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Mammalia 74 (2010): xxx-xxx 2010 by Walter de Gruyter • Berlin • New York. DOI 10.1515/MAMM.2010.006
Short Note
Sample-size effects on diet analysis from scats of jaguars
and pumas
Rebecca J. Foster1,2,*, Bart J. Harmsen1,2 and
C. Patrick Doncaster1
1
School of Biological Sciences, University of
Southampton, Boldrewood Campus, Southampton, SO16
7PX, UK, e-mail: [email protected]
2
Panthera, 8 West 40th Street, 18th Floor, New York, NY
10018, USA
*Corresponding author
Keywords: diet; jaguar; puma; sample size; scat.
The Neotropics support more species of terrestrial vertebrate
than any of the other seven biogeographic realms, including
;1300 mammals and ;2600 reptiles (Mace et al. 2005,
Loyola et al. 2009). These provide a rich base of potential
prey for large neotropical predators. Single rainforest locations have yielded as many as 24 different taxa in the diet
of the jaguar, Panthera onca Linnaeus 1758, and 20 in the
diet of puma, Puma concolor Linnaeus 1771 (Garla et al.
2001, Leite and Galva˜o 2002, Moreno et al. 2006). Published
diets deduced from the scats of top predators rarely acknowledge the taxonomic richness of potential prey in the area
when evaluating whether the sample size can adequately represent the true dietary richness and breadth. Diet studies consequently risk underestimating plasticity in feeding ecology,
and wildlife managers could fail to distinguish predator species that have the potential to adapt to diminishing prey
diversity from those that do not. Jaguars and pumas coexist
in increasingly fragmented and human-dominated landscapes
where they must compete with humans not only for habitat
but also for prey (Leite and Galva˜o 2002, Foster et al. 2010).
Understanding dietary flexibility of such large felids will
allow us to better predict the impact of changes in prey availability on their long-term persistence, and on patterns of
coexistence (Foster et al. 2010). Here, we investigate the
influence of scat sample size on: (1) the number of taxa
detected in jaguar and puma diets, using data from 25 published studies; and (2) the precision of estimates of the relative occurrence of common prey species in jaguar and puma
diets, by subsampling from our own large datasets of geno-
typed scats (Foster et al. 2010). Relative occurrence is
defined as {number of prey items belonging to species X}/
{total number of prey items}=100. Species are considered
common at G5% occurrence in the diet.
The majority of the published diet studies of jaguars from
the neotropics have sampled from populations occupying
tropical and subtropical forest, whereas diet studies of neotropical pumas are more equally divided between tropical
and temperate forest and grassland ecoregions (Table 1).
Across the 18 ecoregions that have been sampled for jaguar
and puma scats (Table 1), terrestrial vertebrate species richness (and thus potential prey richness) is highest on average
in the tropical forests (mean"SDs1045"310, ns10), followed by tropical grasslands (715"74, ns3), temperate
grasslands (357"148, ns3) and temperate forests (229"86,
ns2). Mammalian species richness follows the same pattern.
Although not all these species can be appropriate prey for
big cats, we assume that the general trend for higher terrestrial vertebrate richness reflects the potential prey richness
of the area. The sample sizes of scats reported in the published studies rarely exceed 100 (jaguar medians32 scats,
Quartile 1s13, Q3s73, ns23 samples; puma medians51,
Q1s15, Q3s93, ns28). In these studies, the number of taxa
detected in the diets of both cats increases with increasing
sample size, both for forested and grassland tropical ecoregions (Figure 1). Such a pattern could conceivably occur if
smaller sample sizes were collected in areas with a coincidentally lower richness of prey, in which case we would
expect sample size to correlate positively with species richness. We found no significant correlations between the number of scats collected (for either cat) and the species richness
of terrestrial vertebrates (or of mammals only) in those ecoregions (Spearman rank correlations, all p)0.2, jaguar ns23,
puma ns28). We therefore conclude that the Figure 1 relationships between sample size and dietary richness are a true
cause and effect. The effect appeared to cease above a certain
sample size so a two-process model for significant early
increase (linear regression) followed by a plateau was fitted
to the data to identify the switch from rise to horizontal (Figure 1). The switch occurred at 69 scats for tropical jaguars
and 71 for tropical pumas (Figure 1A,B). No such pattern
was detected for temperate pumas, where the maximum
number of taxa (ns11) were detected in samples of G168
scats, whereas 10 taxa were detected in samples as small as
28 scats (Figure 1C). The insignificant increase in number
2010/016
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2 R.J. Foster et al.: Influence of sample size on scat analysis
Table 1 Ecoregion classification (Olson et al. 2001) of the 25 published studies of neotropical jaguar and puma diets from scats.
Ecoregion
Number of samples (n)
Refs
Jaguar
Puma
Tropical forests
Southwest Amazon moist forests
Alto Parana Atlantic forests
Serra do Mar coastal forests
Isthmian-Atlantic moist forests
Peten-Veracruz moist forests
Dry Chaco
Isthmian-Pacific moist forests
Bahia coastal forests
Yucatan moist forests
Jalisco dry forests
2
2
1
0
5
1
2
2
1
1
1
1
1
1
3
1
2
1
1
1
Temperate forests
Valdivian temperate forests
Magellanic subpolar forests
0
0
Tropical grasslands
Llanos
Pantanal
Caatinga
Temperate grasslands
Espinal
Patagonian steppe
Cordillera Central pa´ramo
Terrestrial vertebrate species
All
Mammals
1, 2
3, 4
5
6
7–10
11
12
13, 14
15
16
1486
1264
1173
1021
988
952
839
827
638
612
303
213
175
217
191
193
190
166
111
137
3
3
17, 18
19
290
168
46
30
1
4
1
1
0
1
20
21, 22
23
766
750
631
223
172
159
0
0
0
5
1
1
24
19
25
502
363
207
81
60
40
Where studies compared between habitats, seasons or sites, each is treated as a distinct sample. Terrestrial vertebrate species richness is
shown for each ecoregion (World Wildlife Fund 2006).
1: Emmons 1987; 2: Kuriowa and Ascorra 2002; 3: Crawshaw et al. 2004; 4: Azevedo 2008; 5: Leite and Galva˜o 2002; 6: Moreno et al.
2006; 7: Rabinowitz and Nottingham 1986; 8: Novack et al. 2005; 9: Weckel et al. 2006; 10: Foster et al. 2010; 11: Taber et al. 1997; 12:
Chinchilla 1997; 13: Facure and Giaretta 1996; 14: Garla et al. 2001; 15: Aranda and Sa´nchez-Cordero 1996; 16: Nu´n˜ez et al. 2000; 17:
Rau et al. 1991; 18: Rau and Jime´nez 2002; 19: Ya´n˜ez et al. 1986; 20: Polisar et al. 2003; 21: Dalponte 2002; 22: Azevedo and Murray
2007; 23: Olmos, 1993; 24: Branch et al. 1996; 25: Romo 1995.
of taxa detected with sample size probably reflects the lower
richness of potential prey available to pumas in temperate
compared with tropical ecoregions (Table 1). Within the neotropics, particularly in tropical ecoregions, Figure 1 suggests
that samples with less than ;70 scats could fail to detect all
taxa present in the diet. Clearly more informative comparisons between cats and regions could be made from estimates
of dietary breadth that evaluate sample sizes in relation to
the potential prey richness of the habitat.
By subsampling from our own large datasets of genotyped
scats (Foster et al. 2010), we demonstrate both under- and
over-representation of common prey types in the diet from
small samples, and significant underestimation of true richness even from samples of 100 scats. We analysed the number of scats required to adequately represent the diet of each
cat species, using 312 jaguar and 126 puma scats collected
in south-east Belize, Central America. Scats were genotyped
to distinguish jaguar from puma, and prey remains were
identified to species (Foster et al. 2010). The total number
of species consumed and relative occurrence of each was
calculated for an initial sample of ten randomly selected
scats, then repeatedly after each incremental addition to the
sample of five scats, up to 100 scats. This procedure was
repeated for 25 sequences of random selections. The species
accumulation curves (Figure 2) demonstrated that even 100
randomly selected scats greatly underestimated the true richness of the jaguars’ diet as defined by the 20 taxa present in
the full sample of 312 jaguar scats. Although as few as 45
scats might suffice to detect the six most common prey (i.e.,
those species making up G5% of the prey items in the full
sample, Figure 2), we can expect that their relative occurrence will be overestimated in proportion to the underestimation of rare prey. Likewise for pumas, 100 randomly
selected scats significantly underestimated the total of 11
taxa identified in the diet from 126 scats; however, 40 scats
were sufficient to detect the five most common prey species
(Figure 2). Our empirical findings corroborate the simulations of Trites and Joy (2005) who predicted that a sample
size of ;60 scats is required to detect principal prey species
()5% occurrence) in hypothetical diets containing up to 15
principal prey.
Variance in the estimates of prey occurrences was high at
low sample sizes (Figure 3). We considered estimates of
mean occurrence derived from multiple subsamples as pre-
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R.J. Foster et al.: Influence of sample size on scat analysis 3
Figure 2 Species accumulation curves for jaguar and puma diet.
Mean and 95% confidence intervals are shown for 25 trials. Dashed
lines indicate the number of prey species of all taxa (upper lines)
and of those with G5% relative occurrence (lower lines) detected
in 312 jaguar scats (A) and 126 puma scats (B).
Figure 1 Variation in number of taxa detected in neotropical jaguar and puma diets with sample size.
Data are from Table 1 and are analysed separately for (A) tropical
jaguars, (B) tropical pumas and (C) temperate pumas. Empty circles
indicate forest ecoregions, circles with black dot indicate grassland
ecoregions. For (A) and (B) a two-process model was fitted to the
data in which the switch from rise to horizontal was identified iteratively from the highest adjusted r2 values derived from significant
linear regression (p-0.001). The mean of the remaining data points
was substituted into the regression equation to calculate the threshold above which the number of taxa does not vary significantly
with sample size (indicated by an arrow).
cise if their 95% confidence intervals fell within "2 of the
‘true’ occurrence derived from the whole sample of scats
(jaguar: ns312, puma: ns126). Under this definition, the
minimum number of scats required for precise estimation of
each of the principle prey varied between prey species (Figure 3). To estimate the occurrence of the most common jaguar prey to within "2 of their ‘true’ occurrence required
;65 scats for armadillos (Dasypus novemcinctus) but only
15 scats for pacas (Agouti paca, Figure 3A,E, 95% confidence limits lie within the "2 band). For pumas, the minimum number of scats required varied from ;65 for pacas
to 25 for kinkajous, Potos flavus (Figure 3G–K). Relative
occurrence was consistently underestimated for some species, e.g., armadillos and pacas (jaguar, Figure 3A,E), but
overestimated for others, e.g., white-lipped peccary (Dictoyles pecari) and domestic sheep, Ovis aries (jaguar, Figure
3C,D,F). We can find no clear explanation for this difference.
Some studies of jaguar and puma diets have attempted to
assess post hoc whether the sample size analysed is large
enough to adequately describe diet (Nu´n˜ez et al. 2000, Azevedo 2008); however, the majority do not address the issue.
We advise that studies of jaguars and pumas from biodiverse
regions such as tropical rainforests should aim to collect samples of at least 70–100 scats to adequately describe diet.
Samples half this size will probably detect the principal prey
species but cannot yield reliable estimates of relative occurrence. The interpretation of findings from studies with low
sample sizes would be helped by presenting dietary components with an accompanying list or count of potential prey
species occurring in the local area and/or a species accumulation curve. Although felid scats are generally difficult
to find, particularly in hot humid climates where faecal material rapidly decomposes or washes away, often scat collection
is opportunistic and given low priority in felid studies. Scat
detector dogs are increasingly used for a range of studies
monitoring carnivore diversity and abundance (Harrison
2006, Long et al. 2007), and these have the potential to greatly improve scat collection rates for diet studies.
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4 R.J. Foster et al.: Influence of sample size on scat analysis
Figure 3 Relative occurrences of the principal prey species in jaguar (A–F) and puma (G–K) diets as a function of sample size, from
random subsamples of scats each replicated 25 times (showing mean and 95% CI).
Dashed lines indicate % occurrence estimates with all 312 jaguar scats and with all 126 puma scats (middle line, upper and lower lines
showing "2).
Acknowledgements
The study was funded by the Wildlife Conservation Society, the UK
Natural Environment Research Council, Tom Kaplan, Panthera, the
Liz Claiborne Art Ortenberg Foundation, the North of England Zoological Society, Brevard Zoo, Woodland Park Zoo and the Darwin
Initiative Grant 17-012 (the UK Department of Environment, Food
and Rural Affairs). Genetic analysis of the faecal samples was conducted by the Sackler Institute for Comparative Genomics at the
American Museum of Natural History. The Belize Audubon Society
was a partner in the research and gave logistical support, and we
are grateful to their park wardens at the Cockscomb Basin Wildlife
Sanctuary (CBWS), particularly Mr F. Tush, Mr F. Coc, and Mr M.
Pau, for helping with scat collection. We also thank Mr E. Pop for
field assistance and expertise, Mr F. Yau for his contribution to
fieldwork, and the numerous landowners who gave permission to
work on their properties. We thank Dr Scott Silver and Dr Linde
Ostro for initiating and facilitating our research in CBWS, and Dr
Alan Rabinowitz for his continued support.
References
Aranda, M. and V. Sa´nchez-Cordero. 1996. Prey spectra of jaguar
(Panthera onca) and puma (Puma concolor) in tropical forests
of Mexico. Stud. Neotrop. Fauna Environ. 31: 65–67.
Azevedo, F.C.C. 2008. Food habits and livestock depredation of
sympatric jaguars (Panthera onca) and pumas (Puma concolor)
¸ National Park area, South Brazil. Biotropica 40:
in the Iguacu
494–500.
Azevedo, F.C.C. and D.L. Murray. 2007. Spatial organization and
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
Article in press - uncorrected proof
R.J. Foster et al.: Influence of sample size on scat analysis 5
food habits of jaguars (Panthera onca) in a floodplain forest.
Biol. Conserv. 137: 391–402.
Branch, L.C., M. Pessino and D. Villarreal. 1996. Response of
pumas to a population decline of the plains vizcacha. J. Mammal. 77: 1132–1140.
Chinchilla, F.A. 1997. La dieta del jaguar (Panthera onca), el puma
(Felis concolor) y el manigordo (Felis pardalis) (Carnivoraa:
Felidae) en el Parque acional Corcovado, Costa Rica. Rev. Biol.
Trop. 45: 1223–1229.
Crawshaw, P.G.J., J.K. Ma¨hler, C. Indrusiak, S.M.C. Cavalcanti,
M.R.P. Leite-Pitman and K.M. Silvius. 2004. Ecology and con¸ National Park,
servation of the jaguar (Panthera onca) in Iguacu
Brazil. In: (K.M. Silvius, R.E. Bodmer and J.M.V. Fragoso, eds.)
People in nature: wildlife conservation in South and Central
America. Columbia University Press, New York. pp. 271–285.
Dalponte, J.C. 2002. Diet del jaguar y depredacio´n of ganado en el
Norte del Pantanal, Brazil. In: (R.A. Medellı´n, C. Equihua,
C.L.B. Chetkiewicz, P.G. Crawshaw, A. Rabinowitz, K.H. Redford, J.G. Robinson, E.W. Sanderson and A. Taber, eds.) El
Jaguar en el Nuevo Mileno. Fondo de Cultura Economica, Universidad Nacional Autonoma de Mexico, Wildlife Conservation
Society, Mexico City. pp. 209–221.
Emmons, L.H. 1987. Comparative feeding ecology of felids in a
neotropical rainforest. Behav. Ecol. Sociobiol. 20: 271–283.
Facure, K.G. and A.A. Giaretta. 1996. Food habits of carnivores in
a coastal Atlantic Forest of southeastern Brazil. Mammalia 60:
499–502.
Foster, R.J., B.J. Harmsen, B. Valdes, C. Pomilla and C.P. Doncaster. 2010. Food habits of jaguars and pumas across a gradient
of human disturbance. J. Zool. (Lond.) 280: 309–318.
Garla, R.C., E.Z.F. Setz and N. Gobbi. 2001. Jaguar (Panthera onca)
food habits in Atlantic Rain Forest of Southeastern Brazil. Biotropica 33: 691–696.
Harrison, R.L. 2006. A comparison of survey methods for detecting
bobcats. Wildl. Soc. Bull. 34: 548–552.
Kuriowa, A. and C. Ascorra. 2002. Dieta y densidad de posibles
presas de jaguar en las inmediaciones de lad zona de reserve
Tambopata-Candamo, Peru´. In: (R.A. Medellı´n, C. Equihua,
C.L.B. Chetkiewicz, P.G. Crawshaw, A. Rabinowitz, K.H. Redford, J.G. Robinson, E.W. Sanderson and A. Taber, eds.) El
Jaguar en el Nuevo Mileno. Fondo de Cultura Economica, Universidad Nacional Autonoma de Mexico, Wildlife Conservation
Society, Mexico City. pp. 199–207.
Leite, R.M.P. and F. Galva˜o. 2002. El jaguar, el puma y el hombre
en tres a´reas protegidas del bosque atla´ntico costero de Parana´,
Brasil. In: (R.A. Medellı´n, C. Equihua, C.L.B. Chetkiewicz, P.G.
Crawshaw, A. Rabinowitz, K.H. Redford, J.G. Robinson, E.W.
Sanderson and A. Taber, eds.) El Jaguar en el Nuevo Mileno.
Fondo de Cultura Economica, Universidad Nacional Autonoma
de Mexico, Wildlife Conservation Society, Mexico City. pp.
237–250.
Long, R.A., T.M. Donovan, P. Mackay, W.J. Zielinkski and J.S.
Buzas. 2007. Effectiveness of scat detection dogs for detecting
forest carnivores. J. Wildl. Manage. 71: 2007–2017.
Loyola, R.D., U. Kubota, G.A.B. da Fonseca and T.M. Lewinsohn.
2009. Key neotropical ecoregions for conservation of terrestrial
vertebrates. Biodivers. Conserv. 18: 2017–2031.
Mace, G., Masundire, H. and Baillie, J. 2005. Biodiversity. In: (R.M.
Hassan, R. Scholes and N. Ash, eds.) Ecosystems and human
well-being: current state and trends: findings of the Condition
and Trends Working Group of the Millennium Ecosystem
Assessment. Island Press, Washington, DC. pp. 77–121.
Moreno, R.S., R.W. Kays and R.J. Samudio. 2006. Competitive
release in diets of ocelot (Leopardus pardalis) and puma (Puma
concolor) after jaguar (Panthera onca) decline. J. Mammal. 87:
808–816.
Novack, A.J., M.B. Main, M.E. Sunquist and R.F. Labisky. 2005.
Foraging ecology of jaguar (Panthera onca) and puma (Puma
concolor) in hunted and non-hunted sites within the Maya Biosphere Reserve, Guatemala. J. Zool. (Lond.) 267: 167–178.
Nu´n˜ez, R., B. Miller and F. Lindzey. 2000. Food habits of jaguars
and pumas in Jalisco, Mexico. J. Zool. (Lond.) 252: 373–379.
Olmos, F. 1993. Notes on the food habits of Brazilian ‘caatinga’
carnivores. Mammalia 57: 126–130.
Olson, D.M., E. Dinerstein, E.D. Wikramanayake, N.D. Burgess,
G.V.N. Powell, E.C. Underwood, J.A. D’Amino, I. Itoua, H.E.
Strand, J.C. Morrison, C.J. Loucks, T.F. Allnutt, T.H. Ricketts,
Y. Kura, J.F. Lamoreux, W.W. Wettengel, P. Hedago and K.R.
Kassem. 2001. Terrestrial ecoregions of the world: a new map
of life on Earth. BioScience 51: 933–938.
Polisar, J., I. Maxit, D. Scognmillo, L. Farrell, M.E. Sunsquist and
J.F. Eisenberg. 2003. Jaguars, pumas, their prey base, and cattle
ranching: ecological interpretations of a management problem.
Biol. Conserv. 109: 297–310.
Rabinowitz, A.R. and B.G. Nottingham. 1986. Ecology and behaviour of the jaguar (Panthera onca) in Belize, Central America.
J. Zool. (Lond.) 210: 149–159.
Rau, J.R. and J.E. Jime´nez. 2002. Diet of puma (Puma concolor,
Carnivora: Felidae) in coastal and Andean ranges of Southern
Chile. Stud. Neotrop. Fauna Environ. 37: 201–205.
Rau, J.R., M.S. Tilleria, D.R. Martinez and A.H. Mun˜oz. 1991. Dieta de Felis concolor (Carnivores: Felidae) en areas silvestres protegidas del sur de Chile. Rev. Chil. Hist. Nat. 64: 139–144.
Romo, M.C. 1995. Food habits of the Andean fox (Pseudalopex
culpaeus) and notes on the mountain cat (Felis colocolo) and
puma (Felis concolor) in the Rı´o Abiseo National Park, Peru´.
Mammalia 59: 335–343.
Taber, A.B., A.J. Novaro, N. Neris and F.H. Colman. 1997. The
food habits of sympatric jaguar and puma in the Paraguayan
Chaco. Biotropica 29: 204–213.
Trites, A.W. and R. Joy. 2005. Dietary analysis from fecal samples:
how many scats are enough? J. Mammal. 86: 704–712.
Weckel, M., W. Giuliano and S. Silver. 2006. Cockscomb revisited:
jaguar diet in the Cockscomb Basin Wildlife Sanctuary, Belize.
Biotropica 38: 687–690.
World Wildlife Fund. 2006. WildFinder: online database of species
distributions, ver Jan-06. Available at: www.worldwildlife.org/
WildFinder.
Ya´n˜ez, J.L., J.C. Ca´rdenas, P. Gezelle and F.M. Jaksic. 1986. Food
habits of the southernmost mountain lions (Felis concolor) in
South America: natural versus livestocked ranges. J. Mammal.
67: 604–606.
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