Animal Biodiversity and Conservation 42.2 (2019)

389

Diet to tissue discrimination factors for
the blood and feathers of the
monk parakeet (Myiopsitta monachus)
and the ring–necked parakeet
(Psittacula krameri)
D. Mazzoni, N. A. Borray–Escalante,
A. Ortega–Segalerva, L. Arroyo,
J. González–Solís, J. C. Senar
Mazzoni, D., Borray–Escalante, N. A., Ortega–Segalerva, A., Arroyo, L., González–Solís, J., Senar, J. C., 2019.
Diet to tissue discrimination factors for the blood and feathers of the monk parakeet (Myiopsitta monachus)
and the ring–necked parakeet (Psittacula krameri). Animal Biodiversity and Conservation, 42.2: 389–395, Doi:
https://doi.org/10.32800/abc.2019.42.0389
Abstract
Diet to tissue discrimination factors for the blood and feathers of the monk parakeet (Myiopsitta monachus)
and the ring–necked parakeet (Psittacula krameri). Stable isotope analyses (SIAs) have been widely used in
recent years to infer the diet of many species. This isotopic approach requires using diet to tissue discrimination
factors (DTDFs) for each prey type and predator tissue, i.e., to determine the difference between the isotopic
composition of the predator tissues and the different prey that conform its diet. Information on DTDF values
in Psittaciformes is scarce. The aim of this study was to assess DTDF values for the carbon and nitrogen
isotopes of the monk parakeet (Myiopsitta monachus) and the ring–necked parakeet (Psittacula krameri), two
invasive alien species of concern. We fed captive birds of the two parakeet species on a single–species diet
based on sunflower seeds to establish the DTDFs for the blood and feathers. In the monk parakeet (N = 9)
DTDFs were Δδ13C 2.14 ‰ ± 0.90 and Δδ15N 3.21 ‰ ± 0.75 for the blood, and Δδ13C 3.97 ‰ ± 0.90 and Δδ15N
3.67  ± 0.74 for the feathers. In the ring–necked parakeet (N = 9), the DTDFs were Δδ13C (‰) 2.58 ± 0.90
‰
and Δδ15N (‰) 2.35 ± 0.78 for the blood, and Δδ13C 3.64 ‰ ± 0.98 and Δδ15N 4.10  ± 1.84 for the feathers.
‰
DTDF values for the ring–necked parakeet blood were significantly higher than those for the monk parakeet
blood. No difference was found between the two species in the DTDF for feathers. Our findings provide the
first values of DTDFs for blood and feathers in these parakeets, factors that are key to infer the diet of these
species based on SIA.
Key words: Stable isotopes, Parrots, Captive birds, Control diet, Invasive species
Resumen
Factores de discriminación entre la dieta y los tejidos para la sangre y las plumas de la cotorra argentina
(Myiopsitta monachus) y la cotorra de Kramer (Psittacula krameri). Los análisis de isótopos estables se han
venido utilizando de forma generalizada en los últimos años para inferir la dieta de numerosas especies. El
método isotópico consiste en utilizar factores de discriminación entre la dieta y los tejidos para cada tipo de
presa y tejido de depredador, es decir, determinar la diferencia entre la composición isotópica de los tejidos del
depredador y la de las distintas presas que integran su dieta. Hay muy poca información sobre los valores de
los factores de discriminación entre la dieta y los tejidos relativa a los psitaciformes. La finalidad de este estudio
fue evaluar los valores de los factores de discriminación de los isótopos de carbono y nitrógeno de la cotorra
argentina (Myiopsitta monachus) y la cotorra de Kramer (Psittacula krameri), que son dos especies exóticas
invasivas motivo de preocupación. Alimentamos a aves en cautividad de las dos especies de cotorra con una
dieta exclusivamente a base de semillas de girasol para establecer los factores de discriminación relativos a
la sangre y las plumas. En la cotorra argentina (N = 9), los factores de discriminación para la sangre fueron:
Δδ13C 2,14 ‰ ± 0,90 y Δδ15N 3,21 ‰ ± 0,75 y para las plumas: Δδ13C 3,97 ‰ ± 0,90 y Δδ15N 3,67 ‰ ± 0,74. Los
factores de discriminación de la cotorra de Kramer (N = 9) para la sangre fueron: Δδ13C (‰) 2,58 ± 0,90 y Δδ15N
(‰) 2,35 ± 0,78 y para las plumas: Δδ13C 3,64 ‰ ± 0,98 y Δδ15N 4,10  ± 1,84. Los valores de los factores de
‰
discriminación entre la dieta y la sangre de la cotorra de Kramer fueron significativamente más elevados que los
de la cotorra argentina. Con respecto a las plumas, no se observaron diferencias entre las dos especies. Nuestros
ISSN: 1578–665 X
eISSN: 2014–928 X

© 2019 Museu de Ciències Naturals de Barcelona
Papers are published under a
Creative Commons Attribution 4.0 International License

390

Mazzoni et al.

resultados proporcionan los primeros valores de los factores de discriminación para la sangre y las plumas en
cotorras, que son fundamentales para inferir la dieta de estas especies mediante el análisis de isótopos estables.
Palabras clave: Isótopos estables, Cotorras, Aves en cautividad, Dieta de control, Especies invasoras
Received: 02 I 19; Conditional acceptance: 08 IV 19; Final acceptane: 02 VII 19
D. Mazzoni, N. Borray, A. Ortega–Segalerva, L. Arroyo, J. C. Senar, Evolutionary and Behavioural Ecology Research Unit, Museu de Ciències Naturals de Barcelona, Psg. Picasso s/n., 08003 Barcelona, Espanya (Spain).– N.
Borray, J. González–Solís, Institut de Recerca de la Biodiversitat (IRBio) and Department de Biologia Evolutiva,
Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 643, Barcelona
08028, Espanya (Spain).
Corresponding author: D. Mazzoni. E–mail: daniele.mazzoni91@gmail.com

Animal Biodiversity and Conservation 42.2 (2019)

Introduction
Diet is a key aspect in ecological studies (Newton
and Brockie, 1998). In the last few decades, analyses
of stable isotopes of carbon and nitrogen have been
widely used as ecological tracers to assess the diet
of several species (Tieszen et al., 1983; Hobson and
Clark, 1992b; Becker et al., 2007; Bearhop and Inger,
2008). Nevertheless, deriving quantitative estimates of
dietary contributions needs precise estimates of the
difference in isotopic composition between predator
tissues and preys (diet to tissue discrimination factor,
DTDF) (Bond and Diamond, 2011; Parnell et al., 2013).
Recently, researchers have documented considerable
variation in DTDF computations. Some reviews and
meta–analyses summarized this variation as a function
of a number of environmental and physiological factors
that included environment (terrestrial, freshwater, marine), trophic level, taxon, tissue, metabolic rate (poikilotherm, homeotherm), nitrogenous excretion (ammonia,
urea, uric acid), and sample treatment procedures (Dalerum and Angerbjörn, 2005; Caut et al., 2008; Phillips
et al., 2014). As the DTDF is highlysensitive to these
factors and is species–specific, it needs to be estimated
for various taxa (McCutchan et al., 2003; Caut et al.,
2009). However, there is a lack of information for the
Psittaciformes order, to date computed only for the kea
Nestor notabilis (Greer et al., 2015).
The aim of this study was to estimate the DTDF of
13
C and 15N, the two most common stable isotopes
used to estimate the diet of a species, for the blood and
feathers of the monk parakeet (Myiopsitta monachus)
and the ring–necked parakeet (Psittacula krameri).
These two parakeets are currently widespread in Europe and other parts of the world and are considered
to cause severe damage to agriculture, ornamental
vegetation, and human facilities (Menchetti and Mori,
2014; Senar et al., 2016). DTDFs obtained from this
study will allow the development of mixing models to
investigate the diet of the species. Such information
may be fundamental in controlling their populations.
Material and methods
The birds used in this study were sampled in the city
of Barcelona. The two species have been present
in the area since the early 1970s (Batllori and Nos,
1985). The population of the monk parakeet reached
5,000 individuals in 2015, while the population of the
rose–ringed parakeet reached 340 individuals in 2014
(Senar et al., 2017a, 2017b).
Avian samples
We collected nine monk parakeets and nine rose–ringed parakeets of different ages and both sexes at the
Ciutadella Park (Barcelona city) during autumn (September) 2017 and winter (January) 2018, after the end
of their reproductive period. The birds were captured
with a modified Yunnick trap located on a terrace of
the Museu de Ciències Naturals de Barcelona. Monk
parakeets were housed in captivity at the museum for

391

90 days and rose–ringed parakeets for 75 days. As
DTDFs differ among food sources, throughout the entire
captivity period we fed parakeets with a single–species
diet based on sunflower seeds. We provided this single
food source for the entire study period to allow the
isotope ratios in the parakeet tissues to equilibrate with
their control diet (Kelly et al., 2012). Blood sampling was
conducted biweekly by puncturing the brachial vein and
collecting blood in an Eppendorf tube. This should allow
the verification of whether the feathers grown after the
acclimatization period reflect the isotope composition
of sunflower seeds and whether they allow a reliable
approximation of DTDF. We verified this by analyzing
the stabilization of isotopes in the blood throughout the
experiment. Breast feathers were removed at day 45
(monk parakeet) and 30 (rose–ringed parakeet) of the
experiment, and hence were forced to grow under the
same conditions for all individuals. We chose to remove
the feathers after six weeks because complete blood
turnover occurs generally in about 30 days (Pearson
et al., 2003). New induced feathers were again removed after six weeks when they were fully grown and
while they were still on the sunflower seed diet. To
calculate the DTDF of the blood in both species, we
used samples of the last biweekly puncturing, at the
end of the experiment, for both species.
Stable isotope analyses
As the lipid component of the diet can affect δ13C
values (Tarroux et al., 2010; Perkins et al., 2013), five
samples of sunflower seeds were previously washed
of lipids using successive rinses in a 2:1 chloroform:
methanol solvent, and were later oven–dried at 50 ºC
for 24 h. Feather samples were cleaned in a 0.1M
NaOH solution to prevent contamination, oven–dried
at 50 ºC for 24 hours and ground into a fine powder.
Blood samples were lyophilized and ground to a fine
powder, and then directly analyzed isotopically. We did
not perform lipid extraction on whole–blood or feather
samples because of the typically low proportion of
lipids in bird blood and feathers (Bearhop et al., 2002)
We did not apply any linear normalization equation
(LNE) to the lipid content of the blood. In fact, when
the ratio C:N is less or around 4, as we found in our
samples, it is not necessary to take the lipid content
of the samples for terrestrial animals into account
(Post et al., 2007). The C:N ratios for the blood were
3.31 ± 0.03 and 3.40 ± 0.17 for the monk parakeet
and the ringed–necked parakeet respectively.
The stable isotope analyses were performed at
the 'Serveis Científico–Tècnics' at the University of
Barcelona. Stable carbon and nitrogen isotope assays
for all samples were weighed using a micro–balance
Mettler Toledo MX5 and placed in tin cups and crimped
for combustion, using an elemental analysis–isotope
ratio mass spectrometry (EA–IRMS). Stable isotope
abundances are expressed in δ notation in parts per
thousand (‰) according to:
δX = [(Rsample/Rstandard) – 1] * 1,000
where X is

13

C or

15

N and R is the corresponding

Mazzoni et al.

392

Table 1. Mean isotopic values (± SD) of δ13C (‰) and δ15N (‰) for the diet item (N = 5), and for
blood samples (N = 9) and regrown feathers (N = 9) for monk and rose–ringed parakeets after being
fed in captivity with a single–source diet based on sunflower seeds over 90 and 75 days, respectively.
Tabla 1. Promedio de los valores isotópicos (± DE) de δ13C (‰) y δ15N (‰) relativos a la dieta (N = 5)
y a las muestras de sangre (N = 9) y las plumas nuevas (N = 9) de las cotorras argentina y de Kramer
tras haber sido alimentadas en cautividad con una fuente de alimentación exclusivamente a base de
semillas de girasol durante 90 y 75 días, respectivamente.
	

Sunflower
seeds	

	

	

Monk parakeet	
Blood	

Feathers	

δ C (‰)	

–27.04 ± 0.89	

–24.90 ± 0.12	

–23.07 ± 0.16	

δ N (‰)	

4.06 ± 0.73	

7.27 ± 0.18	

7.73 ± 0.13	

13
15

C/12C or 15N/14N ratio. The standard values for 13C
and 15N were Pee Dee Belemnite (PBD) and atmospheric nitrogen (AIR), respectively. Measurement
errors (SD) were ± 0.15 ‰ for δ13C and ± 0.25 
‰
for δ15N.
After allowing sufficient time for equilibration between the tissue and the control diet, the DTDF can
be estimated by a calculation:
13

∆δXtissue = δXtissue – δXdiet
i.e. the average isotopic value from the tissue minus
the average isotopic value from the food. We estimate
the variability of this calculation (standard deviation,
SD) as the square root of summed variances for
diet and tissues samples. (Giménez et al., 2016).
We carried out Kruskal–Wallis tests in JMP (SAS
Institute Inc., Cary, North Carolina) to assess whether
there were any statistically significant differences in
the DTDFs of the tissues between the two species
as well as between tissues within the same species.
To estimate the patterns of carbon and nitrogen
turnovers, we applied the exponential model:
y = a + beCT
where y represents the isotope value of the tissue
in question, a and b are parameters determined by
initial and asymptotic conditions, C is the turnover rate
of carbon in the tissue, and T is time (d) since the
diet switch (Tieszen et al., 1983; Hobson and Clark,
1992a; Suzuki et al., 2005) in JMP (SAS Institute Inc.,
Cary, North Carolina).
Results
Table 1 shows the results of our isotopic analyses for
the samples of sunflower seed, blood, and regrown
feathers. The analysis of the stabilization of isotopes
in the blood throughout the experiment provided a
low fit to the exponential model (R2 < 0.20 in all
cases). Half–life turnover rates for ringed–necked
parakeets were estimated in 25.5 ±  20.1 days for
δ13C and 21.3 ± 17.7 days for δ15N, whereas those

Rose–ringed parakeet
Blood	

Feathers

–24.46 ± 0.11	 –23.40 ± 0.40
6.41 ± 0.28	

8.16 ± 1.69

for monk parakeets were 52.2 ± 35.3 days for δ13C
and 10.4 ± 4.31 days for δ15N. However, the curves
approached an asymptote before the feathers were
removed (fig. 1). Birds of both species maintained on
the sunflower seed diet showed remarkably consistent
isotope values for blood after this stabilization (fig. 1).
Since we obtained suitable isotopic dietary shifts and
stabilization was reached before inducing regrowth,
for both the monk and the rose–ringed parakeets,
we proceeded to estimate DTDF for each species
(table 2). The two species differed in blood DTDF
values for both isotopes (Kruskal–Wallis test: δ13C
x2(1) = 12.79, p < 0.001; δ15N x2(1) = 12.79, p < 0.001).
However, the DTDF values of the feathers did not
differ significantly between the two species (Kruskal–
Wallis test: δ13C x2(1) = 2.38, p = 0.12; δ15N x2(1) = 1.22,
p = 0.26). The comparison of DTDF values between
the two tissues within the same species resulted in
statistically significant differences for both isotopes
(monk parakeet blood vs. feathers: δ13C x2(1) = 12.79,
p < 0.001; δ15N x2(1) = 12.79, p < 0.001; rose–ringed
parakeet blood vs. feathers: δ13C x2(1)  = 12.79,
p < 0.001; δ15N x2(1)  = 5.48, p = 0.02).
Discussion
The stabilization of both isotopes in monk parakeet
blood seems to be reached earlier than in ring–necked
parakeets. This suggests that the diet of the individuals
in the wild was similar to the diet provided in captivity
for monk parakeets but not so similar for rose–ringed
parakeets. As a consequence, stabilization in isotope
blood values followed a flat trend, and hence, the
exponential model was not the most suitable model
to explain the turnover patterns. This is not surprising
since the 'exponential–fit' approach overemphasizes
data at the extremes (Cerling et al., 2007).
The DTDFs for δ15N of the feathers in M. monachus
(3.67 ± 0.74  and in P. krameri (4.10 ± 1.84) are
‰)
close to the frequently adopted DTDF value of 3.40 ‰
per trophic level (Post, 2002). Comparisons of δ13C
DTDF values obtained in this work with that of other

Animal Biodiversity and Conservation 42.2 (2019)

393

-24.3

-24.5

-24.5
δ13C (‰)

-24.3

-24.9

δ13C (‰)

-24.9
-25.2

-25.2

-25.5

-25.5

-25.8
0

15

30

-25.8
45 60 75 90
0 15
Day						

45
Day

60

75

90

8.5
δ15N (‰)

9.5

8.5
δ15N (‰)

9.5

30

7.5
6.5

6.5
5.5

5.5
4.5

7.5

0

15

30

4.5
45 60 75 90
0 15
Day						

30

45
Day

60

75

90

Fig. 1. Change in isotopic values for δ13C and δ15N in the blood of captive monk (Myiopsitta monachus)
(left) and ring–necked parakeets (Psittacula krameri) (right) switched on day 1 from the wild diet to a
sunflower seed diet. The yellow dots represent the day on which we removed the feathers. The red
dots represent the day we took the last blood samples, and the regrown feathers. We present element–
turnover patterns for carbon and nitrogen by fitting a single value to the means of the combined data for
all individuals for the diet on each extraction. Error bars represent the standard deviation of the mean
for all experimental birds. (N = 9 for each species).
Fig. 1. Cambio en los valores isotópicos de δ13C y δ15N en la sangre de la cotorra argentina (Myiopsitta
monachus) (izquierda) y la cotorra de Kramer (Psittacula krameri) (derecha) en cautividad en el primer día posterior al cambio de la dieta natural por la dieta a base de semillas de girasol. Los puntos
amarillos representan el día en que se extrajeron las plumas. Los puntos rojos representan el día en
que se tomaron las muestras de sangre y las plumas nuevas. Presentamos los patrones de recambio
del carbono y el nitrógeno ajustando un único valor al promedio de los datos combinados de todos los
individuos para la dieta en cada extracción. Las barras de error representan la desviación estándar de
la media de todas las aves del experimento. (N = 9 para cada especie).

species is obscured by the fact that some studies do
not present the δ13C values with prior lipid extraction
(Hobson and Bairlein, 2003). The need to extract
lipids from the food source derives from the fact that
the carbon from the lipid fraction of the diet may not
contribute to the carbon content of proteins in blood or
keratin in feathers, and therefore the differential lipid
contents of food can contribute to variation in DTDF
as well as inflate its value, since isotopic values of
the lipid fraction are typically isotopically depleted
(Perkins et al., 2013). Regardless, we found that the
DTDFs for δ13C that we obtained for both species

(monk parakeet: 3.97 ± 0.90  and the rose–ringed
‰
parakeet: 3.64 ± 0.98  are among the highest
‰)
values reported for this isotope (Caut et al., 2009),
considerably exceeding the commonly assumed
0–1  DTDF value per trophic level (Post, 2002).
‰
Nevertheless, the high DTDF values for δ13C that we
found was similar to that found by Greer et al. (2015)
in the Kea parrot. This may result from the fact that,
parrots generally have higher basal metabolic rates
(BMRs) than other bird species (McNab, 2012). DTDF
values are positively correlated to the respiration rate
(De Niro and Epstein, 1978). The higher blood DTDF

Mazzoni et al.

394

Table 2. Diet to tissue discrimination factors (Δ13C and Δ15N) for feathers and blood for monk (N = 9)
and rose–ringed parakeets (N = 9) derived from a single–source diet based on sunflower seeds over
90 and 75 days, respectively.
Tabla 2. Factores de discriminación (Δ13C y Δ15N) entre la dieta y las plumas y la sangre de la cotorra
argentina (N = 9) y la cotorra de Kramer (N = 9) obtenidos a partir de una sola fuente de alimentación
a base de semillas de girasol durante 90 y 75 días, respectivamente.
	

Δδ13C (‰)		

Δδ15N (‰)

Feathers	
Monk parakeet	

3.97 ± 0.90	

	

3.67 ± 0.74

Rose–ringed parakeet	

3.64 ± 0.98	

	

4.10 ± 1.84

Blood			
Monk parakeet	

2.14 ± 0.90		

3.21 ± 0.75

Rose–ringed parakeet	

2.58 ± 0.90		

2.35 ± 0.78

in the rose–ringed parakeet compared to that of the
monk parakeet could, therefore, be a consequence of
ring–necked parakeets displaying a higher BMR than
monk parakeets.
The Δ13C and Δ15N values from the feathers of the
two species were higher than those from their blood
(table 2). The differences between Δ13C values from
blood and feathers are probably due to the fact that
the two tissues differ in biochemical composition
(Martínez del Rio et al., 2009). Feathers typically
have more positive Δ13C and Δ15N values than blood
or muscle (Caut et al., 2009).
In conclusion, our study provides the first values of
DTDFs for the monk and the rose–ringed parakeets
and contributes to the scarce knowledge of DTDF
values for the order Psittaciformes.
Acknowledgements
We thank Jéssica Borrego and Pilar Rubio for their
help in the laboratory analyses. We thank Victor
Peracho and Tomás Montalvo, from the Agencia de
Salut Pública de Barcelona, for their support. Birds
were captured and handled with special permission
EPI 7/2015 (01529/1498/2015) from the Direcció
General del Medi Natural I Biodiversitat, Generalitat
de Catalunya. The present study was funded by
CGL–2016–79568–C3–3–P research project to JCS
from the Spanish Research Council (Ministry of Economics and Competitiveness).
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