Global Ecology and Conservation 12 (2017) 9e20

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Global Ecology and Conservation

journal homepage: http://www.elsevier.com/locate/gecco

Review Paper

How are garbage dumps impacting vertebrate demography,

heath, and conservation?
Pablo I. Plaza*, Sergio A. Lambertucci

n, Laboratorio Ecotono, INIBIOMA (Universidad Nacional del Comahue e
Grupo de investigaciones en Biología de la Conservacio
CONICET), Quintral 1250 (R8400FRF), San Carlos de Bariloche, Argentina

a r t i c l e i n f o a b s t r a c t

Article history: Organic waste can be considered a food subsidy which represents an important source of
Received 16 March 2017 energy for different species that exploit it. However, it could produce contrasting impacts,
Received in revised form 3 August 2017 both positive and negative. We reviewed which species of terrestrial vertebrates (birds,
Accepted 3 August 2017
mammals, reptiles and amphibians) exploit rubbish dumps, and the impacts that waste
produces on them. We analysed 159 articles including 98 species that are present in
rubbish dumps. Studies come from all over the world (including Antarctica), but mainly
Keywords:
from Europe, North America and Africa. Impacts reported on vertebrates were manly
Rubbish dumps
Organic waste
considered positive (72.6%) but around a quarter showed negative impacts. Rubbish dumps
Landfills provide food resources that may improve body condition, enhance reproductive perfor-
Introduced species mance and abundance, improve survival rate, alter movements, and they can be an
Endangered species important sustenance for some endangered species. However, these places increase the
Vertebrates risk of pathogen infections and poisoning, can be responsible for the spread of introduced-
invasive species and favour conflicts between humans and animals that use them. More-
over, species that take advantage of these sites can produce negative impacts on others
that do not use them. Worldwide increase in waste production makes this novel ecosystem
important on shaping ecological communities. Therefore, the spatial and temporal effects
of rubbish dumps on wildlife should be evaluated more deeply at a worldwide scale
considering current differences in waste production from developing to developed
countries.
© 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Humans have altered the ecosystem voluntary and involuntary through the activities performed at global scale (Foley
et al., 2005; McKinney and Lockwood, 1999). One of the most important current drivers of ecosystem alteration is the pre-
dictable anthropogenic food subsidies -food remains produced by humans and exploited by other species-, especially those
derived from rubbish dumps (Oro et al., 2013). Solid waste generation is mostly an urban phenomenon and, as urbanization
increases, this problem also increases (Hoornweg et al., 2013). Indeed, waste volumes are growing faster than urbanization
rates and its generation rates will be more than double in the next twenty years, especially in lower income countries
(Hoornweg and Bhada-Tata, 2012). Every day people discard 3 million tonnes of waste around the world, by 2025 the waste

* Corresponding author.
E-mail address: [email protected] (P.I. Plaza).

http://dx.doi.org/10.1016/j.gecco.2017.08.002
2351-9894/© 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).
10 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20

generated is expected to be 6 million tonnes per day and by 2100 it will exceed 11 million (Hoornweg and Bhada-Tata, 2012;
Hoornweg et al., 2013). Therefore, a peak of waste is expected in the early coming century (Hoornweg et al., 2013). In this
complex context of waste overproduction, it is expectable that this problem may enhance the ecosystem alteration and lead to
a novel ecosystem where changes in biodiversity may occur (Hobbs et al., 2009).
Food subsidies derived from rubbish dumps have both positive and negative attributes. On the one hand, they are
worldwide distributed, abundant, spatially and temporally predictable, daily renewed and represent a potential valuable food
source (Oro et al., 2013). Since they are composed of parts of meat, fish, chicken, fresh fruit, meals and eggs (Parfitt et al., 2010)
they can be exploited by different species along the food chain and can be used as part of their caloric requirements (Oro et al.,
2013). On the other hand, however, with these anthropogenic organic items there are also glasses, metals, wire, plastic, paints,
different toxics and dangerous pathogens, which can alter individuals' health and abundances (Flores-Tena et al., 2007;
Houston et al., 2007; Matejczyk et al., 2011). Therefore, taking advantage of these food subsidies could produce contrast-
ing impacts on vertebrate populations that need to be studied in detail.
Many studies around the world document the use of rubbish dumps by different species (Newsome et al., 2015; Oro et al.,
2013). However, there is not much information on the conservation status and population tendencies of species using them.
Moreover, there is little information about the health impacts associated to this foraging strategy, survival rates in these sites
and the impacts that species using rubbish dumps produce on other species that do not use them. Oro et al. (2013) made a
great advance onto this subject, but with a broader focus on different types of food subsidies including food intentionally
provided to wildlife. Therefore, a review specifically addressing this topic, focusing in detail on rubbish dumps as food
sources, direct and indirect impacts of rubbish dumps on wildlife, and consequences at ecosystem level is timely and
necessary. The aim of this study is to review which species of terrestrial vertebrates (birds, mammals, reptiles and am-
phibians) exploit rubbish dumps, and the impacts that waste produces at individual, population and ecosystem levels. We
also study the consequences of the presence of species favoured by these food sources on other species that do not use them,
and on the potential conflicts with humans. This information is relevant to make better policies about waste management,
and to perform better conservation policies, particularly for endangered or invasive species that exploit these sites.

2. Materials and methods

We performed an intensive bibliographic search of articles related to vertebrate presence or use of rubbish dumps-landfills
through Google Scholar and Scopus search engines, without restriction on year or geographic localization. We performed 5
different searches with different relevant terms combinations. The first was performed with the following terms ‘landfills’,
‘garbage’ or ‘rubbish dumps’ coupled with ‘animals’, and the other searches were performed with the following terms:
‘landfills’, ‘garbage’ or ‘rubbish dumps’ coupled with ‘birds’, ‘mammals’, ‘reptiles’ and ‘amphibians’. We then reviewed the first
1000 returns of each one in the case of Google Scholar and all the returns in the case of Scopus, to include only articles that
assess the presence or use of rubbish dumps by birds, mammals, reptiles and amphibians. Finally, we performed a search in
the literature cited in the articles we reviewed.
With the selected articles, we first determined the species of vertebrates present in these sites. Then we extracted in-
formation about direct impacts of these food subsidies on the studied species, particularly on body condition, reproductive
performance, population survival, population abundance, pattern of movement, pathogen infection risk, toxic exposure risk
and foreign body ingestion. We also reviewed the impacts of rubbish dumps on the presence of introduced-invasive species
and threatened species. After that, we reviewed information on indirect impacts of rubbish dumps as the conflicts produced
between animals using these sites and humans, and the impacts that species using these places can produce on others that do
not use them. Finally, we reviewed the consequences produced by these food subsidies at ecosystem level.

3. Results

We found 159 articles studying 98 vertebrate species that are present in rubbish dumps: 54 species of birds, 34 species of
mammals, 5 species of amphibians and 5 species of reptiles (Supplementary Material Table S1). Most studies (72.6%) showed
positive impacts of rubbish dumps on individuals and populations, a little more than a quarter (25.8%) showed negative
impacts and the rest do not assess impacts. We found studies performed all over the globe including Antarctica, but the 61.7%
came from Europe and North America, and a third from Africa, South America and Asia (Fig. 1). Most articles, (96%, 153/159),
showed that the species use rubbish dumps as food resource. Regarding birds that do this, we found a predominance of
studies on carnivores, both predators and scavengers, with Larus as the most represented genus with almost half (46%, 45/98)
of the studies. Regarding mammals, most studies were focused on predators (76%, 35/46), including domestic species as cats
(Felis catus) and dogs (Canis lupus familiaris), and the rest of the studies were focused mainly on rodents, primates and
livestock. Most studies found on reptiles were performed on species of the genus Varanus, and there was no study that
showed organic waste use as food source by amphibians (Supplementary Material, Table S2).
Some studies addressing dumps as food resources (6.3%, 10/159), showed a positive relationship between body mass -
body condition and organic waste use as food resource. There were 13.2%, (21/159) of the studies that addressed the influence
that organic waste produce in the reproductive performance of different species, and 81% (17/21) of them agreed that
exploiting these food subsidies produces an improvement in reproductive parameters such as clutch size, egg volume, and
egg size-hatching mass. However, 19% (4/21) of the studies showed negatives impacts of organic waste use on reproductive
 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20 11

Fig. 1. Waste production map per capita in Kg per capita/day (data obtained from https://www.weforum.org/agenda/2015/08/which-countries-produce-the-
most-waste/- World Economic forum) showing a scheme of animals that use dumps around the world and the percentage of researches found in this review.
There is no information available in the countries painted in white.

performance. Studies that addressed the relationship between feeding on rubbish dumps and population survival, (8.2%, 13/
159), described different impacts, with 54% of the studies showing an increase of survival rates, 31% showing the opposite
effect and 15% showing no differences in survival rates. We found 8.2% (13/159) of the studies addressing the impact of
organic waste use and population abundance and all studies showed a positive relationship between them. There were 15%
(24/159) of studies that addressed the relationship between rubbish dumps and animal patterns of movements showing that
these sites modify the movement patterns of individuals from different species. Surprisingly, we found few studies (10%, 16/
159), which addressed pathogens infection risk, being the half of them on genus Larus (50%). Also, we found 14% (22/159) of
studies regarding toxics exposure risk and foreign bodies ingestion in or near these sites, and (18.2%) of them were conducted
on amphibians.
Regarding introduced-invasive species, we found different species that use rubbish dumps to acquire part of their dietary
requirements. Four of them are described as 100 of the world's worst alien invasive species in the Global Invasive Species
Database: brown rat (Rattus norvegicus), house mice (Mus musculus), domestic cat and wild boar (Sus scrofa) (Supplemen-
tary Material, Table S1). We also found 8 threatened or nearly threatened species (IUCN, 2017) that use these sites: the Andean
condor (Vultur gryphus), the California condor (Gymnogyps californianus), the crowed crane (Balearica regulorum), the
Egyptian vulture (Neophron percnopterus), the hooded vulture (Necrosyrtes monachus), the Malayan sun bear (Helarctos
malayanus), the Olrog's gull (Larus atlanticus) and the polar bear (Ursus maritimus) (Supplementary Material, Table S1). We
found 5% (8/159) of articles studying conflicts between humans and animals that use rubbish dumps. Finally, only the 1.9% (3/
159) of the articles studied the impacts produced to species that do not use rubbish dumps by some species that take
advantage of them (Supplementary Material, Table S2).

4. Rubbish dumps as food sources

In rubbish dumps individuals find a source of food (fish, meat, chicken, offal, eggs, seeds, cheese and fruits), which is
predictable, renewed daily, abundant, and it can be used by some species according to natural food availability. For instance,
rooks (Corvus frugilegus) highest congregations in rubbish dumps are seen during periods of lowest natural food availability
12 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20

(Olea and Baglione, 2008). Similarly, wolves (Canis lupus) eat organic waste when ungulates are not or rarely available
(Meriggi and Lovari, 1996), and the peak use of rubbish dumps by grizzly bears (Ursus arctos) and Malayan sun bears coincided
with a low availability of high quality natural food (Peirce and Van Daele, 2006; Te Wong et al., 2004). The opposite occurs
with spotted hyenas (Crocuta crocuta) in Ethiopia, whose main food source is waste, shifting to donkeys predation when waste
availability decreases (Yirga et al., 2012). Thus, the use of organic waste could be a strategic escape used when natural food is
not available or to alternate with other food sources.
There are individual differences in organic waste use as food resource according to traits as age, sex, or hierarchical ranking
(Oro et al., 2013). In bald eagles (Haliaeetus leucocephalus), rubbish dumps may serve as important scavenging sites for hatch-
year and second-year eagles, whereas older birds may be more successful obtaining higher quality items in other places
(Turrin et al., 2015). In glaucous gulls (Larus hyperboreus) (Weiser and Powell, 2011) and white storks (Ciconia ciconia) (Blanco,
1996), there is a predominance of juveniles in rubbish dumps. Polar bears that feed in these sites are mainly sub adults and
family groups (Lunn and Stirling, 1985). In grizzly bears, rubbish dumps are first used by males followed by females with cubs
(Peirce and Van Daele, 2006) and males of herring gulls (Larus argentatus) tended to be dominant over females in a rubbish
dump after the opening of an incinerator, which changed the availability of food (Pons, 1994). Regarding hierarchical ranking,
low-ranking females of spotted hyenas are the most common groups feeding at these sites (Kolowski and Holekamp, 2008).
On the contrary, in grizzly bears social dominant individuals gained access to organic waste while subordinate bears did not
(Peirce and Van Daele, 2006). It is clear that depending on the species, the sex-age class and hierarchical ranking, rubbish
dumps use could vary producing non-natural imbalances among categories. However, the abundance of each age-sex class in
the population will influence the abundance in rubbish dumps; so, this source of bias should be considered to correct esti-
mations of the age-sex structure of a population using dumps.
There are several foraging strategies and competitive behaviours among species and individuals associated to rubbish
dumps use. Some sub adult individuals can be considered refuse specialists because they are frequently seen feeding in
different dumps (Turrin et al., 2015) and the capability of foraging in these sites may take some time (Galva
n, 2003; Greig
et al., 1983). Fighting and stealing food is commonly seen (Annorbah and Holbech, 2012). For instance, black kites (Milvus
migrans) and herring gulls kleptoparasite conspecifics and other species to acquire food in rubbish dumps (De Giacomo and
Guerrieri, 2008; Galva
n, 2003). Banded mongoose (Mungos mungo) groups sharing dumps had higher encounter rates than
other groups, which can result in increasing fights and competition (Gilchrist and Otali, 2002). Therefore, several species take
advantage or develop alternative foraging strategies to withstand the high competition levels with other individuals.
Finally, rubbish dumps not only provide organic waste that can be used as food resource but also a great number of prey
items for different species. Cattle egrets (Bubulcus ibis), for example, feed on flies and fly larvae of the families Muscidae and
Calliphoridae, in addition to fish fragments and meat (Annorbah and Holbech, 2012). Bald eagles may also prey upon smaller
birds that frequent these places and items like meat and bones (Elliott et al., 2006; Turrin et al., 2015). Foxes (Vulpes vulpes)
and cats visit rubbish dumps and eat micro mammals like rats (Hutchings, 2003; Martina and Gallarati, 1997). Therefore,
several species congregate near rubbish dumps to exploit other food sources like insects, small mammals, and little birds.
In summary, organic waste is the major involuntary food subsidies produced by human activities and most information
regarding wildlife use of rubbish dumps is related to their role as food sources. Although some studies raise questions about
the nutritional quality of this food (Steigerwald et al., 2015), in these sites species may find a nutritionally varied diet
(Parfittet al., 2010) that can be used as a permanent resource.

5. Direct impacts of rubbish dumps on wildlife

5.1. Body condition

Our results show that there is a positive relationship between body mass-body condition and organic waste use as food
resource that is evident in different vertebrate species. For instance, males of silver gulls (Larus novaehollandiae) using rubbish
dumps are heavier than males not using them (Auman et al., 2008), and the body mass and body condition of yellow-legged
gulls (Larus michahellis) decreased after the closure of a rubbish dump (Steigerwald et al., 2015). Grizzly bears and island foxes
(Urocyon littoralis clementae) that eat organic waste are heavier than those in natural areas (Gould and Andelt, 2013;
Blanchard, 1987). Also, the body condition improves in wild boars (Cahill et al., 2012), olive baboons (Papio anubis) (Eley
et al., 1989), banded mongoose (Otali and Gilchrist, 2004), polar bears (Lunn and Stirling, 1985) and lace monitor (Varanus
varius) (Jessop et al., 2012) that feed in rubbish dumps. Indeed, olive baboons improved their growth rates due to the use of
this food source (Eley et al., 1989). Thus, if the size or the body condition of an individual can improve its fitness (e.g. by
improving its competitive abilities) rubbish dumps may play a role as an anthropogenic selector of some genes (Lande, 1998),
which can produce unknown consequences at ecosystem and population levels.

5.2. Reproductive performance

Most studies agree that exploiting these food subsidies produces an improvement in reproductive parameters. For
instance, a colony of yellow-legged gulls located near a rubbish dump has a higher population growth probably due to the
increase in reproductive success (Bosch et al., 1994). Yellow-legged and herring gulls had a drop in their breeding perfor-
€ 1998; Pons,
mance (clutch size and egg volume) after a dump closure or reduction in organic waste availability (Kilpi and Ost,
 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20 13

1992; Steigerwald et al., 2015). In white storks, breeding success, egg size-hatching mass (Tortosa et al., 2002) and clutch size
(Djerdali et al., 2008; Tortosa et al., 2003) are significantly higher in pairs near rubbish dumps. Moreover, some bird species
use waste to provision their chicks (Ramos et al., 2009). Approximately 83% of the nestling diet of the laughing gulls (Larus
atricilla) is food that comes mainly from rubbish dumps, which enhances the growth and survival of chicks (Dosch, 1997).
Similar results are reported for yellow-legged gulls in Spain (Ramos et al., 2009). Black bears (Ursus americanus) using rubbish
dumps have a good reproductive success (Herrero, 1983), and their litter size is above the average (Rogers et al., 1976). Similar
results are described in grizzly bears (Blanchard, 1987), for which, in addition, mean cub size declined 17% concurrently with a
dump closure (Stringham, 1986). All these studies show that rubbish dumps use and reproductive performance are positively
related in different species. However, in the case of birds the final outcome of chicks fitness has seldom been studied.
While there are fewer studies showing negative than positive impacts in reproductive performance the former appear to
have significant consequences, especially for birds and amphibians. For instance, in California condors the main cause of
nestling death is waste ingestion (Rideout et al., 2012). Western gulls (Larus occidentalis) that took mainly fish and other
pelagic preys show superior breeding performance that those feeding on rubbish, probably because the latter is nutritionally
inadequate for chick development (Pierotti and Annett, 2001). Hatching and fledging success rates of herring gulls are lower
in colonies near rubbish dumps than in natural colonies (Belant et al., 1998), and western gulls shift from a diet composed of
organic waste to a fish diet when the egg hatches probably because the chicks hatching reject the waste items (Annett and
Pierotti, 1989). In rubbish dumps, mercury probably coming from discarded batteries, thermometers and general waste
(Lindberg et al., 2001) can produce degeneration of ovarian follicles in river frog (Rana heckscheri) (Punzo, 1993). Tadpoles of
bullfrogs (Rana catesbeiana) exposed to ash of coal, which is discarded mainly in dumps, suffer deformities related to the
pollutants that ash contain (As, Ba, Cd, Cr, Se) (Rowe et al., 1998). These negative impacts have the potential to produce great
impacts on individuals and on the population demography.
It is important to highlight that disposal sites are a variable concept including sanitary landfills and open dumps
(Hoornweg and Bhada-Tata, 2012). Many articles on dumps do not include good descriptions of those places, so it is difficult to
carry out a more detailed evaluation of them. However, depending on the disposal sites, they may provide food of high quality,
or of poor quality (Gre
millet et al., 2008) with different consequences to species. Future detailed descriptions of different
rubbish dumps and species that use them will help to evaluate their positive and negative impacts on wildlife.

5.3. Population survival

Food availability could be positively related to survival rates of individuals (Rotics et al., 2017; Payo-Payo et al., 2015; Bino
et al., 2010), although they have been seldom quantified when studying the effects of food subsides (Oro et al., 2013). We
found that studies addressing this relationship show opposite impacts. For instance, a reduction in organic waste availability
decreased the survival rate of red foxes (Bino et al., 2010). There was a reduction of population size after the closure of
Yellowstone rubbish dump in grizzly bears (Craighead, 1998; Knight and Eberhardt, 1985), probably given to the decreased
nutritional state of individuals due to the elimination of waste items (Stringham, 1986). In American crows (Corvus bra-
chyrhynchos), the survival rate is greater near urban settlements where waste availability is high (Marzluff and Neatherlin,
2006). Also, olive baboons that use rubbish dumps improve their infant survivorship compared with olive baboon that do
not use these sites (Eley et al., 1989).
On the contrary, decreased survival rates can be due to negative interaction between species or adverse effects after waste
ingestion. In banded mongoose, young males belonging to refuse-feeding groups have higher mortality than other non-dump
feeders due to predation by other species (Otali and Gilchrist, 2004). The death of a polar bear was reported as a consequence
of using waste as food resource (Lunn and Stirling, 1985). Some items of waste ingested in rubbish dumps (e.g., plastic) by
white storks can be related to death by collision with power lines (Peris, 2003). Therefore, it is clear that this kind of foraging
strategy is positive in some aspects but can cause important negative impacts like individuals death. However, there is little
information about the survival rates in dumps.

5.4. Population abundance

Food availability from rubbish dumps enhances population abundance, especially in birds but also in mammals and
reptiles (Jessop et al., 2012; Newsome et al., 2015; Oro et al., 2013). Many studies on different bird species as rooks (Olea and
Baglione, 2008), turkey vultures (Cathartes aura) (Torres-Mura et al., 2015) and house crow (Corvus splendens) (Saiyad et al.,
2015) show population increases when using organic waste as food resource. In the case of rooks, the population increase can
be up to 3.7 times compared with birds not using waste (Olea and Baglione, 2008). Also, studies in gulls show that this kind of
€ 1998).
food is related to colonies expansion in different parts of the world (Bosch et al., 1994; Duhem et al., 2008; Kilpi and Ost,
However, some studies suggest that the importance of dump sites may have been exaggerated because the presence of gulls
not always implies foraging behaviour and the population growth could be due to other coexisting factors (Coulson, 2015;
Coulson and Coulson, 2008).
We found fewer studies regarding mammals and reptiles but all of them agree that rubbish dumps use increases the
population abundance. For example, an increase in the abundance of mammalian predators up to 7e8 fold was reported as a
consequence of the use of anthropogenic food resources like waste (Newsome et al., 2015). A comparison of two populations
of lace monitor in different landscapes concludes that there is a higher abundance in rubbish dumps (up to 3 fold) than in
14 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20

natural areas (Jessop et al., 2012), as also happens in the common water monitor lizard (Varanus salvator) (Uyeda, 2009). The
positive impacts of dumps in populations abundances may be due to an increase in reproduction performance or because they
may act as sink areas, producing changes in individuals movements.

5.5. Impacts on movement patterns

Food resources from dumps are an important factor influencing animal movement (Ciucci et al., 1997; Mirmovitch, 1995;
Tennent and Downs, 2008). Interestingly, this kind of food subsidies could cause changes in white stork migration patterns
(Tortosa et al., 2002), and have facilitated the establishment of resident populations in Europe (Rotics et al., 2017; Gilbert et al.,
2016). In black vultures (Coragyps atratus) these sites determine their roost selection since close food resources reduce en-
ergetic cost of movement (Novaes and Cintra, 2013). Similarly, rubbish dumps are more used by bald eagles from closest
communal roosts (Turrin et al., 2015). Crows and ravens have smaller home ranges near human settlement where they exploit
organic waste (Marzluff and Neatherlin, 2006). Similarly island foxes, have smaller home ranges in urban landscapes than in
rural populations due to food availability, especially refuse containers (Gould and Andelt, 2013). Also, the home range of
refuse feeders banded mongooses is more concentrated than that of no refuse feeders groups (Gilchrist and Otali, 2002), and
spotted hyenas and red foxes increased their home range after a change in waste availability (Bino et al., 2010; Kolowski and
Holekamp, 2008). In reptiles as the desert monitor (Varanus griseus) the home range is affected by the presence of Tel Aviv
municipal dump (Stanner and Mendelssohn, 1987). Therefore, these food subsidies alter vertebrate space use, particularly
reducing their home ranges but also modifying migration behaviour. This change in the movement patterns can have
different ecological consequences, like changes in pathogen distribution that those species carry (Mc Kay and Hoye, 2016).

5.6. Pathogens infection risk

The presence of pathogens in rubbish dumps is very common (Collins and Kennedy, 1992; Flores-Tena et al., 2007;
Matejczyk et al., 2011) and could be an important risk to the animals using them (Ortiz and Smith, 1994). However, we found
few studies addressing this topic and most of them were on genus Larus. Several studies on gulls show different pathogens
isolates on faecal samples, mainly Salmonella sp. (Butterfield et al., 1983; Fenlon, 1983, 1981; La Sala et al., 2013). In fact, gulls
from rubbish tips were responsible for a Salmonella outbreak in sheep and cattle in Scotland (Coulson et al., 1983). Influenza
virus infection in black headed gulls (Chroicocephalus ridibundus) may have been produced during aggregations in large
numbers on rubbish dumps (Jurinovi
c et al., 2014). Mammals (dogs, cats, foxes, wolves and monkeys, among others) that
congregate at rubbish dumps can acquire pathogens and be potential transmitters of zoonotic diseases. For instance, ingestion
of waste (cow meat) from rubbish dumps caused a tuberculosis outbreak (important zoonotic disease) in olive baboons
(Sapolsky and Else, 1987; Tarara et al., 1985) and after the decline of scavenger birds in India, dogs predominated in dumps
increasing the risk of Rabies and Leptospirosis infection to humans (Markandya et al., 2008; Ogada et al., 2012).
The few studies concerning pathogens and emerging pathogens that species can be exposed to, in rubbish dumps, do not
allow for general conclusions. This is an important research gap that should be covered. The role of those sites as pathogen
infection sources and the potential harm of pathogens on the individual health status and population trends are still almost
unknown and should be evaluated. Moreover, it is important to estimate the net balance between fitness improvement by
organic waste use and infection rates in these sites (Becker et al., 2015).

5.7. Toxics and foreign body ingestion

Toxic exposure is another important problem in rubbish dumps, particularly for amphibians that are at high risk of suffering
poisoning due to contaminants presents in these sites (García-Mun ~ oz et al., 2010; Reeves et al., 2008). In this sense, the toxicity
of the water from landfills induces mortality, malformations, decreased pathogen resistance and growth inhibition in embryos,
with decreasing effects at higher distance from these sites (Bruner et al., 1998; Gibble and Baer, 2011). In Spain, mortality and
malformation are present at higher values in the groups of amphibians exposed to soils of a dump due to the effects of the
different chemicals present in these sites (De Lapuente et al., 2014). For birds, like white storks, rubbish dumps are the most
important sources of toxic metals (particularly lead, but also mercury, cadmium and arsenic) found in blood samples of chicks
breeding next to them (De la Casa-Resino et al., 2014). Similarly, chicks and eggs from nests of black kites exposed to emissions
from a solid-waste incinerator have higher lead concentrations when they were closer to the incinerator (Blanco et al., 2003).
Bald eagles poisoned with barbiturates in rubbish dumps were reported as a consequence of euthanized animals ingestion
(Millsap et al., 2004), and contamination by a discarded battery killed a polar bear (Lunn and Stirling, 1985).
Plastic and foreign bodies ingestion seem to be important especially in birds, since those items commonly appear in pellets
or stomach contents (Ballejo and De Santis, 2013; Henry et al., 2011; Houston et al., 2007; Ballejo et al. in press). This acci-
dental ingestion can produce toxicity or intestinal obstruction. Plastic ingestion is observed in different species as white storks
~ igo Elías, 1987; Sazima, 2013; Torres-Mura et al., 2015), particularly when roosting
(Peris, 2003), turkey and black vultures (ln
close to rubbish dumps (Ballejo and De Santis, 2013). There could be a differential foreign body ingestion according to age,
since in some species immature birds eat more of this material than adults (Henry et al., 2011; Peris, 2003; Turrin et al., 2015).
In this sense, the ingestion of micro trash is the main cause of death of California condor nestlings (Rideout et al., 2012;
 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20 15

Walters et al., 2010). Unfortunately, despite the negative effect of the foreign bodies ingestion, particularly plastic ingestion
(Thompson et al., 2009), their impacts on the individual and population health are still poorly known.

5.8. Impacts on invasive and threatened species

5.8.1. Introduced-invasive species

Organic waste could be responsible for the population expansion of different introduced-invasive species. We found
different introduced-invasive species, some of them listed as 100 of the world's worst alien invasive species in the Global
Invasive Species Database, which use rubbish dumps to acquire part of their dietary requirements. For example, feral cats
determine their spatial organisation according to the availability of food and the rate of food renewal from dumps (Mirmovitch,
1995; Tennent and Downs, 2008). The sacred ibis (Threskiornis aethiopicus) is an alien species in Florida, USA, that can survive
and increase its population by taking advantage of rubbish dumps (Calle and Gawlik, 2011) and its behavioural flexibility to use
organic waste as food sources is believed to favour its spread in Europe (Clergeau and Ye
sou, 2006). So, it is reasonable to think
that many other alien species can use this food source and they may increase and spread their populations favouring the in-
vasion process. This requires special attention in studies evaluating the potential for invasion of alien species.

5.8.2. Threatened species

In rubbish dumps threatened species, particularly scavenger birds, can find an alternative and predictable food resource to
sustain their populations. For instance, an endangered species as the Egyptian vulture takes advantage of food discards (waste
and carcasses) provided by humans in Socotra, Yemen (Gangoso et al., 2013). In fact, there is a novel mutualism where people
provide food resources, which facilitate the maintenance of the population of this species, whereas vultures provide a
regulating service by cleaning up carrion. Interestingly, the densest population known for this endangered vulture is reached
in this geographic location (Gangoso et al., 2013). Other critically endangered species, the hooded vulture and the endangered
crowed crane use these food subsidies in Africa (Annorbah and Holbech, 2012; Pomeroy, 1975). The critically endangered
California condor, the threatened Andean condor, the vulnerable Malayan sun bear and the vulnerable polar bear regularly
use rubbish dumps as a food resource (Finkelstein et al., 2015; Pavez, 2014.; Lunn and Stirling, 1985; Te Wong et al., 2004). It is
clear that some species of conservation concerns use and may depend on this kind of food subsidies. However, it is crucial to
know both the positive and negative effect of rubbish dumps on the population health of those species.

6. Indirect impacts of rubbish dumps on wildlife

6.1. Conflicts with humans

The congregation of animals in rubbish dumps near human settlements may increase human-animal conflicts like animal
attacks to people, livestock depredation and aircraft collision risk. In this sense, a great number of Hamadryas baboons (Papio
hamadryas) associated to dumps near cities, produce high conflicts with people since they encroach crops in agricultural areas
(Biquand et al., 1994). In Australia, dingoes (Canis lupus dingo) using organic waste attack people, and even the death of a
person has even been reported (Thompson et al., 2003). In Ethiopia, the intensity of livestock predation by hyenas is higher
near rubbish dumps (Girmay et al., 2015). Birds abundances are determined by the distance to dumps (Novaes and Cintra,
2013), and if they are located near airports the risk of aircraft collision increases (Burger, 2001; Francoeur and Lowney,
1997). All these examples of conflicts produce a negative perception of these species which is augmented by the non-
natural abundances of these species favoured by dumps.

6.2. Impacts on species that do not use rubbish dumps

Species that exploit rubbish dumps can negatively affect others that do not use these sites. For instance, a species that benefits
from these sites as the sacred ibis in Africa, predates on eggs of a threatened species, the cape cormorants (Phalacrocorax capensis)
(Williams and Ward, 2006). Similarly, the population growth of kelp gulls (Larus dominicanus) can be negative for Magellanic
penguins (Spheniscus magellanicus) and other sea birds because of their predation on eggs and immatures (Yorio et al., 1998).
Gulls also attack whales modifying their behaviour and possibly contributing to the death of calves (Maro
n et al., 2015; Sironi
et al., 2009). The enhancement in crows and ravens population by food subsidies could also elevate predation risk in other
birds (Marzluff and Neatherlin, 2006). In the case of mammals, predator abundance and group size increase in populations that
include rubbish dumps, and can produce indirect impacts on other species like increased competition and predation (Newsome
et al., 2015). Therefore, an important indirect effect of dumps exists, and this might be stronger than it is known.

7. Ecosystem consequences of rubbish dumps

The use of organic waste by different species that improve reproductive parameters, increase their abundances and change
their movement patterns could have important implications at ecosystem level. Most species that exploit this kind of food
16 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20

subsidies are predators, so the increase in their populations can generate impacts on the food web (e.g., hyper predation) that
could lead to a cascade of ecological effects (Chapin Iii et al., 2000; Newsome et al., 2015). This is especially important if the
availability of organic waste is reduced because species shift to other food sources (Payo-Payo et al., 2015) and they can
produce changes in the predator-prey relationship and biodiversity loss (Chapin Iii et al., 2000; Newsome et al., 2015).
Rubbish dumps may favour the invasion process through the increase in the abundances of invasive species, not only
vertebrates but also parasites and plants (Pysek et al., 2003;). This may impact the ecosystem in different ways (e.g., by
competence, diseases, changes in nutrient cycling process etc.; Chapin Iii et al., 2000; Pysek et al., 2003; Ehrenfeld, 2003).
Moreover, non-invasive species that exploit these sites can influence the spread of invasive species to the landscape (Vidal
et al., 1998). For instance, over abundances of gulls may favour invasive plant species by producing soil disturbances (Vidal
et al., 1998).
Rubbish dumps can sustain populations of suboptimal individuals using this food resource to survive (Genovart et al.,
2010). These suboptimal individuals can introduce undesirable characters to the entire population (Parvinen, 2005), as
malformations or low pathogen resistance, which may affect the population fitness, and disease transmission in the entire
ecosystem. Moreover, the alterations in the movement patterns produced by these food subsidies can generate expansion of
different species to new territories, modifying species interactions, diseases spread and consequently ecosystem functioning
(Chapin Iii et al., 2000). For instance, the increment of gulls populations due to organic waste use may produce the
contamination of surface waters through faecal pollution in places far from dumps (Converse et al., 2012) affecting ecosystem
health (Rapport et al., 1998).
Finally, as highlighted before, some endangered species use these food subsidies to sustain their population, thus, changes
of availability of this source can produce reduction in reproductive parameters and decrease of population (Pons and Migot,
1995), and therefore the loss of their ecological role. The same for any species providing an important ecosystem service as
organic waste reduction (Ogada et al., 2012). For instance, scavenger birds carry out ecosystem services in dumps that can be
important for human health since they can be considered cleaners of organic waste and are important to avoid disease spread
(Gangoso et al., 2013; Ogada et al., 2012). If those species decrease, the problems associated to organic waste (pests,

Fig. 2. Direct and indirect impacts of dumps on vertebrate species.

 P.I. Plaza, S.A. Lambertucci / Global Ecology and Conservation 12 (2017) 9e20 17

pathogens) will increase (Markandya et al., 2008; Ogada et al., 2012). Therefore, while it is desirable to reduce the availability
of organic waste to wildlife, all of the mentioned ecosystem impacts should be considered in detail to evaluate the potential
contrasting impacts produced by changes in policies about waste management.

8. Conclusions

Rubbish dumps may produce contrasting impacts on wildlife and ecosystems (Fig. 2). In this review we found that more
studies are focused on positive than on negative impacts, except in amphibians. This could be because most studies are
focused on dumps as a food source, but it can also be because it is difficult to acknowledge and study negative sub lethal
effects. As positive impacts we found the enhancement of body condition and body mass, the improvement of reproductive
performance, the increment of population abundance, and survival rates. Also, these places can support endangered species
and can be used as a refuge. However, there are negative impacts like high probability of pathogen infections, poisoning,
foreign body ingestion and impacts on species that do not use these sites. Moreover, rubbish dumps can sustain introduced-
invasive species and enhance different kind of conflicts with humans. In addition, these sites change the pattern of move-
ment, migration, home ranges size, and behaviours of individuals from different species.
Therefore, it is important to highlight some consequences produced by this kind of food subsidies. First, the enhancement
of body condition, the improvement of reproductive performance, the increment of population abundances and survival rates
can be responsible for populations' growth of the species that exploit rubbish dumps. As a result of this, severe consequences
in species and populations that do not use these sites may occur due to inter specific competition and depredation. Second,
the high risk of poisoning, foreign bodies ingestion and pathogen infection may make these places ecological traps (Battin,
2004), with negative consequences for several species using them. Third, rubbish dumps could be a source of emerging
pathogens transmitted from the species that use these sites to other species that do not, and even to humans (Dobson and
Foufopoulos, 2001). Moreover, they can be transferred to other geographical sites by ecological processes as migrations.
Fourth, rubbish dumps might behave as invasion centres favouring the invasion process of exotic species, a subject that merits
special attention. Finally, changes in space use produced by these sites can be responsible for conflicts with humans like
disease transmission, attacks or aircraft collision risk, which produce important damages and economic costs.
Despite the fact that the different kind of waste disposal sites do not produce the same availability of organic waste, and
that some agencies in Europe are trying to reduce availability of this kind of food subsidies (Landfill Waste Council Directive,
European commission 2008, EU 2009), waste production is an acute problem which will worsen in the coming years
(Hoornweg et al., 2013). Therefore, large impacts can be expected for the near future associated with the important increase in
waste production (Hoornweg et al., 2013). It is necessary to focus on studying these impacts to adequately establish con-
servation and waste management practices. Undoubtedly, more research is needed to weigh positive and negative conse-
quences of rubbish dumps and to answer questions like: Are these sites important buffer places which are only used when
natural food is scarce? Are the populations of animals that use rubbish dumps refuse specialists that only forage in these sites?
How do introduced-invasive species benefit from waste places enhancing their invasion success? Are rubbish dumps
necessary for some endangered species to survive? What are the final consequences of the unbalances of the species that use
these sites in the ecosystem? Under the current scene of huge waste production there is a need of studies answering those
questions in order to make better decisions and to formulate better waste management policies.

Acknowledgements

n, G. Ignazi, F. Barbar, J. Guido, A. Macchia, O. Mastrantuoni,

We thank the comments of K. Speziale, A. Di Virgilio, P. Alarco
N. Rebolo Ifr

an, S. Crespi and three anonymous reviewers which helped to improve the first version of the manuscript. We
also thank to Consejo Nacional de Investigaciones Científicas y Te
cnicas (CONICET PIP(2014) 0758, Argentina) and Agencia
Nacional de Promocio
n Científica y Tecnolo

gicaAgencia Nacional de Promocio
n Científica y Tecnolo
gica (ANPCYTeFONCYT,
PICT (BID) 0725e2014, Argentina) for the financial support.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.gecco.2017.08.002.

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