Urban Ecosystems (2024) 27:231–237

https://doi.org/10.1007/s11252-023-01448-3

Evaluation of the diet of Didelphis virginiana in an urban area using

stable isotopes
Yury Glebskiy1,2 · Marcela Negrete-González2,3 · Luis Zambrano3 · Zenón Cano-Santana1

Accepted: 27 September 2023 / Published online: 3 October 2023

© The Author(s) 2023

Abstract
Human food waste is an essential resource for many animals that inhabit urban ecosystems and has allowed some spe-
cies to proliferate in cities. Virginia Opossums (Didelphis virginiana) are considered a good example of this process;
however, the real role of waste in this animal’s diet is still unclear. Therefore, this study aims to compare opossums’ diet
from urban and natural areas in Mexico City. Opossums were live-trapped, and samples of hair and blood were taken to
perform a stable isotope analysis of C and N. The results show that opossums from natural and urban areas, in general,
have a very similar isotopic niche; however, one natural location fell out of this pattern, and here opossums based their
diet on C3 plants. This suggests that opossum diets have a similar carbon source and occupy a similar trophic position in
urban and natural areas. However, there is a separation between opossums in urban and natural areas, not so much in the
isotopic niche, but in the feeding habits since natural areas, opossums prefer to feed in their distribution area despite the
availability of better quality food in the nearby urban areas.

Keywords Mexico City · Stable isotopes · REPSA · Terrain ruggedness

Introduction their behavior, for example birds change their singing pitch
to avoid interference by the urban noise (Slabbekoorn and
Urban ecosystems have become habitats for an important Peet 2003). One of the critical changes in the habitat is the
number of animals, such as large mammals as Puma con- increment of food for omnivorous animals (Gardener and
color, and other mammals as Bassariscus astutus, Didel- Sunquist 2003, Wright et al. 2012).
phis virginiana (Wright et al. 2012; Cisneros-Moreno and Urban areas provide many food sources for different ani-
Martínez-Coronel 2019; Robins et al. 2019). Those ecosys- mal groups. For example, birds eat seeds from trees and gar-
tems provide different types of habitats than wilderness; for den plants that grow in cities artificially provided food like
example, larger and more intense heat islands (Ackley et al. seeds and hummingbird feeders (Fuller et al. 2008; Coogan
2015), higher noise levels (Slabbekoorn and Peet 2003), and et al. 2018). Mammals also have a great selection of foods
different illumination patterns (Hopkins et al. 2018), and ranging from natural prey (even elk and deer; Robins et al.
animals had to adapt to these new conditions by changing 2019) to human trash (Hopkins and Forbes 1980; Smith
2016), which can be very abundant since worldwide urban
food waste is over 450 Gkg per year and is common in cities
Yury Glebskiy all around the world (Adhikari et al. 2006). Trash food pro-
agloti@ciencias.unam.mx vides a significant amount and variety of alimentary items
1
for the animals that can take advantage of them.
Laboratorio de Interacciones y Procesos Ecológicos,
Departamento de Ecología y Recursos Naturales, Facultad However, it is difficult to accurately determine the impor-
de Ciencias, Universidad Nacional Autónoma de México, tance of human-provided food for urban wildlife since many
Mexico City, Mexico of these food items leave little or no identifiable trails in
2
Posgrado en Ciencias Biológicas, Universidad Nacional the animal feces (Newsome et al. 2010). At the same time,
Autónoma de México, Mexico City, Mexico fecal analyses tend to sub or overestimate the importance of
3
Laboratorio de Restauración Ecológica, Instituto de Biología, certain alimentary items depending on their size and digest-
Universidad Nacional Autónoma de México, Mexico City, ibility (Roth and Hobson 2000; Milakovic and Parker 2011).
Mexico

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232 Urban Ecosystems (2024) 27:231–237

An alternative approach is based on the stable isotopic anal- Methods

ysis that has proved to be an efficient tool to establish the
alimentary resources of wild species and provides informa- The study was performed on the Pedregal de San Angel lava
tion about the assimilated alimentary items and not just the field left by the eruption of Xitle (in 280 ± 35 A. D.; Siebe
ingested ones (Hobson et al. 1996; Herrera et al. 2001). This 2000) in Mexico City (henceforth Pedregal). The original
method has allowed determining the food habitats (Craw- location is characterized by a very heterogeneous terrain
ford et al. 2008; Wurster et al. 2012), comparing alimentary and xerophilous shrub vegetation (Rzedowski 1954). Most
patterns among populations of the same species, and esti- of the lava field has been urbanized in the last decades, yet
mating anthropogenic food use by wild animals (Wurster some remnants of the natural vegetation remain, and some
et al. 2012). There are several studies on the alimentary of those are well preserved, consisting of up to several hun-
patterns in urban environments of species like foxes, bears, dreds of hectares (Lot and Camarena 2009). Therefore, the
coyotes, and raccoons (Merkle et al. 2011; Murray et al. study location is a very particular mosaic of urban and natu-
2015; Scholz et al. 2020; Nicholson and Cove 2022). How- ral areas in various states of conservation that allows for
ever, studies regarding other species, such as opossums in comparisons between natural and urban areas and isolated
urban environments, are lacking (although there are stud- natural remnants.
ies on the relation between opossums and their environment Opossums were live-trapped in eight locations inside the
including several anthropogenic factors; Walsh and Tucker Pedregal area (Fig. 1) using Tomahawk and pit-fall traps
2020, 2023). (description provided in Glebskiy and Cano-Santana 2021)
Therefore our study model is the Virginia opossum in 2018 and 2020. Samples of hair were taken from the
(Didelphis virginiana), an omnivorous mammal that has trapped animals. In some cases, 0.2–0.5 ml blood samples
greatly expanded its distribution range thanks to human were taken by puncturing the coccygeal vein. Samples were
activity (Walsh and Tucker 2020) and is well adapted to handled according to the instructions provided by the ana-
live inside urban areas (Wright et al. 2012). Its success in lyzing laboratories; Stable Isotope Laboratory at the Univer-
colonizing anthropogenic habitats has mainly been attrib- sity of Davis, California, for 2018 samples and Laboratorio
uted to omnivorous habits and its ability to consume human de Análisis de Isótopos Estables, UNAM for 2020 samples.
waste (Gardener and Sunquist 2003, Wright et al. 2012) to The δ of 14 C and 15 N isotopes and the proportion of C:N
the point that opossums in urban areas have consistently was calculated for each sample (for details on the method
smaller home ranges since the don’t need much area to see: https://stableisotopefacility.ucdavis.edu/carbon-and-
search for food (13.4–37.3 ha for urban males, 5.1–18.8 ha nitrogen-solids and Sharp 2017).
for females compared to 78.6–141.6 ha and 28.0–64.4 ha The isotopic niche (SEAC ‰2) was calculated using the
of the rural animals; Wright et al. 2012). This makes opos- SIBER package (Jackson et al. 2011) for opossums in each
sums the perfect model of successful use of human habitats location, based on their hair samples. Human hair-based iso-
by mammals. However, it is yet to be fully understood how topic niche was used to establish human food niche reference
these new habitats modify opossums’ diet. At the same time, values (Newsome et al. 2015). At the same time, a compari-
since it is a very common urban animal (Wright et al. 2012), son of the δ14C, δ15N and C:N ratio among locations, year
the knowledge of its behavior and ecology in urban eco- of sample collection, and the season (dry or rainy) were per-
systems will be a keystone in urban wildlife conservation. formed using a multifactorial ANOVA analysis, and a Tukey
Although there have been some studies related to its diet in HSD as a post-hoc test. The samples of hair and blood col-
urban areas, those studies are surprisingly scarce and con- lected in 2018 were analyzed using a multifactorial ANOVA
centrated on the northern portion of the species distribution using as factors: the location where samples were collected,
(Hopkins and Forbes 1980; Smith 2016). season (dry or rainy), and type of sample (hair or blood); a
This project aims compare the alimentary niche of Didel- Tukey test was used as a post-hoc.
phis virginiana in natural and urbanized locations inside
Mexico City using the stable isotope analysis. This data is
expected to provide information on the species’ behavior in Results
urban environments and help create more efficient manage-
ment programs for opossums. Differences in δ14C between the locations were found
(F = 11.543, p < 0.001), specifically, NA1 was different
from all other locations (lower δ14C values), and NA5 and
NA3 were different between them (p < 0.01 in all cases; see
Table 1). The δ15N analysis showed no significant differ-
ences. There were significant differences between locations

13
Urban Ecosystems (2024) 27:231–237 233

Fig. 1 Location of the sampling points

when comparing the C:N ratio (F = 13.517, p < 0.001), 12.45‰2 for NA4, and 4.02‰2 for UA3. The isotopic niche
NA1 had a higher C:N proportion than all other locations analysis shows a separation of the NA1 from the rest of the
(p < 0.05 in all cases; see Table 1). locations due to a lower δ14C (Fig. 2) and that the possums
The ANOVA test of hair and blood samples δ14C shows from the NA4 zone have the widest isotopic niche.
that there are differences between seasons, sample types,
locations, and the interaction between location and sample
type (F = 8.741 p = 0.006, F = 8.686 p = 0.006, F = 6.021, Discussion
p = 0.006 and F = 10.323, p < 0.001 respectively) but no dif-
ferences between years were found. Particularly, NA3 area Contrary to previous studies (Murray et al. 2015; Scholz
opossums have lower δ14C than UA1 and NA5 (p < 0.05), et al. 2020; Nicholson and Cove 2022), there are no differ-
and NA1 hair samples had lower δ14C than all the other ences in opossum isotopic data between the urbanized and
samples in all locations, including the blood sample from natural areas. All opossums are grouped in a small isotopic
the same location (p < 0.05 in all cases). The δ15N value was area (except for NA1 area Fig. 2); therefore, opossums do
higher in the NA1 area than in NA3 (F = 3.534, p = 0.041, not modify their isotopic niche when they feed on urban
Tukey p = 0.032). Comparisons of C:N proportions show areas. At the same time, there were no differences in δ15N,
differences between location (F = 12.544, p < 0.001) and which suggests that opossums maintain similar trophic posi-
the interaction of location and sample type (F = 13.954, tions in all locations. Therefore it appears that urbanization
p < 0.001). NA1 hair samples had a higher C:N ratio than has little effect on opossum’s isotopic niche. There are two
all other samples (p < 0.01), including blood samples from possible explanations for this: (1) opossums maintain the
NA1; however, there were no differences between NA1 same diet and search for the same food in urban and natural
blood samples and samples from other locations. environments, or (2) the isotopic values of the food avail-
According to SEAC ‰2 the isotopic niche was 7.03‰2 able to opossums are similar in both environments. The
for NA1 opossums, 3.23‰2 for NA2, 3.23‰2 for NA3 second hypothesis seems to be the most likely since human

13
234 Urban Ecosystems (2024) 27:231–237

populations commonly rely on C4 plants as the primary car-

-18.89 ± 0.82
Institute area

6.82 ± 1.23
3.08 ± 0.06
bon source (WHO 2003), and in our study locations, C4 and

Urbanized
CAM plants are very common and represent an important

2020
UA3

NA
NA
NA
proportion of primary production (Cano-Santana 1994).

8
8

0
Moreover, it is confirmed by the isotopic analysis of human
hair that appears close to the opossum’s hair (Fig. 2).

7.22 ± 0.56
Urbanized
Faculty of

-18.24 ± 1

3.2 ± 0.11
The year of data collection did not affect the isotopic
science

2020
niche (Fig. 2), suggesting that the opossum diet tends to
UA2

NA
NA
NA
be constant over time. When comparing the isotopic niche
2
2

0
amplitude, the widest niche (12.45‰2) was found in a small
Olympic village

2.99 ± 0.0001
-16.49 ± 0.32
7.89 ± 0.61 natural area NA4 this is likely due to the fact that this area
Urbanized

is too small (3 ha) to host an opossum population and indi-

viduals trapped there had to obtain food in different natural
2020
UA1

NA
NA
NA
and urban areas that surround NA4 (Fig. 1). On the other
2
2

hand, opossums in more extensive natural areas tend to have

-17.63 ± 0.42

smaller isotopic niches (except NA1), suggesting that they

Natural area

6.56 ± 0.57
3.05 ± 0.05
Cuicuilco

prefer to feed inside those areas when possible.

(20 ha)

In both natural and urban areas, opossums appear to

2020
NA5

NA
NA
NA

consume both C3 and C4/CAM plants in similar propor-

6
6

tions. However, the NA1 location stands out in terms of

δ14C (Fig. 2) and the C:N ratio. Opossums in this area rely
-18.93 ± 1.56
Natural area

7.05 ± 1.8
3.11 ± 0.1

more on C3 plants as their carbon source and have a greater

C:N ratio, which suggests a lower-quality diet (Crawfort et
(3 ha)
2020
NA4

NA
NA
NA
A8

al. 2008). This points out an important trait in opossum’s

6
6

dietary behavior. The NA1 is a mid-size natural area sur-

Table 1 Characteristics of the sampling sites used for this study. Values given with standard deviations

rounded by urban terrain (generally characterized by C4

West core NA2 West core NA2 Tlalpan forest

-19.84 ± 0.93
Natural area

-20.6 ± 0.77

diets; Walsh and Tucker 2023) and two of our sampling

6.52 ± 1.98
2.93 ± 0.02

6.35 ± 0.94
3.42 ± 0.1
(253 ha)

sites the UA2 and UA3, are located very closely to this area
2018
NA3

(Fig. 1; approximately 200 m in both cases), and cases of

14

12
9

opossums crossing between those areas were registered (by

GPS tracking between UA3 and NA1; López-Saldívar in
-18.48 ± 0.73
Natural area

prep. and capturing the same individual in the vicinity of

5.39 ± 0.83
3.03 ± 0.03
(114 ha)

UA2 and inside NA1; pers. obs.). However, there are sig-
2020

2020

nificant differences in carbon sources and even the quality

NA
NA
NA
8
8

of food. This suggests that even though opossums can move

across different locations and have proven to be omnivorous
-19.52 ± 0.66

-19.36 ± 0.68
Natural area

and opportunistic (McManus 1974); they conserve their

6.47 ± 0.74
3.01 ± 0.05

6.99 ± 1.01
3.43 ± 0.05
(114 ha)

feeding area and are unwilling to search for food in other

2018

2018

types of ecosystems, even when food is of lower quality and

8
2

they have access to different food sources. Therefore, there

is a separation between opossums in urban and natural areas
-22.19 ± 1.05

-19.38 ± 0.73
Natural area

based on their foraging habits.

7.94 ± 1.57
4.64 ± 1.03

7.73 ± 0.72
3.35 ± 0.01
East core

At the same time, there were differences in δ14C between

(54 ha)
2018
NA1

blood and hair samples in NA1. Both sample types were col-
Number of possums trapped 5
5

lected during the rainy season, but blood samples represent the
diet of the last months before collection (Crawfort et al. 2008),
while hair samples represent the diet over a more extended time:
Year of data collection

Blood samples taken

years or even the entire lifespan of this species since it does not
Average δ15N blood
Average δ14C blood
Average δ15N hair
Average δ14C hair

undergo seasonal molt (Walsh and Tucker 2021). Therefore,

Hair samples

NA1 Opossums only have their C3 diet during the dry season.
C:N blood
Area type

This raises two questions: why do opossums mainly consume

C:N hair

a C3-based diet, and why does this happen only during the dry

13
Urban Ecosystems (2024) 27:231–237 235

Fig. 2 Isotopic niche area (SEAC

‰2) of opossum groups from
different areas. Analysis based on
hair samples

season? The heterogenous terrain could explain the dominance dietary preferences. Furthermore, terrain ruggedness plays
of the C3 plants in the diet of the NA1 opossums; the Pedregal an important role in mid-size mammal ecology.
vegetation depends heavily on the amount of soil and the water
it can store (Cano-Santana 1994; Rzedowski 1954). In particu- Acknowledgements We are thankful to I. Castellanos-Vargas, M.
Guzmán-Torres D. E. Mejia-Figueras and K. Ramos-Rendon for tech-
lar NA1 is characterized by a more rugged terrain consisting of nical support, to the working teams of SEREPSA (S. Cram-Heydrich),
rocky formations and fissures in the rock that store important Cuicuilco archeological zone (R. López-Valenzuela), Villa Olímpica
amounts of soil, which in turn acts as water storage. This com- sports center (M. Barrera-Rangel) and Taller de Plantas of the Faculty
bination increases water availability which gives an advantage of Sciences UNAM (M. E. Muñiz-Díaz) for facilitating the permis-
sions and support for our study. This work was possible thanks to a
to the C3 plants; this is consistent with Cano-Santana (1994), scholarship by the CONACYT to YG (CVU 817316) and a PAPIIT
who observed that trees (generally C3) are more common in grant IN212121 (El efecto de la urbanización sobre el tlacuache Didel-
rugged terrain while plants of the family Poaceae (C4) are phis virginiana en un matorral xerófilo de la Ciudad de México) to
more common in the plain terrain. Therefore NA1 opossums ZCS. We thank the Posgrado en Ciencias Biológicas of the Universi-
dad Nacional Autónoma de México for its support to MNG and YG.
have access to C3-based food. However, it appears to be a sub- This paper is part of the requirements to obtain a Doctoral degree at the
optimal food source since they only resort to it during the dry Posgrado en Ciencias Biológicas, UNAM of YG.
season when resources are scarce and use their common C4/
CAM-based food sources (probably based on annual grasses) Author contributions All authors contributed to the study design
when available. This trait is of interest since a previous study and data interpretation. Data collection and statistical analysis were
performed by YG and MNG. All authors read and approved the final
showed that the terrain ruggedness is one of the most important manuscript.
factors to predict another mid-size mammal in the region: the
eastern cottontail (Glebskiy et al. 2018) suggesting that small- Funding This work was supported by a scholarship by the CONACYT
scale terrain characteristics (a factor generally overlooked in to YG (CVU 817316) and a PAPIIT grant IN212121 (El efecto de la
ecological studies) could have effect on the animals inhabiting urbanización sobre el tlacuache Didelphis virginiana en un matorral
xerófilo de la Ciudad de México) to ZCS.
the area.
Declarations
Conclusions Competing interests The authors have no relevant financial or non-
financial interests to disclose.
Virginia Opossums tend to be more conservative in their
feeding locations than expected from an opportunistic omni- Open Access This article is licensed under a Creative Commons
Attribution 4.0 International License, which permits use, sharing,
vore generalist. Urbanization has little effect on the isotopic
adaptation, distribution and reproduction in any medium or format,
niche of opossums; however, there is a separation between as long as you give appropriate credit to the original author(s) and the
opossums that inhabit urban and natural areas based on their source, provide a link to the Creative Commons licence, and indicate

13
236 Urban Ecosystems (2024) 27:231–237

if changes were made. The images or other third party material in this Lot A, y Camarena P (2009) El pedregal de san Ángel de la ciudad
article are included in the article’s Creative Commons licence, unless México: reserva ecológica urbana de la universidad nacional.
indicated otherwise in a credit line to the material. If material is not Págs. 19–25, en Lot, A., Cano-Santana, Z. (eds.). Biodiversidad
included in the article’s Creative Commons licence and your intended del ecosistema del Pedregal de San Ángel. Universidad Nacional
use is not permitted by statutory regulation or exceeds the permitted Autónoma de México, México
use, you will need to obtain permission directly from the copyright Merkle JA, Derbridge JJ, Krausman PR (2011) Using stable isotope
holder. To view a copy of this licence, visit http://creativecommons. analysis to quantify anthropogenic foraging in black bears.
org/licenses/by/4.0/. Human-Wildlife Interact 5(1):159–167
Milakovic B, Parker KL (2011) Using stable isotopes to define diets
of wolves in northern British Columbia, Canada. J Mammal
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