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):

Bovine tuberculosis in cervids. Chronic wasting disease in deer. Bovine brucellosis in elk and bison. 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. Psoroptic mange in elk. Demodectic mange in white-tailed deer. Starvation of white-tailed deer when feeding delays migration to winter yards or when feeding is terminated abruptly Mycoplasmal conjunctivitis in house finches Salmonellosis in passerine birds due to eating food contaminated with feces 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 maint