bacteria (ibid). High rates of bacteria re-exposure may have caused higher bacterial burdens and more pathological effects (ibid). Hematological indexes indicative of chronic immune stimulation (leukocytes and monocytes) are elevated in food-supplemented populations (ibid).

Disesed coyotes are more likely to use anthropogenic food (for instance, by killing sheep) (M. Murray, Edwards, Abercrombie, & St Clair, 2015). They are probably unable to eat non-anthropogenic food, which is more difficult for diseased animals to get (ibid). Chimpanzees may also be more likely to get bananas when they’re sick, because it is a low-effort food source (Lonsdorf et al., 2011, p. 32). In coyotes, the wide ranges associated with living on primarily anthropogenic food may cause more exposures to disease (M. Murray et al., 2015). The low-protein diet associated with eating anthropogenic food may cause immunosuppression and increased energy requirements (ibid).

Non-Disease Negative Effects of Aggregation

In one review, three of seven studies found a negative effect of crowding on immune function (M. H. Murray et al., 2016, p. 5).

Increased density of elk may worsen nutrition, lead to sociobehavioral stressors, and reduce immunocompetence (Smith, 2001, p. 182).

Stingrays, a normally solitary species, aggregate when fed by tourists. Tourist-provisioned stingrays have lower hematocrit and total serum proteins, differential leukocrit and leukocyte reactions, and higher levels of oxidative stress (Semeniuk, Bourgeon, Smith, & Rothley, 2009/8). Low hematocrit indicates a higher chance of infections, micronutrient deficiency, or starvation; low total serum protein indicates lower total protein reserves and thus dietary inadequacies; differential leukocrit and leukocyte reactions are correlated with health problems; oxidative stress indicates high levels of environmental stress and energy demand, and is correlated with many diseases (ibid). The stingrays’ poor health is believed to be due to a non-natural diet, higher rates of parasites, and chronically high injury rates (ibid); the latter two are directly caused by the unnatural level of aggregation. Under no circumstances should one ever feed a stingray, and this example suggests caution when feeding other solitary species.

Predation

Feeding wild animals may attract predators to the place where the animals are fed (Newsome & Rodger, 2013; Orams, 2002; Oro et al., 2013, pp. 19–20). This phenomenon is called hyperpredation (Oro et al., 2013, pp. 19–20).

Stingrays experience hyperpredation (Semeniuk & Rothley, 2008, p. 275). Cottontails do not (Weidman & Litvaitis, 2011).

In a chimpanzee troop, provisioning may have led to increased predation on baboons because of close contact between the chimpanzees and baboons; however, this may have also been due to a protein deficiency due to excessive banana consumption (Asquith, 1989). Small rodents do not increase in population when fed because predators are attracted to where they are fed (Oro et al., 2013). Quail supplemental feeding sites attract hawks, due to the increased presence of prey (A. S. Turner, Conner, & Cooper, 2008). Fish feeding appears to increase mortality of prey animals due to aggregation of predators (Milazzo, Anastasi, & Willis, 2006). Bobcats tend to be ten times closer to bobwhite supplemental food sources than one would expect, probably because these food sources also feed a variety of other small herbivores (Godbois, Conner, & Warren, 2004).

On average, participants in a study of predation at bird feeders witnessed one predation death per winter (Dunn & Tessaglia, 1994, p. 14). This is biased because people who didn’t witness predation might not have reported it, and conversely people may have missed predation events (ibid: 14). However, estimates of avian predator population suggest that avian predators kill most of their birds elsewhere (ibid: 14-15). It is unclear whether feeders increase predation risk or decrease it by providing a safe haven for birds (ibid: 16).

In some cases, feeding animals may reduce the rate of predation. Feeding song sparrows reduces the rate of nest predation through allowing song sparrows to engage in more anti-predator behavior (Duncan Rastogi, Zanette, & Clinchy, 2006). Backyard bird feeding may reduce rates of predation through increasing density and allowing animals to devote more resources to avoiding predators (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 481).

Spreading food over a field may reduce risk of attracting predators (Morris et al., 2010). Avian predation at bird feeders is more likely if the feeding area is near a deciduous woodlot, is large, is in a yard with many plantings, operates year round, has more than six feeders, or has more than five types of food (Dunn & Tessaglia, 1994, pp. 11–13). Cat predation is more likely if food is on the ground or feeding practices are unspecialized (ibid: 13). Cats concentrate on what is locally available while avians seek out the most active feeding sites (ibid: 14).

Habituation

Wild animal feeding may cause animals to become habituated to humans (Orams, 2002, p. 285).

Areas full of humans have many dangers which animals have not typically adapted to, such as cars (Newsome & Rodger, 2013; Orams, 2002). Provisioned bottlenose dolphins experience more boat-strikes and fishing line entanglements (Donaldson, Finn, & Calver, 2010). Tourist-provisioned stingrays have higher rates of injuries (Semeniuk & Rothley, 2008), particularly boat-related injuries (ibid: 278). Feeding animals may encourage them to spend more time around human-dominated areas, increasing the risk of collision with vehicles (Green & Higginbottom, 2000, p. 188; Higginbottom, 2004, p. 87; Newsome & Rodger, 2008, p. 263). Animals at risk of being hit by cars include deer (Dunkley & Cattet, 2003, p. 27), bears (Inslerman et al., 2006, pp. 33–34), and red foxes (Reese, 2007, p. 40).

The effect of feeding on animal/vehicle collisions is not uniformly negative. Intercept feeding, in which feeding sites are placed so that they lure animals from the road, may prevent collisions. Intercept feeding probably decreases the rate of deer-vehicle collisions in a cost-effective way, looking only at effects on humans (Wood & Wolfe, 1988). Intercept feeding leads to a 40% reduction in moose-train collisions (Andreassen, Gundersen, & Storaas, 2005, p. 1128). While less effective than forest-clearing it is more effective than scent-marking (ibid: 1128). Intercept feeding of moose, while an effective strategy for reducing collisions, is not cost-effective if you are concerned only with economic benefit (ibid: 1129).

Habituated animals are more likely to approach humans who have ill intent, such as hunters or those who want to attack them (Orams, 2002, p. 285).

While some animals become docile when regularly fed, others become hostile or even dangerous (Higginbottom, 2004, p. 87). Habituated animals may attack humans, causing harm to humans as well as the animal, which might be put down (Dunkley & Cattet, 2003, p. 27; Green & Higginbottom, 2000, p. 188; Newsome & Rodger, 2008, p. 263; Orams, 2002, p. 285). For instance, a dingo fed by tourists killed a child, which led to a dingo cull (Burns & Howard, 2003). Fed turkeys may become aggressive to humans because they expect humans to give them food (Inslerman et al., 2006, p. 19). Feeding bears can habituate them to humans and get them to associate food with human scent, which can result in negative human-bear interactions, bear attacks, and the death of the bear (ibid: 32). Habituated red foxes may injure humans, possibly leading to the fox being killed (Reese, 2007, p. 37). However, it is unclear to me how bad death in a cull typically is; the primary negative effect of this sort of habituation may be on humans.

Contact with humans may also spread disease. Provisioning of chimpanzees may have led to two disease outbreaks due to close contact with humans (Asquith, 1989). In a study of Barbary macaques, provisioned macaques had higher levels of endoparasites, either because they were aggregating near the food or because of contact with human feces due to tourists (Borg et al., 2014, pp. 60–61).

Dolphins fed by tourists are more likely to approach even humans that don’t feed them, leading to an increased rate of risky behaviors (Samuels & Bejder, 2004). One juvenile dolphin fed by tourists engaged in behavior risky to himself once every ten minutes and behavior risky to humans every half an hour (ibid: 73). While one of these behaviors was accepting food, the negative consequences of which is what they set out to prove in the first place, the others are worse (ibid: 72). That dolphin was more likely to be close to humans (which risks disease transmission, injury because the human or dolphin has become aggressive, submissive behavior on the dolphin’s part, and the dolphin or human inadvertently touching vulnerable parts  of the other); be close to vessels (which risks propeller injury, being hit by a moving vessel, or injury from an object); be close to fishing gear (which risks entanglement or being hooked); or be offered an object (which risks that the dolphin will ingest the object and sustain internal injuries). (ibid: 72).

Effects on Offspring

Some researchers argue that provisioning wild birds leads to an increase in egg size and an improvement in egg composition (Kate Elizabeth Plummer, 2011, pp. 20–21). Others claim that studies mostly show no effect on bird egg size and quality (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 478).

The eggs of provisioned buff-throated partridges are larger (Yang et al., 2016). In magpies, supplemental feeding led to a 4.1% increase in egg size (De Neve et al., 2004). When randomized to the feeding condition, magpies laid an egg .33 grams heavier than when they were randomized to the non-feeding condition (Hogstedt, 1981, p. 223). The difference was significant one year but not the other; in the significant year, the fed eggs were 0.89 grams heavier (ibid: 223). The second-laid eggs of fed kittiwakes are larger, but single-egg clutches have smaller eggs, perhaps because lower-quality females are breeding (V. A. Gill et al., 2002, p. 10). Feeding European starlings makes the eggs heavier in some years but not others, possibly because in some years they are less food-constrained (Källander & Karlsson, 1993, p. 1032). In blue tits there is no effect of supplemental feeding on egg size (Nilsson, 1994, pp. 202–203; Kate Elizabeth Plummer, 2011, pp. 49–51).

Fat-provisioned blue tits have smaller egg yolks the following spring, possibly because they don’t get enough antioxidants to make the yolks (Kate E. Plummer, Bearhop, Leech, Chamberlain, & Blount, 2013). Tits who ate the fat had lower-quality eggs, perhaps because they are lower-quality birds, and perhaps because the stress of early laying leads them to reallocate vitamin reserves to self-maintenance (Kate Elizabeth Plummer, 2011, p. 133). Blue tits provisioned with both fat and vitamin E had improved egg quality, probably because of their improved condition due to overwinter provisioning (ibid: 49). This is also true if you look only at the birds that ate the fat and Vitamin E, as opposed to all the birds in a provisioned area (ibid: 133).

Increased deposition of antioxidants in the yolk of wild bird eggs due to provisioning may lead to improved nestling immunity and improved survival and sexual signalling in adulthood (Kate Elizabeth Plummer, 2011). Provisioned nestlings have faster growth rates, improved immunity, and brighter feathers (ibid: 23). Blue tits provisioned with fat but not vitamin E showed improved antioxidant deposition, although oddly birds provisioned with both showed no such effect (ibid: 49). There was no effect of provisioning on egg yolk antioxidant capacity (ibid: 49-51).

The nestlings of fed songbirds showed lower fluctuating asymmetry, which may indicate higher quality (Zanette et al., 2006a, p. 2476).

In general, fed ungulates have improved fetal growth rates (Inslerman et al., 2006, p. 5). However, supplemental winter feeding does not appear to affect elk fetal growth rates, perhaps because it ends before pregnancy is particularly metabolically taxing (Smith, 2001, pp. 176–177). Feeding red deer has no effect on fetal growth rates (Putman & Staines, 2004).

Fed elk have improved lactational performance (Inslerman et al., 2006, p. 5). Providing year-round high-energy food for bears improves milk production (ibid: 29). Feeding red deer increases lactation, which likely increases calves’ gowth rates in spring (Putman & Staines, 2004).

Miscellaneous

Feeding wild animals may cause them to stay for long periods in locations they otherwise would have abandoned (Orams, 2002). For example, provisioned mule deer migrate later in the winter and return earlier in the spring (Peterson & Messmer, 2007). Storks who have access to anthropogenic food may shorten their migration distance or even skip migrating entirely (Flack et al., 2016). This may result in higher survival and fitness for the birds (ibid). However, supplemental food may also cause birds to migrate at inappropriate times or conditions (Inslerman et al., 2006, p. 22). Staying too long in an inappropriate location can cause serious health effects (Orams, 2002). For example, provisioning by humans may keep red wattlebirds from migrating in winter (Paton, Dorward, & Fell, 1983, pp. 152–153). Since there are not enough insects for red wattlebirds to eat in winter, they may acquire a thiamine deficiency (ibid: 152-153). Thiamine deficiency leads to head retraction, convulsions, apathy towards food, and death (ibid: 147).

Provisioning may cause animals to stay at the same location over time, which increases the rates of inbreeding and incest. This phenomenon may occur in sharks (Clua et al., 2010). In Japanese macaques, provisioning is correlated with an increased rate of congenital disability, possibly due to incest (although possibly also due to food given or pesticide residue) (Asquith, 1989, p. 147).

Since provisioning causes earlier laying, provisioned adult birds have more time to molt and lay down fat reserves before winter (Yang et al., 2016).

Provisioned whitetip reef sharks are more likely to approach the top of the water during the day, when non-provisioned whitetip reef sharks are resting, which may harm their overall health, although it’s not clear (Fitzpatrick, Abrantes, Seymour, & Barnett, 2011).

Open or exposed feeding sites lead animals to lose energy standing about in exposed areas (Putman & Staines, 2004, p. 296).

A small study of Barbary macaques suggested that there may be negative health effects of food provisioning by tourists (Maréchal et al., 2016). One Barbary macaque died of food poisoning in the provisioned group and provisioned-group Barbary macaques were far more likely to be lame (ibid: 11). Males (but not females) in the provisioned group were more likely to experience alopecia (ibid: 13). Both sexes experienced higher levels of stress (ibid: 12-13). However, these results may be a product of the stress of interacting with tourists (ibid: 13) and of tourists dropping garbage and failing to take precautions against disease transmission (ibid: 11). In another study of Barbary macaques fed by tourists, provisioned macaques showed poorer coat condition, which may indicate a diet lacking in essential nutrients or may indicate the stress of interacting with tourists (Borg et al., 2014). It is likely that wildlife feeding by individual humans is equally stressful to members of other species.

Effects on Population Dynamics

Supplemental feeding may cause animals to have more offspring. Studies of birds almost never show a downwards effect on population dynamics indicators (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 478). Effects of provisioning may carry over to the next year, increasing the magnitude of the effect (ibid: 478). In one meta-analysis, eleven studies showed a positive effect of feeding on reproduction, while two showed no effect (M. H. Murray et al., 2016). However, this effect is mostly driven by populations fed for conservation purposes (ibid: 3), which may not be representative.

A species may be limited by top-down or bottom-up control (Power, 1992, p. 733). Top-down control means that the species is limited by parasites, predators, diseases, disturbances, or other biotic or abiotic consumers (ibid: 733). Bottom-up control means that the species is limited by resources, primarily food (ibid: 733). The “world is green” hypothesis suggests that most herbivores are limited by top-down control, because green biomass accumulates in mature ecosystems and is not consumed (ibid: 733). In reality, most species’ population dynamics are far more complex and include both top-down and bottom-up components (ibid: 734). However, to the extent that a population is limited through bottom-up control, we can expect food to improve their welfare and increase their population size. To the extent a population is limited through top-down control, we can expect food to leave both population size and welfare unchanged.

Eventually, a fed population will stabilize at a higher carrying capacity (Oro et al., 2013, p. 14). However, the fed animals may not experience higher welfare. While animals may temporarily have positive psychosocial and physical health effects from supplemental feeding, they may reproduce more, leading to a larger population enduring an equal amount of suffering at great expense. One fairly pessimistic writer observes that “supplemental feeding does not prevent malnourishment; it usually just increases the population size at which malnourishment occurs” (Brown & Cooper, 2006).

In fact, an anthropogenic higher carrying capacity may lower wild animal welfare. In nature, populations are limited in various undesirable ways, such as diseases, predators, and food limitation (Gortázar, Acevedo, Ruiz-Fons, & Vicente, 2006). Humans may intervene to limit the effectiveness of these natural means of population control, such as by vaccinating, treating parasites, controlling predators, providing water or, most relevantly for our purposes, feeding (ibid: 84). This intense intervention can lead to overabundance (ibid: 81). Overabundance can be understood through four groups of signs: adverse effects on soil, vegetation, or other fauna; poor body condition or low reproductive performance; increased parasite burdens; and increased infectious disease prevalence (ibid: 84). Overabundance causes negative welfare for many animals and should be avoided. Overabundance can be reduced through increasing hunting or decreasing feeding and other population-increasing interventions (ibid: 85).

Feeding animals may decrease their population size if it creates an ecological trap, a situation where animals are attracted to an environment that lowers their overall fitness (Schlaepfer, Runge, & Sherman, 2002). An example of an ecological trap is food causing animals to aggregate in a place in which they will be eaten by predators (Oro et al., 2013, p. 13). Many feeding-related ecological traps may lower overall welfare: for instance, by leading to the transmission of parasites or diseases. However, if an ecological trap only reduces reproduction– for example, by causing more males to be born than females– it may be a simple method to prevent population growth from supplemental feeding in some species.

In general, food supplementation increases the amplitude of seasonal or multiannual fluctuations in mammal populations, but does not alter the overall pattern (Boutin, 1990, pp. 215–216). The two most consistent results of supplemental feeding are the twofold increase in density and the unchanged general pattern of population dynamics (ibid: 216-217). Possible explanations for these results include factors other than food being limiting, food not being provided to all individuals, most of the increase being due to immigration from outside the study area, and food additions not being conducted continuously for a long enough time over a large enough area to show results (ibid: 217).

It is probable that sufficiently long-term supplemental feeding has some sort of evolutionary effect. For example, supplemental feeding may allow more low-quality adults to survive (Blanco, 2006, p. 346) – e.g., provisioning blue tits with vitamin E allows lower-quality birds to survive to reproduce (Kate Elizabeth Plummer, 2011, p. 80). Relatively rapid evolution can result from evolutionary pressure exerted by humans, perhaps unintentionally (Blanco, 2006, p. 346). This may render the population maladapted for its natural environment (ibid: 346). In addition, even if an animal breeds slowly and thus doesn’t have a short-term population response to increased food, consistent supplemental feeding may select for increased clutch or litter size, more reproductive bouts per reproductive season, or other traits which result in the animal having more offspring in the long run. The evolutionary effect of long-term supplemental feeding has been understudied.

Not all studies of supplemental feeding track whether the animals are actually eating the food, which may underestimate the effects of supplemental feeding on population dynamics (Newey et al., 2010). When a study of mountain hares compared hares that actually ate the food to hares that did not, hares that ate the food had higher fecundity (ibid). We may care more about the effects of having a feeder than the effects of the feeder on any particular animal. However, if only some animals use the feeder, there may be evolutionary effects: for example, supplemental feeding may select for feeder-using hares, thus increasing fecundity on an evolutionary time scale.

Whether additional food tends to go into reproduction or growth depends on the species and sex (Boutin, 1990, pp. 209–211). There are strong differences in the reproductive effects of nutritional stress between kittiwake colonies, suggesting that animals may do the survival/reproduction tradeoff differently within populations and not just within species (Kitaysky et al., 2010). Therefore, an overall generalization may be difficult to make.

Abundance

Animal populations increase to the limits of food and space availability in a density-dependent pattern– that is, the denser they are, the lower the rate of increase (Barboza et al., 2008). Supplemental feeding may increase local carrying capacity (Reese, 2007), increasing a species’ abundance. There is a strong association between population size and availability of anthropogenic food (Oro et al., 2013, pp. 12–13). Food supplemented populations are usually more abundant than control populations, but the timing and rate of population change are similar (Boutin, 1990, p. 216).

Apparent increases in abundance may be due to immigration rather than increased population size: animals are often attracted to food and may choose to live near food. In one study, there were more mouse immigrants on food-supplemented grids (Teferi & Millar, 1994, p. 116). In the decline period of their population cycle, immigration of voles is higher to food grids than to control grids (Schweiger & Boutin, 1995, p. 424). Persistence rates (i.e. how long a vole stays on a particular grid) are higher on food grids but they are far below the persistence rates found prior to peak densities (ibid: 424). However, in a study of tropical mice, food addition did not increase the number of immigrants or how long they stayed (Duquette & Millar, 1995, p. 352), perhaps because this mouse already lived in relatively dense conditions (ibid: 357). The lack of immigration may have caused the observed lack of change in abundance (ibid: 352), suggesting that immigration is a major cause of increases in abundance.

Nevertheless, considerable evidence suggests that supplemental feeding increases populations, at least locally.

Provisioned macaques have higher populations (Kurita, 2014). Gradually decreasing macaque provisioning with an eye towards ending it appears to decrease macaque populations, but in potentially unethical ways (increased infant mortality) as well as morally irrelevant ways (increased age at first birth, decreased birth rate) (ibid: 50). Supplemental feeding of hispid cotton rats increases their abundance (Morris et al., 2011). Population sizes of snowshoe hares on fed grids were on average double those on control grids (O’Donoghue & Krebs, 1992, p. 634. Red squirrels fed for two years had a 3.9 to 4.3 times higher abundance, and although the populations decreased after the cessation of feeding they continued to be higher on experimental grids (Sullivan, 1990). Feeding of stingrays by tourists may have resulted in a population explosion (Shackley, 1998, p. 336).

Food addition increased thorn scrub small mammal populations, but not during an El Nino year in which there was an unusually high amount of food (Meserve et al., 2001, p. 553). Two of the core species, which persist in the thorn scrub even during non-El-Nino years (ibid: 550), increased in population, but one did not (ibid: 553). The one that did not was probably a victim of interference competition by at least one of the other core species (ibid: 553). Quasi-core species, which fluctuate heavily and persist only at low densities during dry years (ibid: 550), increased (ibid: 553). Opportunistic species, which disappear from the thorn scrub in dry years (ibid: 550), were unaffected, perhaps because the two opportunistic species studied were insectivorous and granivorous, respectively, and thus didn’t eat the food (ibid: 553).The addition of food did not successfully prevent the decline of populations in the second year (ibid: 553-554). This could be because of a ‘pantry effect’ where predators are attracted to areas with lots of animals in them, but the declines also affected species which are rarely predated upon, and the animals did not change behavior the way one would expect if they were being predated upon (ibid: 553-554). Instead, this may be because of unsustainably high immigration rates into the food addition grids, which were not able to sustain such high populations (ibid: 554).

Feeding birds increases their abundance (Galbraith, Beggs, Jones, & Stanley, 2015). Bird populations are higher in areas with more bird feeding (Fuller, Warren, Armsworth, Barbosa, & Gaston, 2008). Anthropogenic food increased house crow populations in Singapore (Oro et al., 2013, p. 12). The availability of bird food has a positive direct effect on house finch populations (Fischer & Miller, 2015, p. 49). Finch populations level off at about 40 feeders/km (ibid: 49). Even after conjunctivitis reduced finch populations, there were more finches in places with more feeders (ibid: 50). Feeding willow tits and crested tits leads to populations staying stable or increasing overwinter, instead of decreasing (Jansson et al., 1981, p. 316). Additional food leads to immigration in autumn, but from December onwards extra food does not attract more birds (ibid: 316), suggesting immigration plays a negligible role.

It is believed that food is one of the most important resources driving the increased populations of corvids near settlements and campgrounds (Marzluff & Neatherlin, 2006). Near settlements and campgrounds, 75% of crow feeding bouts are on anthropogenic food (ibid: 309). Steller’s jays near settlements and campgrounds feed on anthropogenic food, but jays far from campgrounds do not (ibid: 309-310). Crows are far more abundant near settlements and campgrounds, while ravens and jays are equally abundant near to and far from settlements and campgrounds (ibid: 306). Notably, this result may be due to supplemental food changing corvid dispersion, rather than a change in population size.

In the short term, food supply typically only has an effect on bird populations when natural food supply is poor; however, this does not apply to longer-lived species or longer-term provision of food (Amrhein, 2014, p. 31). Still, very few studies have been done in urban environments in which bird feeders are the most common, and year-round or over-winter feeding may have different effects than the breeding-season feeding most commonly studied (ibid: 33).

A few studies show a null effect of feeding on abundance. Feeding northern flying squirrels had no effect on their abundance or movement (Ransome & Sullivan, 2004). However, there may have been methodological problems, such as squirrels not being motivated to go into food-baited traps when food is supplemented (ibid). Squirrels were, however, more likely to use nest boxes if they were in a food-supplemented location (ibid). Supplemental feeding of bettongs, a threatened Australian mammal, did not increase the chance of a successful reintroduction, possibly because bettongs are primarily limited by predation (Bannister, Lynch, & Moseby, 2016).

Australian desert rodents had weak reactions to being fed (Predavec, 2000, p. 517). The effects appeared to be short-term and transitory, rather than long-term changes in population dynamics (ibid: 517). One species showed an increase in body mass and within-trip recaptures, while another species showed an increase in within-trip recaptures in one experiment and total captures in another (ibid: 517). Not all the food was consumed, suggesting the population is not food-limited (ibid: 517). Changes in population numbers depended more on remaining food than on amount of food consumed (ibid: 517). The species appear to respond to increased food not by caching food or by coming out of torpor but instead by living near the food rather than in other places (they are nomadic) (ibid: 518). The supplemental food was not able to reverse population decline (ibid: 519-520).

Many studies are short-term, which may cause null results if feeding takes several years to increase abundance. Feeding sharks increases their abundance, even years after supplemental feeding of sharks began (Brunnschweiler & Baensch, 2011).

Population Density

Feeding wild animals may increase population density (Orams, 2002, p. 283). Food supplementation of mammals typically leads to a two- to threefold increase in density, although increases can be as high as tenfold (Boutin, 1990, p. 211). Overwinter feeding results in increased breeding densities for mammals (ibid: 216). Populations are less likely to respond when conditions are fair to good (ibid: 211). The two most consistent results of supplemental feeding are the twofold increase in density and the unchanged general pattern of population dynamics (ibid: 216-217).

It is rather odd that population density would increase without any other population dynamics factors changing. Possible explanations for these results include factors other than food being limiting, food not being provided to all individuals, and food additions not being conducted continuously for a long enough time over a large enough area to show results (Boutin, 1990, p. 217). A particularly thorny issue is immigration from outside the study area, which would lead to a deceptively high estimate of the effect of food on population density. Animals may be attracted to supplemental food, thus increasing the density (Koford, 1992). This may have a major effect on population density in study sites, at least in the short term (Boutin, 1990, p. 217).

Provisioning birds may increase their density, but it’s unclear if this is because of increased birth rates or because of immigration (Amrhein, 2014, p. 31). There are more than twice as many birds in areas with bird feeders, and birds are more likely to spend the winter in cities than in rural areas, because cities have more food (Tryjanowski et al., 2015). Cities have very dense bird populations, but they may still not have enough food; in some places the food demand is so high that it is impossible for scientists to create a rich patch of food (Shochat, Lerman, Katti, & Lewis, 2004, p. 240).

Food experimentally supplied to pheasants increased their densities (Oro et al., 2013, p. 12). Willow tit and crested tit densities were 2.2 times higher in experimental populations compared to control populations (Jansson et al., 1981, p. 319). While deaths increased, there were still twice as many breeding pairs in experimental groups compared to controls (ibid: 319). However, supplemental feeding of chickadees has no effect on densities (Margaret Clark Brittingham & Temple, 1988b, p. 585).

Feeding cotton rats doubles their density, but does not dampen seasonal fluctuations (Doonan & Slade, 1995, p. 818). The number of transients is higher in supplemented populations, but they make up a lower proportion of the overall population (ibid: 819). Control populations have more juveniles and supplemented populations more small adults (ibid: 820). Increased density was due to both increased survival of juveniles and increased immigration (ibid: 823).

In a muroid rodent, added food did not clearly increase population density (Castellarini & Polop, 2002).

When low-quality oats were provided, Yukon rodent densities did not increase (B. S. Gilbert & Krebs, 1981, p. 327). However, when high-quality sunflower seeds were provided, densities became two to three times higher (ibid: 327). When feeding stopped, densities gradually declined to the control level (ibid: 327). Six times as many males and twice as many females of one species immigrated into sunflower-seed areas than into control areas (ibid: 329). In another species, this result was observed in one year but not the other, but again sample sizes are small (ibid: 330). In one case out of four, 44% of change in density can be explained by immigration (ibid: 330). In the other three cases, immigration could have occurred without being detected because there weren’t enough tagged individuals in the source areas (ibid: 330).

In one species of rodent that lives in the Argentinean Pampas, winter food supplementation had no effect on density (Cittadino et al., 1994, p. 448). In another species, densities doubled (ibid: 448). The number of immigrants was significantly greater in July but not in August or September (Argentina is in South America so July is winter) (ibid: 448). Persistence rates were significantly greater from July through August but not from May through July (ibid: 448). The reason only one species responded is probably because it is larger and competitively dominant (ibid: 451). The largest difference in numbers of immigrants between control and supplemented sites corresponded to the peak density on supplemental sites (ibid: 451). Immigration had the largest effect at the beginning, but frost and low temperatures lead to increased survival having the largest effect (ibid: 451).

Food-supplemented vole populations have slightly higher population densities (Forbes et al., 2015). In bank voles, provisioning increases density but does not otherwise change population dynamics (Yoccoz, Stenseth, Henttonen, & Prévot-Julliard, 2001). The density of adult bank vole females and immature voles increased threefold on food supplemented grids and remained the same on control grids (Löfgren et al., 1996, p. 386). However, the density of adult males remained the same on both grids (ibid: 387). Total density was about three times higher in the fed area than in the unfed area (ibid: 387). No adults moved between grids after supplemental feeding started (ibid: 388). The rise in density was not explained by a prolonged breeding season or a higher maturation rate of young voles (ibid: 392). The loss rates of immature bank voles were lower on fed grids than on unfed grids (ibid: 387). The loss rates of adults was the same on both grids (ibid: 387-388). Loss rates can be mostly explained as dispersal from the unfed grid to the fed grid (ibid: 391). Densities of prairie voles increase during the mid- to late-breeding season at a higher rate in enclosures with supplementary food, but at the same rate during the early- to mid-breeding season (Cochran & Solomon, 2000).

Food addition produces densities 1.5 to 6 times higher during the peak and decline phases of snowshoe hares’ population cycle (Krebs et al., 1995, p. 113). Combining food addition with predator exclusion increases density elevenfold, with a peak of 36-fold in the late decline phase (ibid: 113). Late-decline-only food supplementation has unclear effects on snowshoe hare density (D. L. Murray, 1999, p. 52). In winters the effect was marginally significant (ibid: 52). Food did not affect immigration rates or spatial distribution (ibid: 55-56). Food supplementation may have a stronger effect earlier in the population decline– in the late decline there was enough food for all the animals (ibid: 57). Most animals who died died of predation (ibid: 57).

Food supplementation increases arctic ground squirrel densities fourfold (Byrom et al., 2000; Karels et al., 2000) to sevenfold (Karels et al., 2000).

Provisioning typically increases primate populations to some degree, but food availability is generally not the primary limiting factor on primate density, which means the population size increases are relatively small (Asquith, 1989).

Provisioned ungulates typically have higher density (Milner et al., 2014, pp. 7–8). At very high densities, provisioning ungulates reduces density due to year-round use of limited winter ranges or negative impacts on summer or autumn forage density (ibid: 9). However, supplemental feeding may still increase deer density beyond the carrying capacity (Palmer et al., 2012, p. 2).

Wild canids are more dense in human-populated areas with access to dumps (Oro et al., 2013, p. 12). Fed bears have a three times greater density (Inslerman et al., 2006, p. 27).

While many studies do not examine the effects of immigration, immigration consistently accounts for a considerable fraction of the increase in population density. Nevertheless, the increased population densities due to supplemental feeding appear to reflect a genuine increase in abundance.

Overall Reproductive Success

Food provisioning may increase animals’ overall reproductive success, leading to overabundance. Unlike increased survival, which delays death but can also cause overabundance, under many sets of values there is no benefit to increasing wild animal reproductive success at the cost of their welfare.

Some studies show that artificial feeding improved reproductive success of black bears, ungulates, white-tailed deer, bald eagles, and white-tailed eagles, but other studies suggest that it does not improve reproductive success for bald eagles and elk (Dunkley & Cattet, 2003, p. 12). Many researchers are concerned about artificial feeding because of the risk of population growth exceeding the carrying capacity of the range (ibid: 12).

Provisioning of food seems to improve the reproductive success of birds (Amrhein, 2014, p. 32). Provisioning birds increases yearly reproductive output often but not always (D. N. Jones & James Reynolds, 2008, p. 7). According to a meta-analysis, food supplementation in birds increases the breeding success of the birds (Ruffino, Salo, Koivisto, Banks, & Korpimäki, 2014).

There are several reasons that supplemental feeding might increase reproductive success. For example, supplemental feeding of Florida scrub jays significantly increases their reproductive output due to increased opportunities for renesting after a failed nest due to earlier laying, increased clutch size, and increased investment in parental care (Schoech et al., 2008, p. 351). Exact mechanisms for increased reproductive success due to feeding will be discussed more completely in later sections.

Species that have a higher rate of reproductive success when fed include:

  • Ungulates (reproductive rate) (Milner et al., 2014, pp. 7–8).
  • Deer (doe reproductive status switches from poor to fair) (Ozoga & Verme, 1982, p. 297).
  • Bears (cub productivity, fecundity, reproductive success) (Inslerman et al., 2006, pp. 27–29).
  • Tropical mice (lifetime productivity) (Duquette & Millar, 1995, p. 354).
  • Voles (fed population had 39 new voles, unfed population 0) (Forbes et al., 2015).
  • Hihi (productivity) (Castro et al., 2003, p. 278).
  • Songbirds (annual reproductive success) (Zanette et al., 2006a, p. 637).
  • Song sparrow (four times more independent offspring) (Peter Arcese & Smith, 1988, p. 127).
  • Seabirds (breeding success; when food is dumped from fishing boats) (Oro et al., 2013, p. 11).
  • Kittiwakes (productivity) (V. A. Gill et al., 2002, pp. 8–9).
  • Kittiwakes (number of fledglings) (Vincenzi et al., 2015).
  • Upland gamebirds (number of offspring) (Inslerman et al., 2006, p. 15).
  • Migratory birds (reproductive success) (Inslerman et al., 2006, p. 22).

Species that have an unchanged rate of reproductive success when fed include:

  • Snowshoe hares at population peak (total reproductive output) (O’Donoghue & Krebs, 1992, p. 636).
  • Alpine accentors (young fledged per nest or per year) (Nakamura, 1995, pp. 5–6).

A few animals do not appear to respond to supplemental food with increased reproductive success. For example, supplementation appears to have no effect on the reproduction, survival, or breeding success of Iberian lynx (López-Bao, Palomares, Rodríguez, & Delibes, 2010). However, this is probably because the population is so small that the negative effects of small populations outweigh any effect of supplemental food (ibid). We presumably do not only want to feed very small populations. Feeding red deer does not increase fecundity, perhaps because of density-dependent reduction in reproductive rates (Putman & Staines, 2004, p. 291). However, since many animals find high densities unpleasant or aversive, this solution is unsatisfactory.

Earlier Breeding

Food supplementation tends to advance or extend breeding seasons (Boutin, 1990, p. 208).

Feeding birds consistently seems to cause them to breed earlier (D. Jones, 2011; D. N. Jones & James Reynolds, 2008, p. 7; Kate Elizabeth Plummer, 2011, pp. 20–21; Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 477). Fed magpies initiate each phase of breeding significantly earlier (O’Leary & Jones, 2006) and lay their eggs three (De Neve et al., 2004; Hogstedt, 1981, p. 221) to seven (Dhindsa & Boag, 1990, p. 597) days earlier. Suburban scrub-jays, who eat food that humans provide, breed earlier than rural scrub-jays (Fleischer et al., 2003, p. 518). Human-provided food allows scrub-jays to lay eggs earlier (Schoech & Bowman, 2003). Supplemental feeding of European starlings advances lay dates by five days (Källander & Karlsson, 1993, p. 1032).

Kittiwakes lay their eggs earlier if fed (V. A. Gill et al., 2002, pp. 9–10) and delay laying in times of nutritional stress (Kitaysky et al., 2010). Fed alpine accentors breed earlier (Nakamura, 1995, p. 7). Fed pairs of song sparrows laid on average 18 days before controls (Peter Arcese & Smith, 1988). Song sparrows who are fed have a more synchronous lay date, while controls are more variable (ibid: 124). Supplemental feeding of kingfishers causes them to lay their eggs earlier (Kelly & Van Horne, 1997, p. 2507). However, if too little supplemental food is provided and feeding begins in April rather than March, there is no effect (ibid: 2507-2508).

If supplementally fed, willow tits lay two to five days earlier, and crested tits lay five to eight days earlier (von Brömssen & Jansson, 1980, p. 175). Supplementally fed willow tits’ second clutches were also laid seven days earlier (ibid: 175). Fed blue tits lay their eggs four ((Svensson & Nilsson, 1995, p. 1809) to six (Nilsson, 1994, p. 202) days early. Lay dates do not advance in high-quality territories that have already reached the food saturation point, and additional food past the amount necessary to reach the saturation point does not lead to further advancement of lay dates (Svensson & Nilsson, 1995, p. 1810). Laying date did not change when blue tits were fed fat (Kate Elizabeth Plummer, 2011, p. 112). However, blue tits that actually consumed the supplemental food did have earlier lay dates, whether they ate fat or fat plus Vitamin E, suggesting that increased energy leads to earlier lay dates (ibid: 133).

Supplemental feeding does not affect the lay date of kakapo (Powlesland & Lloyd, 1994) or pheasants (Hoodless et al., 1999).

Of 20 studied bird species which were supplementally fed, 15 showed an advancement in laying date (Meijer & Drent, 1998, p. 409). In ten species, the laying date was advanced about a week (ibid: 409). In four species, the laying date was advanced three to four weeks (ibid: 409). All of those species have long laying windows of three to four months, and three of the four species were multi-brooded (ibid: 409). Of the species that did not show an advancement in laying date, three were not fed long enough to have an effect and two were gulls, a colonially breeding species (ibid: 409). Colonially breeding species are typically very synchronized in lay date (ibid: 409).

Over-winter feeding makes lay dates earlier, possibly because the over-winter feeding convinced birds that there was more food (Robb, McDonald, Chamberlain, Reynolds, et al., 2008). Birds fed a high-protein high-fat diet bred earlier than those fed a low-protein high-fat diet, and unfed birds bred latest (Schoech et al., 2004, p. 568). Lower-latitude birds are more likely to advance their egg-laying date in response to supplemental food than are higher-latitude birds (Schoech & Hahn, 2007).

Supplemental feeding may also cause mammals to breed earlier. Mammal species which breed earlier if fed include:

  • Ungulates (Inslerman et al., 2006, p. 5).
  • Snowshoe hares (one week earlier) (O’Donoghue & Krebs, 1992, p. 634).
  • Arctic ground squirrels (juvenile emergence date) (Karels et al., 2000).
  • Bank voles (Haapakoski et al., 2012).
  • Northern red-backed voles (juveniles are also trapped earlier) (Schweiger & Boutin, 1995, p. 422).
  • Wood mice (Díaz & Alonso, 2003, p. 2687).
  • Tropical mice (earlier litters) (Duquette & Millar, 1995, p. 354).
  • Yukon rodents (one species by one to two weeks; the other didn’t change) (B. S. Gilbert & Krebs, 1981, p. 328).

However, in very high-density environments, such as those caused by supplemental feeding to the point of overabundance, yearling does delayed their breeding season (Ozoga & Verme, 1982, p. 290).

While the evidence is clear that supplemental feeding results in an advancement of the breeding season across taxa, it is unclear to me whether earlier laying is good or bad. Few studies have been conducted on the effects on mammals, so the rest of this section will discuss effects on birds.

Nestling mass and the propensity for renesting were both higher if there was supplemental feeding (Kelly & Van Horne, 1997, p. 2507). However, it may also be that females who are laying earlier for some other reason are more likely to be able to get high-quality, food-supplemented habitat (ibid: 2508). For instance, in a migratory species, the first-arriving females may be more likely to mate with the male with the highest-quality territory, which would be the supplementally fed males (ibid: 2508). Most current research is unsuitable for distinguishing between these hypotheses (ibid: 2509-2510).

Advancement of laying could have a negative effect on the fitness of and lower the survival of parents (Meijer & Drent, 1998, p. 411; Svensson & Nilsson, 1995, p. 1810). Females who bred early may have lower survival due to the difficulties of successfully breeding, but males may not (Nilsson, 1994, p. 207). This is probably because females have to go through two energetically intense periods (incubation and feeding young) while males only have to go through one (feeding young) (ibid: 207). On the positive side, early breeding might mean there’s more time for parents to moult and recover before winter (Nilsson, 1994, p. 201; von Brömssen & Jansson, 1980, p. 176).

Great and coal tits who fledge earlier survive longer, suggesting that earlier breeding is adaptive (Naef-Daenzer, Widmer, & Nuber, 2001). Earlier blue tit broods survive better and have a higher recruitment rate, perhaps because food supply declines later in the season, and perhaps because of competition between early and late young (Svensson & Nilsson, 1995, p. 1804). Early fledging willow and crested tits might have an easier time finding groups with which to try to survive the winter (von Brömssen & Jansson, 1980, p. 176).

Early breeding may give young an advantage in finding territories (Nilsson, 1994, p. 201). Suitable habitats may be filled up quickly, leaving late-fledging willow and crested tits with poor habitats (von Brömssen & Jansson, 1980, p. 176). They may be less likely to survive and more likely to be predated upon (ibid: 176). In song sparrows, early breeders are more likely to be dominant, winning conflicts at feeders (P. Arcese & Smith, 1985). The competition for good territories and winning conflicts at feeders are zero-sum games; while it may appear to benefit these birds to feed them, in reality there is no benefit.

Too-early breeding can result in lower nestling mass and survival (Svensson & Nilsson, 1995, p. 1810). Broods of females manipulated to start breeding early suffered more total losses than did the broods of control females, reducing nestling survival and fledging rates (Nilsson, 1994, p. 205). Some earlier-breeding birds encountered bad weather and the chicks starved (Nakamura, 1995, p. 8). Starting feeding too early could result in low food supply later in the season (Svensson & Nilsson, 1995, p. 1810).

An earlier laying date tends to lead to more eggs being laid (Meijer & Drent, 1998, p. 411). Early breeding may also allow the bird to lay a second clutch (Nilsson, 1994, p. 201).

Number of Reproductive Bouts

Supplemental food increases the number of breeding attempts a bird makes in a single season (D. N. Jones & James Reynolds, 2008, p. 7) and the likelihood that a bird will produce a second nest (Nagy & Holmes, 2005).

Fed song sparrow pairs had more nesting attempts than control pairs, probably because they began breeding earlier and renested more quickly (Peter Arcese & Smith, 1988, p. 126). Fed willow and crested tits are slightly more likely to lay a second clutch (von Brömssen & Jansson, 1980, pp. 175–176). While kakapo did not renest, no kakapo females had nested the year before feeding began, but two females nested once feeding began (Powlesland & Lloyd, 1994, p. 104). The kakapo females nested two years in a row, the first time this behavior was ever seen (ibid: 104).

However, not all bird species renest more often if fed. Feeding pheasants did not change the number of nests initiated per female or the number of replacement clutches laid after nest or brood loss, (Hoodless et al., 1999). In fed magpies there is no difference in number or success of renesting attempts (Dhindsa & Boag, 1990, pp. 598–599). Experimental blue tit females had no more laying gaps than controls (Nilsson, 1994, p. 202). Food supplementation reduced the interval between hihi clutch attempts but did not increase the overall number of clutches produced (Castro et al., 2003, p. 278). Nevertheless, if second clutches are hatched earlier they may be more likely to survive longer (ibid: 278).

Supplemental feeding may also have an effect on the number of reproductive bouts per season in mammals. For one Yukon rodent species, significantly more fed females had two litters (B. S. Gilbert & Krebs, 1981, p. 328). While some fed red squirrels had two litters, no unfed red squirrels did. (Sullivan, 1990, p. 584). Fed does had more pregnancies in a single breeding season (Ozoga & Verme, 1982, p. 291), 1.7 fawns per doe instead of 1.3 (ibid: 297). However, feeding did not change the number of litters or inter-birth intervals for tropical mice (Duquette & Millar, 1995, p. 353). Fed rattlesnakes reproduce more often (Taylor et al., 2005); this is the only study I could find on the effects on rattlesnakes.

Number of Animals Reproducing

Supplemental feeding may cause more individual animals to reproduce, which may increase overall fecundity. Studies suggest that food supplementation among small temperate vertebrates consistently increases the percentage of animals breeding (Boutin, 1990, p. 208).

For many mammal species, supplemental feeding causes more animals to reproduce. A higher percentage of supplementally fed kit foxes bred than control kit foxes (Warrick et al., 1999). In the fed group, five of six adult females and four of eight yearling females whelped, while in the unfed group three of five adult females and one of four yearling females whelped (ibid). Provisioning arctic foxes causes more foxes to give birth; of 65 food dens, 17 had a litter, while of 103 control dens, only 3 had a litter (Angerbjörn et al., 1991). Feeding snowshoe hares increases pregnancy rates by 5% relative to controls (O’Donoghue & Krebs, 1992, p. 634). Fed arctic ground squirrels have a higher percentage lactating and percentage weaning litters (Karels et al., 2000). One small mammal species in Chile had higher reproductive rates (Meserve et al., 2001, p. 553). The other five species did not change population parameters (ibid: 553).

In a study of overwinter supplemental feeding of rodents in the Argentinean Pampas, in September a greater percentage of rodent females were reproductively active in supplementally fed sites (Cittadino et al., 1994, p. 449). However, only one species had a higher percentage of reproductive individuals, probably because it was larger and competitively dominant (ibid: 451). More female tropical mice were reproductively active on fed plots, but there was no change in how many males were reproductively active (Duquette & Millar, 1995, p. 352). Feeding did not change the percentage of females that were pregnant (ibid: 353).

Eight of nine pregnant or lactating vole females were from food-supplemented populations (Forbes et al., 2015). At the peak stage of their population cycle, extra food increases the ratio of bank vole females who are pregnant, lactating, or breeding to those who are not (Löfgren et al., 1996, p. 388).

Some studies of mammals, however, show no effect. There was no significant difference in the proportion of red squirrels who bred (Sullivan, 1990, p. 582). Feeding northern flying squirrels had no effect on percentage of males breeding (Ransome & Sullivan, 2004). However, this study here may have had methodological problems, such as squirrels not being motivated to go into food-baited traps when food is supplemented (ibid). The rate of reproductively active adults did not increase over time for supplemented coastal sand dune rodents (Koekemoer, 2000).

In summer, control cotton rat populations have a higher proportion of reproductive females than fed populations, but in other seasons there is no difference (Doonan & Slade, 1995, pp. 818–819). Cotton rats are territorial, so non-reproductive females are better tolerated by dominant reproductive females and thus are more likely to be permitted (ibid: 823). Therefore, this effect is caused by immigration rates and not the effect of supplemental food on breeding.

Birds seem to be rarely studied, but the effects are more mixed. Feeding pheasants did not change the percentage of hens that nested (Hoodless et al., 1999). Supplemental feeding of Pyrenean bearded vultures lowers dispersal rates, causing many birds to either not have a territory (and thus not breed) or to have a low-quality territory (Carrete, Donázar, & Margalida, 2006). This lowers overall productivity (ibid).

Birth Rates

Supplemental feeding may have an effect on the number of animals born. Supplemental feeding increases fecundity for ungulates (Inslerman et al., 2006, p. 5) and bears (ibid: 29). At the vole population peak, the number of litters born on food grids averages 2.8 times larger (Schweiger & Boutin, 1995, p. 423). During the decline, the number of litters born on food grids averages 5.3 times larger (ibid: 423). Closing a dump decreased fertility for herring gulls (Oro et al., 2013, p. 10). Opportunistic seabirds who feed on discarded fish have higher birth rates (ibid: 8).

For one population, provisioning increases Barbary macaque birth rates (Fa, 2012a). In another population, it lowers birth rates, although this is probably due to stress related to human visitors and not supplemental feeding per se (Fa, 2012b).

Supplemental winter feeding does not appear to affect elk fecundity (Smith, 2001, pp. 176–177). Supplemental feeding does not significantly influence elk birth rates, probably because it ends before the metabolic demands of pregnancy are particularly large (Smith et al., 1997, p. 35).

Sex Ratios

Supplemental feeding may have an effect on sex ratios.

Supplemental winter feeding leads to the production of more male elk, because male fetuses are more energetically expensive (Smith, 2001, p. 177). Male turkeys outcompete female turkeys for supplemental food, which means there are more and more male turkeys and fewer and fewer female turkeys; sufficiently isolated populations may eventually go extinct (Inslerman et al., 2006, p. 14). Provisioning bears skews their sex ratios towards males in urban areas (ibid: 27). Provisioned kakapo have more male offspring than female offspring (Clout, Elliott, & Robertson, 2002/9). This is believed to be because kakapo are a polygynous species in which the males engage in competitive breeding displays to attract females (ibid). Large male birds are far more sexually successful than small males, while there is little advantage to having large females (ibid).

Supplemented prairie vole enclosures recruit males at the same rate as unsupplemented enclosures, but are more likely to recruit females (Cochran & Solomon, 2000). Food increased the percentage of snowshoe hares who are female during the late decline (D. L. Murray, 1999, pp. 53–54). Both effect sizes were fairly small.

Number of Offspring

Supplementally fed animals could conceivably allocate resources towards having more offspring by increasing clutch or litter size. In reality, clutch or litter size rarely increases because it is limited by developmental and genetic factors (Boutin, 1990, p. 208). However, in poor territories or years or in high-density communities, food supplementation can increase clutch or litter size to those typical in good environments (ibid: 208). Supplemental feeding may also lead to selection pressure for higher clutch or litter size, which is understudied because of how long such studies generally take.

Among different bird species, clutch size is positively correlated with the amount of food provided to chicks (Saether, 1994, p. 1399). This may be for one of two reasons (ibid: 1400). First, all bird species may feed their chicks at the maximum rate; food limits reproductive output for birds (ibid: 1400). Second, clutch sizes may be small to reduce the reproductive effort spent by birds on any particular batch of offspring: for instance, to save energy for future reproductive bouts or to reduce the risk of attracting predators to the nest (ibid: 1401). To the extent the second hypothesis is true, we may provision without fear of increasing populations unsustainably due to increased clutch size.

Many experts believe that feeding birds does not have strong effects on clutch size and may even lower clutch size (D. Jones, 2011, p. 6; Meijer & Drent, 1998, p. 411; Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 478). Arctic-breeding waterfowl are a possible exception (Meijer & Drent, 1998, p. 411). However, a recent meta-analysis found that food supplementation in birds increases clutch size (Ruffino et al., 2014). Food supplementation has no effect on clutch size for bird species that don’t cache food, perhaps explaining earlier negative results (ibid).

Provisioned American coots lay about one more egg than controls, representing three percent of observed variation in clutch size (Arnold, 1994). Provisioned buff-throated partridges produce more offspring than non-provisioned birds do (Yang et al., 2016). In herring gulls, the closure of a dump decreased clutch size (Oro et al., 2013). When fishing ships dump non-commercial fish, seabirds increase clutch size (ibid: 11). However, clutch size did not change for fed European starlings (Källander & Karlsson, 1993, p. 1032) or pheasants (Hoodless et al., 1999). Nutritional stress is uncorrelated with clutch size in kittiwakes (Kitaysky et al., 2010).

Supplementing blue tits and great tits appears to reduce brood size significantly, by approximately half a chick on average (Harrison et al., 2010). In both species, it is driven by significantly smaller clutches and, in blue tits, in a reduction in the number of eggs which hatch (ibid). This is similar to the typical laying habits of blue tits and great tits in urban areas, who are probably supplemented with bird feeders (ibid). Other studies found no change in clutch size in willow and crested tits (von Brömssen & Jansson, 1980, p. 175) and blue tits (Nilsson, 1994, pp. 202–203; Kate Elizabeth Plummer, 2011, p. 134).

Fed songbirds had significantly larger broods (Zanette et al., 2006a, p. 2476; Zanette, Clinchy, & Smith, 2006b). Song sparrows had 1.1 more offspring if there was supplemental food, which went up to 4 more offspring if combined with low predator pressure (Zanette, Smith, van Oort, & Clinchy, 2003, p. 800). Fed song sparrow pairs produce larger clutches than controls, on average about one half-egg bigger (Peter Arcese & Smith, 1988, p. 125). High-quality food may increase clutch size, while lower-quality food does not (ibid: 131). In addition, clutch sizes may be depressed by high densities, which lead to low food availability, and supplemental feeding allows the clutch size to increase to the size it is at low densities, but not above (ibid: 131). The number of young produced is also comparable to the number of young observed at small densities (ibid: 132).

In hihi, an endangered New Zealand bird species, clutch size increased from 3.9 to 4.4 eggs per attempt by the bird to nest (Castro et al., 2003, p. 271). The study was long-term, which means it is more likely to find an effect, because it is more likely to include years in which the natural food availability is sufficiently low that it depresses clutch size (ibid: 276-277).

In magpies supplemental feeding led to no change in clutch size (De Neve et al., 2004; Dhindsa & Boag, 1990, p. 598). However, one study found that supplementally fed magpies lay about .5 more eggs than unfed magpies (Hogstedt, 1981, p. 223). One year the experimental group laid .37 more eggs and the other year they laid .62 more eggs (ibid: 223).

Food-supplemented alpine accentors did not have a larger clutch size or more clutches (Nakamura, 1995, p. 4). The clutch size may have been unchanged because the food was low-quality (ibid: 7-8). The food was not fed to nestlings unless the parents had trouble provisioning natural food (ibid: 7).

A few studies have been done on the effect of supplemental feeding on mammals. Provisioned mule deer produce more fawns (Peterson & Messmer, 2007). Food addition has no effect on litter size in snowshoe hares (O’Donoghue & Krebs, 1992, p. 635) or cotton rats (Doonan & Slade, 1995, p. 819). Fed arctic ground squirrels have a higher litter size (Karels et al., 2000). I am aware of one study on reptiles, which found that fed rattlesnakes have the same number of offspring per reproduction (Taylor et al., 2005).

Hatching and Pregnancy Success

Studies mostly show no effect of supplemental feeding on hatching success (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 478). There appears to be no effect of supplemental feeding on hatching success in magpies (Hogstedt, 1981, p. 223), alpine accentors (Nakamura, 1995, p. 5), or blue tits (Nilsson, 1994, p. 204). Feeding pheasants did not change the percentage of nests that resulted in at least one hatched chick, number of chicks hatched per hen, or number of chicks hatched in general (Hoodless et al., 1999).

There is a very small positive effect of feeding on hatching success for song sparrows (Peter Arcese & Smith, 1988, p. 125). Seabirds who eat bycatch have higher rates of hatching success (Oro et al., 2013, p. 11). Nutritional stress leads to lower hatching success in kittiwakes (Kitaysky et al., 2010) and supplemental feeding of kittiwakes increases hatching success (V. A. Gill et al., 2002, pp. 8–9). Perhaps supplemental feeding only has a strong effect on hatching success for seabirds.

In Mauritius parakeets, supplemental feeding significantly reduces hatch success, perhaps because it increases susceptibility to a disease which reduces the rate of hatching success (Tollington et al., 2015). Fed birds were not more likely to be infected but they may have been affected more strongly (ibid).

The influence of vitamin E supplementation on hatching success in blue tits is inconsistent across years but positive (Kate Elizabeth Plummer, 2011, p. 113).

Few studies have been done on mammals. Stillbirth rates for snowshoe hares are higher on food grids, possibly as an effect of higher densities (O’Donoghue & Krebs, 1992, p. 636).

Recruitment

Recruitment is the number of juveniles that survive to be added to the population. It may reflect decreased immigration, increased number of juveniles being born, or increased juvenile survival.

Recruitment of the following species increased with food supplementation:

  • Hihi (Castro et al., 2003, p. 278).
  • Squirrels (Sullivan, 1990, p. 581).
  • Tropical mice (Duquette & Millar, 1995, p. 352).

Recruitment of bighorn sheep did not increase with food supplementation, with or without parasite treatment (M. W. Miller et al., 2000). Feeding northern flying squirrels also had no effect on recruitment (Ransome & Sullivan, 2004). However, there may have been methodological problems, such as squirrels not being motivated to go into food-baited traps when food is supplemented (ibid).

In one Yukon rodent species, supplemental feeding increased the number of juveniles by 35-66% (B. S. Gilbert & Krebs, 1981, p. 328). Twice as many juveniles were caught when the animals were fed with oats, and two to four times as many when they were fed with sunflower seeds (ibid: 328). Sample sizes were small, making generalization difficult (ibid: 328). Production is probably higher because juvenile survival increased (ibid: 328).

In the first year of supplemental vole feeding, the number of vole juveniles captured in food grids was 2.8 times larger than in control grids (Schweiger & Boutin, 1995, p. 423). In the second year, it was 9.6 times larger, which itself is probably an underestimate (ibid: 423). A study of bank voles found that extra food did not affect the ratio of immature to adult females, but there were more immature males than adult males (Löfgren et al., 1996, pp. 388–389). No significant differences were found between fed and unfed grids in the ratio of year-born to overwinter breeders (ibid: 389).The rate of immature bank voles moving from one grid to another was small (ibid: 388), suggesting the effect is genuine.

Supplemental feeding appears to increase recruitment rates, but it is unclear why.

Miscellaneous

Fed male wood mice had enlarged testes, a sign of increased reproductive effort (Díaz & Alonso, 2003, p. 2687).

Studies mostly show no effect of supplemental feeding on incubation time (Robb, McDonald, Chamberlain, & Bearhop, 2008, p. 478). Control blue tit females started incubation an average of three days after they laid their last egg, while experimental females waited an average of five days (Nilsson, 1994, p. 203). Conversely, blue tits provisioned throughout the egg-laying process waited an average of less than a day to begin incubation (ibid: 203).

Feeding decreases age at first reproduction (Boutin, 1990, p. 208). Fed ungulates have decreased time to sexual maturity (Inslerman et al., 2006). However, age at sexual maturation for tropical mice did not change with food (Duquette & Millar, 1995, p. 355).

A competitively dominant rodent species in the Argentinean Pampas had a lengthened breeding season (Cittadino et al., 1994, p. 451). Fed squirrels had a significantly longer breeding season (Sullivan, 1990, p. 582). Provisioning rats that typically do not mate over winter causes them to mate over winter, presumably increasing population (Banks & Dickman, 2000). However, there was no effect on the end date of the breeding season for bank voles (Löfgren et al., 1996, p. 388) or male snowshoe hares (O’Donoghue & Krebs, 1992, p. 634).

The population growth rates of yellow-legged gull and rook colonies are positively associated with the increase in total annual tonnage of the nearest dumps (Oro et al., 2013, p. 12). The availability of middens and restaurants influences variation in the population of griffon vultures (ibid: 12).

Fed female tropical mice during the wet season got pregnant more quickly (Duquette & Millar, 1995, p. 355). This difference did not exist during the dry season (ibid: 355).

Barbary macaques may be distracted from breeding by highly palatable food provided by tourists (Fa, 2012a, pp. 150–151).

Environmental Effects

There is a high degree of uncertainty about the effects of supplemental feeding on the environment. Few studies have been done on the effects of supplemental feeding on communities (Boutin, 1990, p. 216). Feeding may increase biodiversity through the addition of new resources or increased resource availability or may decrease it due to increasing populations of superior competitors (ibid: 216). The uncertainty is increased because of the likely complexity of these effects: for example, feeding ungulates has extremely complicated effects on biodiversity and other species (Milner et al., 2014, p. 219). For this reason, experts argue, “the potential consequences [of feeding] for the stability and functioning of these ecosystems remains unknown” (Oro et al., 2013, p. 22).

Effects on Vegetation

Ungulates

Provisioning deer can cause harm to the habitat around the location of the deer. Deer want to stay near the location of the feeder, which can lead to serious damage around the feeder location (Brown & Cooper, 2006; Putman & Staines, 2004, p. 294). Increased density also causes more harm to habitats (Milner et al., 2014). Long-term supplemental feeding of deer reduces their ranges, causing them to feed more near the feeders; seedlings near feeders are more likely to be browsed than other seedlings (S. M. Cooper, Owens, Cooper, & Ginnett, 2006).

Some researchers believe that supplementally fed deer will disproportionately eat highly nutritious plants, which may reduce biodiversity (Brown & Cooper, 2006; Murden & Risenhoover, 1993). However, a recent study suggested the species richness of deer diets is not influenced by access to supplemental feed (Timmons, Hewitt, DeYoung, Fulbright, & Draeger, 2010). Supplemented deer diets have a far higher percentage of forbs in autumn and browse in spring and lower percentage of mast in both autumn and spring (ibid: 998). In winter and summer there was no such diet change (ibid: 998). Pelleted food may be low in fiber, causing deer to consume high-fiber food (ibid: 999). Supplemental food may also enable deer to detoxify plants they otherwise wouldn’t eat, especially if the plants had secondary plant chemicals with beneficial effects (ibid: 999). Supplement provision may reduce deer effects on vegetation (ibid: 1000). Another study showed that the use of food plots to maintain high densities may result in higher deer consumption of natural forbs, which leads to loss of species and simplification of native plant communities (Hehman & Fulbright, 1997).

Supplemental feeding of deer can increase or reduce damage to forests (Putman & Staines, 2004, p. 294). The degree of ungulate utilization of preferred forage species is highly dependent on the duration and severity of the nutritional stress, population density, and the quality and quantity of supplement provided (Inslerman et al., 2006). In particular, infrequent emergency feeding is unlikely to have any negative effects on foliage, because snow protects all but the tallest plants (ibid: 12). Damage is particularly bad when deer are fed a diet lacking in fiber and thus strip bark from trees to obtain fiber (Putman & Staines, 2004, p. 294). Inconsistent feeding or withdrawal of food result in local forestry damage from deer aggregating around the feedless feeding site (ibid: 297). In one study, supplementally fed deer had only minor effects on vegetation until they reached peak density (Ozoga & Verme, 1982). Trampling probably did as much damage as grazing (ibid: 295). Palatable plants decreased in abundance while unpalatable plants increased (ibid: 295).

While most studies are short-term and don’t focus on the overall effects on the landscape (as opposed to on the area around the feeding site), they do not appear to show any reduction in species richness (Priesmeyer et al., 2012). A randomized controlled trial appears to show little effect of Iberian red deer on shrubs (Miranda et al., 2015). Deer favor plants that have nutrients they aren’t getting in their food concentrate, suggesting that providing a reasonable balance of all nutrients reduces the harm to plants (ibid).

Habitat heavily browsed by white-tailed deer has less understory but larger trees, with greater basal area and more dead standing timber (Casey & Hein, 1983, pp. 831–832). It has a distinctly different set of birds (ibid: 832). Species richness, density of breeding pairs, and overall abundance of birds are not significantly different (ibid: 835). Ranked abundance is no different inside or outside the habitat (ibid: 834-835). Bird species diversity is higher in heavily browsed habitat (ibid: 835). Heavily browsed habitat reduces the prevalence of birds associated with undergrowth, the transgressive layer of saplings, or overgrown small openings (ibid: 835). It increases the prevalence of bark-foraging and cavity-nesting species, as well as those which prefer open canopy (ibid: 835).

Increased density of deer may reduce the number of flowering plants, increase the number of ferns and grasses, and reduce the number of intermediate-canopy-nesting birds. Deer were maintained at various densities in an environment which simulated a timber forest (deCalesta, 1994, pp. 712–713). Deer did not affect percent ground cover (ibid: 713). Increased deer densities were associated with decreases in flowering plants and increases in fern and grasses (ibid: 713). Deer reduced mean sapling height (ibid: 713). Species richness of ground-nesting and upper-canopy nesting birds was unrelated to sapling height (ibid: 714). Species richness of intermediate-canopy-nesting birds was weakly correlated with sapling height on clear-cut sites, moderately correlated on thinned sites, and uncorrelated on uncut sites (ibid: 714). Abundance of intermediate-canopy-nesting birds was correlated with sapling height on thinned and clearcut sites, but not on uncut sites (ibid: 714). Mean richness of intermediate canopy nesting species declined 27% from the lowest deer density to the highest (ibid: 714). The threshold for deer effect occurred at between 7.9 and 14.9 deer per kilometer squared (ibid: 714). Mean richness of ground-nesting and upper-canopy-nesting birds was unaffected by deer density (ibid: 714-715). Abundance of intermediate canopy nesting species declined 37% from the lowest to highest deer density (ibid: 715). Ground-nesting and upper-canopy-nesting species did not change (ibid: 715). The effect is linear, without a threshold density (ibid: 715).

Supplemental feeding of deer in semi-arid rangeland has little to no effects on rodent populations, probably because rodents in semi-arid environments are adapted to large changes in vegetable productivity (Moseley, Cooper, Hewitt, Fulbright, & Deyoung, 2011).

Warm-season planting sites for deer had significantly lower vegetative species richness than control sites, but cool-season planting sites had no difference (Porter, 2008). Cool-season sites had a higher rate of preferred browse for white-tailed deer and of browse not known to be eaten by white-tailed deer, while control sites had a higher rate of bare ground and of browse used by white-tailed deer but not preferred (ibid: 17-18). Warm-season sites had no significant difference in rate of preferred browse species or unused browse species, but they had less bare ground and more browse used by white-tailed deer but not preferred (ibid: 18). Cool-season sites were primarily composed of forbs, while control sites had a more diverse array of vegetation, even though they had more bare ground (ibid: 18). Warm-season sites were primarily composed of grasses and forbs, and again control sites had a more diverse array of vegetation in spite of having more bare ground (ibid: 18-19).

Neither order nor family species richness for invertebrates was different from controls for either warm-season or cool-season sites (Porter, 2008, p. 19). Cool-season sites had a significantly lower diversity at the order level according to the Shannon Diversity Index, which measures the probability of collecting two individuals of the same type (ibid: 19). However, there was no difference on the family level (ibid: 19). There was no difference between warm-season and control sites on the Shannon Diversity Index on either the order or the family level (ibid: 19-20). The Shannon Evenness index determines the distribution of the number of individuals collected in each order or family (ibid: 20). Evenness was significantly higher on control sites than on cool-season sites on the order and the family level (ibid: 20). Warm-season sites were less even on the order level than controls, and there was no difference on the family level (ibid: 20). The cool-season and warm-season sites were not significantly different from controls in terms of invertebrate biomass (ibid: 20).

No significant difference in browse pressure was detected between warm-season or cool-season and control sites (Porter, 2008, p. 21). However, more vegetation was collected outside of the cool-season site than inside it, indicating that the cool-season sites had lower browse pressure (ibid: 21-22). These results suggest a minimal impact of supplemental feeding on biodiversity (ibid: 27). No herbicide was applied to warm-season or cool-season plots due to drought, which is not standard agricultural practice and may have increased biodiversity and prevalence of species not preferred by deer (ibid: 23). Bare ground was lower in warm-season and cool-season sites because they are agricultural plantings (ibid: 24). Invertebrate diversity may have been higher due to the presence of bare ground (ibid: 25). However, without further study, it is impossible to know what specific factors are reducing invertebrate diversity (ibid: 25-26).

While deer have been most studied, other ungulates also have effects on vegetation. Feeding elk can lead to overgrazing of palatable plants near the range, particularly if the elk are maintained at a density above the carrying capacity (Smith, 2001, pp. 179–181). Elk overpopulation leads to declines in aspen recruitment and growth (ibid: 181). Reductions in plant diversity may have negative effects on bird biodiversity (ibid: 181). Elk maintained on artificial feed reduced the amount of willow in the area, which reduced the carrying capacity of moose (Dunkley & Cattet, 2003, p. 19). In areas with fed elk, deer, and mouflon sheep, the understory was decreased, little ground cover remained, trees were larger, there were more dead trees, ground-nesting birds were less abundant, and bark-foraging and cavity-nesting species were more abundant (ibid: 19).

Non-Ungulates

Supplemental feeding may introduce invasive weeds into a habitat (Dunkley & Cattet, 2003, p. 18; Milner et al., 2014). The effects of invasive species include reduction of biodiversity, loss of and encroachment upon endangered and threatened species, loss of habitat, loss of food sources, changes to natural ecological processes such as succession, alterations to fire frequency and intensity, alterations in soil characteristics which can cause soil erosion, and disruption of plant-animal associations such as pollination, seed dispersal, and host-plant relationships (Dunkley & Cattet, 2003, p. 18).

Higher macaque densities due to feeding cause significant amounts of ecological damage, since the macaques consume more natural vegetation than they would at a lower density (Kurita, 2014, p. 47).

Effects on Water Quality

Feeding waterbirds may lead to water pollution (Newsome & Rodger, 2013, p. 437). Fish food contains high levels of phosphorous and may play a significant role in eutrophication of some particularly popular lakes (A. M. Turner & Ruhl, 2007). Excessive amounts of phosphorous lead to algae blooms, hypoxia, and fish kills (ibid).

Higher Densities

Supplemental feeding often leads to higher densities of animals (for more, see the “Population Density” section). Increased population densities due to feeding cause cascading and hard-to-predict effects across entire ecosystems, altering the structure and species composition of their communities (Oro et al., 2013).

For example, seabirds consume discarded food (Oro et al., 2013, pp. 20–21). Increased seabird density leads to many consequences, such as increased ammonia emissions excreted by seabirds and increased movement of nutrients, detritus, and pollutants between marine and terrestrial environments, altering both ecosystems, including relatively pristine and untouched environments (ibid: 20-21). These consequences can change species composition, particularly affecting keystone species in marine zones, with consequences for community structure (ibid: 21). Higher seabird density increases nitrogen inputs on islands, causing cascading effects: altering vegetation structure and plant species turnover, which favors non-native plants, which affects beetle and vertebrate communities (ibid: 21). Opportunistic seabirds can act as seed dispensers for both native and invasive plants, which has unknown effects (ibid: 21).

Feeding birds may increase their density in a location, which causes environmental damage and negative effects on other species (e.g. species the birds eat or compete with) (Robb, McDonald, Chamberlain, & Bearhop, 2008, pp. 480–481). Feeding birds may lead to trophic cascades, but this is hard to tell, because trophic cascades are notoriously hard to study (ibid: 481). Feeding geese may result in habitat degradation due to increased concentrations of birds, including higher bacteria concentrations, poorer water quality due to high amounts of fecal matter, and excessive consumption of plants by birds (Inslerman et al., 2006, pp. 20–21).

Effects on Which Species Survive

Increased food supply should decrease competition, which increases species richness (Oro et al., 2013). When interference competition is light, because supplemental feeding occurs on low trophic levels, richness remains stable and population densities increase (ibid: 22). When dominant species monopolize supplemental food, species richness decreases (ibid: 22). For example, provisioning rodents decreases the species diversity of the rodent community due to an increase in numbers of the dominant species; this is probably due to immigration rather than survival or dispersal (Koekemoer, 2000, pp. 56–57). Increased animal density can lead to increased competition, which may lower biodiversity, plant abundance, and community function (Dunkley & Cattet, 2003, p. 18). Cascading effects may also reduce species richness (Oro et al., 2013, p. 22).

Supplemental feeding favors some species over others. Supplemental feeding may favor the species which are capable of accessing the feeders over species which are not (D. N. Jones & James Reynolds, 2008, p. 5). In general, food provisioning favors more aggressive species and scavengers over other species (Newsome & Rodger, 2008, p. 264). Food provisioning favors larger species over smaller ones (Newsome & Rodger, 2008, p. 264; Oro et al., 2013). In cities, high populations and absence of predators lead to a lack of food even with supplemental feeding, which tends to favor very efficient foragers (Shochat et al., 2004).

It seems probably positive to favor large species, which tend to be longer-lived. It seems probably negative to favor highly aggressive species, which may cause harm to other animals. Leaving aside the cost to biodiversity, favoring scavengers and efficient foragers seems neutral (or perhaps positive if scavengers are favored instead of predators). Whether favoring species that can access the feeders is positive, neutral, or negative seems to depend on which traits allow a species to better access a feeder.

Supplemental feeding may help protect endangered migratory bird species from extinction (Inslerman et al., 2006, p. 23). Increased goose presence reduces invertebrate diversity, richness, and abundance (ibid: 23). Feeding increases density of small mammals due to non-target feeding (ibid: 28).

Predation

Supplemental feeding may increase predation through attracting and increasing populations of carnivorous and omnivorous species (Oro et al., 2013, pp. 19–20). For example, predation increases around upland gamebird feeding sites (Inslerman et al., 2006, p. 15). The presence of a bird feeder causes increased predation on nearby mealworms, probably because it attracts insectivorous birds (Martinson & Flaspohler, 2003).

Feeding white-tailed deer increases predation on the nests of ground-nesting birds like wild turkeys (Susan M. Cooper & Ginnett, 2000; Dunkley & Cattet, 2003). Raccoons and striped skunks are the most common predators (Susan M. Cooper & Ginnett, 2000). The effect did not happen in dry years with sparse ground cover (ibid). One study found the proportion of nests depredated near ungulate feeding sites is 30% higher, probably because it is attracting predators to the area (Selva et al., 2014, p. 4). 82% of identified animals at ungulate feeding sites were potential ground-nest predators (ibid: 4). Ground-nest predation does not matter in and of itself, assuming the eggs have not hatched yet, but is an indicator of how supplemental feeding may affect other predation. Note that even though ungulates are herbivorous, supplemental feeding still increases the rate of predation, presumably because non-target omnivores eat much of the available food.

On simulated murrelet nests, corvids are responsible for a third of all predation attempts; however, most of this effect is jays (Marzluff & Neatherlin, 2006, p. 310). While crows and ravens are rare nest predators, they are more important close to settlements and campgrounds rather than far from them (ibid: 310). Crow and raven abundance increases near settlements and campgrounds due to anthropogenic food, but jay abundance does not change (ibid: 310). Increasing crow and raven populations increases the amount of predation on nests.

Conversely, supplemental feeding of predators may reduce predation pressure on their prey (Reese, 2007).

Supplemental feeding may also lead to the spread of disease to members of other species (Dunkley & Cattet, 2003).

Migration

In storks, supplemental feeding suppresses migration (Flack et al., 2016). Migratory animals alter ecological networks, influence pest control and pollination, and affect infectious disease dynamics (ibid). It is unknown what the environmental effects of migration suppression would be.

Fed elk migrate 19.2 km less, spend 11 more days on stopover sites, arrive to summer range 5 days later, reside on summer range 26 fewer days, and depart in the autumn 10 days earlier (J. D. Jones et al., 2014). Fed elk spending less time on summer range may increase the costs of feeding programs (ibid: 1777).

Conclusions

Overall, we expect the effect of feeding wildlife on their well-being to be negative. For a longer summary, please see the Intervention Report.

Supplemental Feeding: Reducing the Harm

Supplemental feeding may still be the right choice in a few, limited situations: for example, supplemental food may be used as bait to get animals to consume a contraceptive or vaccine, or it may be used to direct animals away from a road or other dangerous area. People may also choose to feed animals for the human-benefiting reasons discussed in the introduction. Encouraging people to use best practices for feeding wild animals may be a cost-effective intervention to promote wild animal welfare.

One expert provides the following advice for people considering a supplemental feeding program (M. H. Murray et al., 2016, pp. 7–8):

  1. All wildlife must be fed species-appropriate, high-quality feed with adequate vitamins, minerals, and protein content.
  2. Design and maintain feeders to have lower exposure to pathogens. Use raised containers that keep feed from being spilled on the ground, are made of non-porous material, protect feed from moisture, and limit access to a small number of individuals at one time. Regularly decontaminate soil and water around feeders.
  3. Provide feed on a random schedule. Avoid feeding during sensitive periods for disease and overwinter feeding for migratory animals.
  4. Broadly space feeding stations. Keep them well away from humans and domestic animals. Locate feeders in cool places adequately protected from the rain. Periodically change the location of feeders.
  5. Understand the biology of the target species to make sure your feeding methods are species-appropriate.

Aggression

Spreading food resources over a wide area may reduce aggression (Maréchal et al., 2016, pp. 12–13). While light feeding stations appear to allow younger vultures to feed more, they cause a slight increase in aggression (Duriez, Herman, & Sarrazin, 2012)

Contamination

There is no discernible pattern in aflatoxin production in feed with regards to climate or storage container (C. Thompson & Henke, 2000, p. 174). However, three-quarters of contaminated samples became contaminated in the third month of storage (ibid: 176). Aflatoxin may be more likely to grow if feeders are not cleaned, new feed is placed on top of old feed, and the feeder is open, which allows direct access of moisture to grain (Deanna G. Oberheu & Dabbert, 2001, p. 476).

Disease

No method of arranging food appears to completely eliminate disease transmission risk for deer, although ad libitum food spread over a large area appears to reduce the risk the most (A. K. Thompson et al., 2008).

The harm of bovine tuberculosis could be reduced by providing less desirable food (which attracts fewer deer) and by putting the feed sites near open or heavily forested areas which keep the deer from congregating near each other (R. Miller et al., 2003, p. 93). Sites that fed more deer or higher quantities of food or were near other feeding sites or hardwood forests have a higher rate of tuberculosis transmission (Palmer et al., 2012, p. 4).

Low-density feeding dramatically reduces the contact rates between elk and miscarried elk fetuses, thus probably reducing the transmission rate of brucellosis (Creech et al., 2012, p. 882). Longer feeding periods and those which coincide with peak brucellosis transmission rates are more likely to result in transmissions of brucellosis (Cross, Edwards, Scurlock, Maichak, & Rogerson, 2007, p. 961). Disease transmission rate is unrelated to population size or density (ibid: 961).

Cleaning bird feeders regularly decreases rates of disease transmission (Wilcoxen et al., 2015). Leaving feeders empty between feedings and feeding a small amount at a time may decrease rates of disease transmission, but this has been understudied (ibid). Tube-type feeders, which have limited numbers of perches and greater crowding potential, are linked to increased risk of conjunctivitis (Hartup et al., 1998, p. 287). Conjunctivitis in house finches spreads more from August to October (Altizer, Davis, Cook, & Cherry, 2004), suggesting that birds should not be supplementally fed in the fall.

To avoid transmitting disease while feeding birds (Margaret Clark Brittingham & Temple, 1988a, p. 201):

  1. Clean and disinfect the bird feeder with a weak bleach solution at least once a year, and more often if it is a platform feeder.
  2. Store seed in a dry place. Do not use moldy seed. If seed in the feeder becomes moldy, throw it out.
  3. Avoid feeding on the ground.
  4. Do not feed in the summer if mourning doves or rock doves use your feeder.
  5. If you see a dead or dying bird:
    1. Wearing gloves, pick up all carcasses and either bury them or wrap them in plastic bags and dispose of them.
    2. Clean and disinfect the feeder.
    3. Sweep up and dispose of seeds spilled on the ground.
    4. Move the feeder to a new location but continue to feed to avoid infected individuals introducing disease at someone else’s feeder.

The vast majority of people who feed birds do not use best practices to prevent disease transmission and are unaware that disease transmission is a risk (Galbraith et al., 2014). Educating people who feed birds about how best to prevent disease transmission may be a tractable way of reducing wild-animal suffering.

Inappropriate Food

Choose food intended for consumption by the species in question, such as fish pellets or bird feed. Do not feed birds nutritionally poor food like bread or popcorn. Always give ungulates food rich in fiber. Never feed an animal heavily processed, so-called “junk” food, such as candy, cakes, or potato chips.

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