Écoscience

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Contrasting responses of generalized/specialized

mistletoe-host interactions under climate change

Juan Francisco Ornelas, Yuyini Licona-Vera & Andrés E. Ortiz-Rodriguez

To cite this article: Juan Francisco Ornelas, Yuyini Licona-Vera & Andrés E. Ortiz-Rodriguez
(2018): Contrasting responses of generalized/specialized mistletoe-host interactions under climate
change, Écoscience, DOI: 10.1080/11956860.2018.1439297

To link to this article: https://doi.org/10.1080/11956860.2018.1439297

Published online: 16 Feb 2018.

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ÉCOSCIENCE, 2018
https://doi.org/10.1080/11956860.2018.1439297

Contrasting responses of generalized/specialized mistletoe-host interactions

under climate change
Juan Francisco Ornelas , Yuyini Licona-Vera and Andrés E. Ortiz-Rodriguez
Departamento de Biología Evolutiva, Instituto de Ecología, A.C, Xalapa, Veracruz, Mexico

ABSTRACT ARTICLE HISTORY

Considering that parasitic plant distributions are constrained by host availability, we measure the effects Received 14 October 2017
Accepted 3 February 2018
of adding information of host distributions to predict distributions of mistletoes under climate change
using ecological niche modeling (ENM). We contrasted ecological niche models of two Psittacanthus KEYWORDS
mistletoe species, P. schiedeanus, a host-generalist species inhabiting cloud forests, and P. sonorae, a Climate change;
Bursera-specialist restricted to the Sonoran Desert. Mistletoe models that use only climate variables host-parasite interaction;
were contrasted with models that also take into account biotic interactions (i.e., host) to evaluate the Loranthaceae; mistletoes;
potential effects that future climatic conditions have on the distributions of these mistletoe-host Psittacanthus schiedeanus;
interactions. Current potential distributions of both mistletoe species were affected by environmental Psittacanthus sonorae
conditions under future climate change scenarios. However, future projected distributions differed MOTS CLÉS
between mistletoe species when including host interactions, with improved accuracy models for P. changement climatique;
schiedeanus. Our results are consistent with previous studies showing that biotic interactions can be interaction hôte-parasite;
important in structuring species distributions at regional scales. Loranthaceae; guis;
Psittacanthus schiedeanus;
Psittacanthus sonorae
RÉSUMÉ
Puisque les aires de répartition des plantes parasites sont contraintes par la disponibilité des hôtes,
nous avons mesuré l’effet de l’ajout d’information sur la répartition des hôtes dans la prédiction de
répartition d’espèces de gui sous changement climatique en utilisant la modélisation de niche
écologique (MNE). Nous avons comparé les modèles de niches écologiques deux espèces de
Psittacanthus, P. schiedeanus, une espèce généraliste des forêts ombrophiles, et P. sonorae, une
espèce spécialiste associée à Bursera et confinée au désert de Sonora. Les modèles n’utilisant que
des variables climatiques ont été comparés à des modèles prenant également en compte les
interactions biotiques (c.-à-d. les hôtes) pour évaluer les effets potentiels des conditions climatiques
futures sur la répartition des interactions gui-hôte. Les répartitions potentielles actuelles des deux
espèces de gui étaient affectées par les conditions environnementales sous les scénarios de
changement climatique. Toutefois, les répartitions futures projetées différaient entre les espèces
de gui lorsque les interactions avec les hôtes étaient prises en compte, avec amélioration de la
précision du modèle pour P. schiedeanus. Nos résultats confirment ceux d’études précédentes ayant
montré que les interactions biotiques peuvent jouer un rôle important dans la structuration de la
répartition des espèces à l’échelle régionale.

Introduction Infante et al. 2016; Pérez-Crespo et al. 2016). Given

the tied relationship and dependence of mistletoes on
Mistletoes (Loranthaceae) are constrained to co-occur
their hosts (Kuijt 1969, 2009), their geographical ranges
with their hosts, and if avian vectors disperse their
are then directly related to the distributions and the
genes, the distributions of these parasitic plants are
availability of suitable host trees (Norton and
also constrained by the distributions of their mutualis-
Carpenter 1998).
tic partners. However, most avian vectors of mistletoe
Watson (2009) proposed that host quality is one of the
parasites do not seem to be sufficiently specialized in
critical proximate factors determining which potential
their movements and foraging behaviors to isolate mis-
host plants are susceptible to infection, whereas vector
tletoe populations on different hosts (Watson 2001 and
behavior and host occurrence ultimately limit the poten-
references therein), and likely to be shared by mistle-
tial distribution of parasitic plants. This hypothesis
toes on different host species within a community (for
known as the ‘host quality’ hypothesis (Watson 2009)
alternative scenarios see Ollerton et al. 2007; Díaz

CONTACT Juan Francisco Ornelas francisco.ornelas@inecol.mx Departamento de Biología Evolutiva, Instituto de Ecología, A.C. (INECOL), Carretera
Antigua a Coatepec No. 351, El Haya, Xalapa, Veracruz 91070, Mexico
2018 Université Laval
2 J. F. ORNELAS ET AL.
posits that there are measurable differences in potential
host plants that define a group of individuals physiologi-
cally capable of supporting a parasite (i.e., truly suscep-
tible to infection). According to this hypothesis, variation
in the quality of potential hosts can account for nonran-
dom occurrence patterns of parasitic plants in many
systems, and broad-scale changes in host quality may
underlie geographic patterns of host switching and geo-
graphic range of parasites (Watson 2009). Given that host
specialization and the potential for host race formation
have been suggested for several mistletoe species (e.g.,
Nickrent and Stell 1990; Overton 1994, 1996, 1997;
Jerome and Ford 2002; López De Buen and Ornelas
2002; Lara et al. 2009; Ramírez and Ornelas 2012; Pérez-
Crespo et al. 2016), it is possible to expect that the
ecological niche of the mistletoe will not be distinct
from that of its hosts or vectors, and that their responses
to climatic changes over time would be concerted. Lira-
Noriega and Peterson (2014) used an ecological niche
modeling approach and tested whether the distribution
of the mistletoe Phoradendron californicum (Viscaceae)
in the Sonoran Desert is mediated by host distributions,
or by factors such as the mistletoe’s autecology or that of
its vectors. They found that P. californicum infections
occur in non-random subsets of the niche of each tested
host species and mistletoe infections in different hosts
occur under similar niche conditions, leading to the con-
clusion that host species get infected with mistletoe only
where they range into suitable and accessible areas for the
mistletoe.
The often tightly linked interactions between mistletoes
and their host species offer an interesting opportunity to
investigate the possible effects of climate change on their
geographic distributions, particularly when range shifts get
out of synchrony and lead to co-extinctions. Here we
contrast the performance of ecological niche models
under climate change scenarios of two Psittacanthus
(Loranthaceae) species, one widely distributed, host-gen-
eralist mistletoe species inhabiting cloud forests, P. schie-
deanus, and the other a Bursera-specialist mistletoe species
restricted to the Sonoran Desert, P. sonorae. Comparing
models that use only climate variables of the mistletoe
species with models that also take into account biotic
interactions (i.e., host niche), the resulting models are
contrasted to evaluate the potential effects that climate
change might have on the distributions of these mistle-
toe-host interactions. We expect that the host-generalist
and host-specialist mistletoe species will differ in their
responses to future climate change scenarios. Specifically,
shifts in current predicted distribution are expected for the
host-generalist mistletoe species, whereas contraction/
expansion of current predicted range is expected for the
Bursera-specialist mistletoe species.
Methods
Study system
Psittacanthus schiedeanus (Schltdl. & Cham.) G. Don is
a hemiparasite characteristic of cloud forests edges in
northern Mesoamerica, from northeastern Mexico to
the Guatemalan highlands (Kuijt 2009; Ornelas et al.
2016). Its dense-flowered inflorescences produce long-
lived (5–6 d), orange-to-yellow, self-compatible her-
maphroditic flowers (c. 7.5–8.5-cm long) from June
to September (Figure 1(a)). Flowers are mainly visited
by several species of hummingbirds, bananaquits
(Coereba flaveola Linnaeus), flowerpiercers (Diglossa
baritula Wagler), and several species of butterflies and
bees (Ramírez and Ornelas 2010; J. F. Ornelas, unpub-
lished data). Purplish-black, lipid-rich, fleshy (one-
seed) fruits occur asynchronously from November to
April. Ripe fruits are consumed and dispersed by sev-
eral bird species (López De Buen and Ornelas 2002),
most frequently Bombycilla cedrorum Vielliot,
Ptilogonys cinereus Swainson, and Myiozetetes similis
Spix (López de Buen and Ornelas 1999, 2001;
Ramírez and Ornelas 2009, 2012). Psittacanthus schie-
deanus parasitizes more than 20 host tree species in the
cloud forests (Cházaro and Oliva, 1988; López de Buen
et al. 2002), but in central Veracruz its prevalence
(number of infested trees of a given host divided by
the total number of trees) is higher on Liquidambar
styraciflua (L.) (27%) than it is on Quercus leiophylla A.
D.C. (4.4%), Quercus germana Cham. & Schldl. (1.5%)
and Acacia pennatula (Cham. & Schltdl.) (0.4%; López
de Buen and Ornelas 1999; Figure 1(a)). Cross-seed
inoculation experiments showed that seedling develop-
ment is greater on the most abundant host tree species
(Liquidambar styraciflua) and survival is greater when
mistletoe seeds are placed on their source host species.
Seeds collected from plants growing on L. styraciflua
and P. mexicana had a higher surviving when seeds
were inoculated on branches of the same host tree
species from which they were collected, from L. styr-
aciflua to L. styraciflua and from P. mexicana to
P. mexicana, whereas those from Q. germana to Q.
germana and from A. pennatula to A. pennatula,
respectively, had a lower success (Ramírez and
Ornelas 2012). These results suggest the potential of
some of the host species to influence the distribution of
P. schiedeanus at a larger geographical scale.
Psittacanthus sonorae (S. Watson) Kuijt, endemic to
the southern half of the Baja California Peninsula and
adjacent portions of Sonora and Sinaloa from near sea
level up to 720 m above (Kuijt 2009), has the northern-
most distribution of a species in the genus. It is the most
xeromorphic Psittacanthus species, with terete fleshy
 ÉCOSCIENCE 3

+ Host prevalence –
a) Liquidambar styraciflua Quercus germana Quercus leiophylla Acacia pennatula

H1 H2 H3 H4

b) Bursera microphylla Bursera hindsiana c)

H1 + H2 + H3 + H4

H1 H2
Figure 1. Conceptual framework of the effects of adding distribution areas of interacting host species based on local prevalence on
the ecological niche models (ENMs) of (a) the host-generalist mistletoe Psittacanthus schiedeanus, and (b) the Bursera-specialist
mistletoe, Psittacanthus sonorae (‘mistletoe’ model). Models were calibrated using the areas (H) delineated by the distribution of
one (‘single host’ model) or more host species (‘multiple host’ model) according to prevalence of P. schiedeanus (H1 = Liquidambar
styraciflua, H2 = Quercus germana, H3 = Quercus leiophylla, H4 = Acacia pennatula, H1+H2, H1+H2+H3, or H1+H2+H3+H4) and
P. sonorae (H1 = Bursera microphylla, H2 = Bursera hindsiana, or H1+H2), which represent the species barriers to dispersal and
infection (Table 1) (c). Final ENMs were projected under future climate change scenarios based on the evaluation of adding
sequentially one or more host species using true skill statistics (TSS) as presented in Table 2. Photos by P. J. Brewster (a) and E.
Gándara (b).

Table 1. Final ecological niche models of Psittacanthus schie-

deanus and P. sonorae using the occurrence of each mistletoe
mainly visited by Calypte costae hummingbirds and but-
species and the bioclimatic variables annual mean temperature terflies (Ornelas et al. Forthcoming 2018). Its ripe pur-
(BIO1), temperature seasonality (BIO4), annual precipitation plish-black, fleshy (one-seed) fruits (9 × 13 mm)
(BIO12), and precipitation seasonality (BIO15) from the produced from March to May are consumed and dis-
WorldClim database with or without the inclusion of layers of persed by several bird species, mainly Myiarchus ciner-
one or more host species (H).
ascens Lawrence, Phainopepla nitens Swainson and
Mistletoe species Ecological niche model Species
Toxostoma cinereum Xantus de Vesey (Overton 1994,
Psittacanthus Mistletoe model No interaction
schiedeanus 1996). Bursera microphylla A. Gray is commonly para-
Single host models Liquidambar styraciflua (H1) sitized by P. sonorae in the Sonoran Desert, and less
Quercus leiophylla (H2)
Quercus germana (H3) frequently B. hindsiana (Benth.) Engl., B. laxiflora S.
Acacia pennatula (H4) Watson, B. fagaroides (Kunth) Engl. (Burseraceae), and
Multiple host models H1+H2
H1+H2+H3
Cyrtocarpa edulis (Brandegee) Standl. (Anacardiaceae) in
H1+H2+H3+H4 the northern portion of the peninsula (Overton 1994,
Psittacanthus Mistletoe model No interaction 1996; Figure 1(b)). In Sonora, 27% of all B. microphylla
sonorae
Single host models Bursera microphylla (H1) trees were infected with mistletoe, whereas only 6% of B.
Bursera hindsiana (H2) hindsiana trees were infected (Rodríguez-Pacheco 2015).
Multiple host model H1+H2
Cross-dispersal experiments in northern Baja California
gave no evidence that P. sonorae consisted of two host-
leaves and the dry viscin area forming a sealed resinous specific races, one specializing on B. microphylla and the
capsule around the developing seedling considered adap- other specializing on B. hindsiana (Overton 1994).
tations to the desert environments (Kuijt 2009). Its few- Mistletoe seeds collected from plants growing on B.
flowered inflorescences produce one-day, partially microphylla and then hand-dispersed to B. microphylla
protandrous red-pinked flowers (c. 13–14 mm long) and B. hindsiana had a lower or equal establishment
from November to March (Figure 1(b)). Flowers are success when growing on B. microphylla than seeds
4 J. F. ORNELAS ET AL.

Table 2. True skill statistics (TSS) to evaluate the ideal cut suitability threshold of the modelled species into presence/absence maps
(see Methods). TSS was calculated using the minimum training presence logistic threshold (MinTPLT), the 10th percentile training
presence logistic threshold (T10LT) and the equal training sensitivity and specificity logistic threshold (ETSSLT), and then TSS values
were averaged among replicates.
TSS
Mistletoe Interacting hosts MinTPLT T10LT ETSSLT
Host generalist: Psittacanthus schiedeanus No interaction 0.132 ± 0.08b 0.505 ± 0.09bc 0.538 ± 0.11a
Liquidambar styraciflua (H1) 0.182 ± 0.03b 0.609 ± 0.09abc 0.631 ± 0.09a
Quercus leiophylla (H2) 0.191 ± 0.03b 0.631 ± 0.07ac 0.632 ± 0.10a
Quercus germana (H3) 0.119 ± 0.08b 0.604 ± 0.09abc 0.570 ± 0.08a
Acacia pennatula (H4) 0.203 ± 0.06b 0.544 ± 0.12bc 0.546 ± 0.10a
H1+H2 0.201 ± 0.04b 0.662 ± 0.07ab 0.648 ± 0.07a
H1+H2+H3 0.213 ± 0.05b 0.661 ± 0.07ab 0.637 ± 0.08a
H1+H2+H3+H4 0.320 ± 0.05a 0.684 ± 0.05a 0.669 ± 0.12a
Bursera specialist: Psittacanthus sonorae No interaction 0.541 ± 0.11a 0.608 ± 0.14a 0.632 ± 0.18a
Bursera microphylla (H1) 0.502 ± 0.13a 0.563 ± 0.14a 0.563 ± 0.22a
Bursera hindsiana (H2) 0.522 ± 0.14a 0.630 ± 0.15a 0.514 ± 0.28a
H1+H2 0.494 ± 0.14a 0.563 ± 0.20a 0.500 ± 0.26a
Numbers with different letters are significantly different after comparisons within each mistletoe species and TSS at P = 0.05 using the adjustment Tukey’s
method.

growing on B. hindsiana (Overton 1994). These results
along with the restricted host species range of P. sonorae
(Rodríguez-Pacheco 2015) suggest that the distribution of
both Bursera host species influence the distribution of P.
sonorae at a larger geographical scale (see also Ornelas
et al. Forthcoming 2018).
Ecological niche modeling: input occurrence data
Ecological niche modelling (Elith et al. 2011) was used
to predict the distributions of P. schiedeanus and P.
sonorae under current and future climate change sce-
narios. Mistletoe occurrence data were assembled
mainly from herbarium records from the Global
Biodiversity Information Facility (GBIF; http://www.
gbif.org/species/), and supplemented with records
from Kuijt (2009) and our geo-referenced records
from field collection for phylogeographic studies
(Ornelas et al. 2016, Forthcoming 2018). After careful
verification of every data location, excluding duplicate
occurrence records or in close proximity to each other
(c. 2.5 arc min) to reduce the effects of spatial auto-
correlation, we restricted the data set for the analysis to
119 unique presence records for P. schiedeanus and 34
for P. sonorae. We also collected occurrence data based
on herbarium voucher specimens of most common
host species of P. schiedeanus (L. styraciflua, Quercus
germana, Q. leiophylla, A. pennatula) and P. sonorae
(B. microphylla, B. hindsiana) across their entire range
from the GBIF database. The numbers of unique
occurrences used for these species were: L. styraciflua,
617; Q. germana, 196; Q. leiophylla, 58; A. pennatula,
859; B. microphylla, 241; and B. hindsiana, 44. Special
attention was paid to obtaining adequate numbers of
occurrence well spread across the species’ range.
Distributional records were input and analyzed to
infer an ENM with the maximum entropy algorithm
in MAXENT v. 3.4.1 (Phillips et al. 2006) and using the
raster package v. 2.5–8 (Hijmans et al. 2016) to extract
the data and the ‘resample’ package for convert the
LGM layers at the same resolution to the other layers
(30 arc-seconds) in R v. 3.4.1 (R Development Core
Team; http://www.r-project.org/).
Ecological niche modeling: potential distribution
maps
The models were calibrated using a geographical clipping
based on the biogeographic provinces proposed by
Morrone (2005, 2014)) as a hypothesis of the accessible
areas of P. schiedeanus and P. sonorae and altitude range
limits, which represent the species historical barriers to
dispersal and potential boundaries along the landscape
(Barve et al. 2011). First, we projected the verified occur-
rence records from the host species of P. schiedeanus or P.
sonorae in a map from Mexico. Then, we used the sha-
pefile from the biogeographic provinces provided for
Morrone (2005) and selected all the provinces that
included the points of occurrence of the host species of
P. schiedeanus and P. sonorae. As a second filter to clip the
layers, ecological or climatic barriers of each species were
delimited using a map of ecoregions (http://maps.tnc.org/
gis_data.html). We finally obtained one hypothetical ‘M’
region that integrates the distribution range of their host’s
species or accessible area for each species of mistletoe (i.e.,
accessible areas to the species via dispersal over relevant
periods of time; Barve et al. 2011), which combined the
ecological preferences and biogeographic barriers of P.
schiedeanus and P. sonorae. Climate layers were clipped
with the ‘M’ region for use in MAXENT analysis.
 ÉCOSCIENCE 5

We constructed niche distribution models to present Ecological niche modeling: threshold decision
and future scenarios for each of the host species to
We used the true skill statistic (TSS) to estimate the
evaluate the effects of adding host species distributions
accuracy of predictions of the modelled species into
on the niche model of each of the two mistletoe species,
presence/absence maps. TSS is a threshold-dependent
and the resulting models were then used as variables
measure of model performance that evaluates the accu-
(‘H’) during niche modeling of each mistletoe species
racy of predictive maps generated by presence-only
(Figure 1(c)). The host niche models for each of the
data, i.e., the ideal cut suitability threshold (Allouche
mistletoe species were constructed with 70% of the
et al. 2006; Liu et al. 2013). The TSS threshold corre-
locality records as training data and the other 30% as
sponds to the sum of sensitivity and specificity minus
testing data. Models were constructed with 10 cross-
one (the sensitivity is the proportion of presences cor-
validation replicates without clamping and extrapola-
rectly predicted, and the specificity is the proportion of
tion, and considering the average output grids as the
absences correctly predicted). There are different opi-
final predictive models. We ran 1,000 iterations for
nions on what threshold is more suitable (Liu et al.
each of the species with no clamping or extrapolation
2005). Here, we calculated the TSS for each replicate
to avoid artificial extrapolations from extreme values of
using the minimum training presence logistic threshold
the ecological variables; as such parameters are biased
(MinTPLT) that considers the least prediction value
towards the environmental envelope of background
associated with a presence record, the 10th percentile
points and occurrence data (Phillips et al. 2006) and
training presence logistic threshold (T10LT) that
considering the average logistic output grids as the
removes 10% of the most extreme presence values,
final predictive models. All other parameters in
and finally we used the equal training sensitivity and
MAXENT were maintained at default settings.
specificity logistic threshold (ETSSLT) in which the
obtained model has the same probability to predict
Ecological niche modeling: bioclimatic variables true presences or true absences. The MinTPLT,
T10LT and ETSSLT values from each of the model
To characterize environmental variation for each of the
comparisons (e.g., ‘mistletoe’ model, ‘single host’ mod-
two regions corresponding to the distributions of P.
els, ‘multiple host’ models; Table 1) were averaged and
schiedeanus and P. sonorae and their host species, we
TSS values were calculated from the 10,000 back-
obtained climatic variables representing current condi-
ground-replicates among replicates. TSS varies from
tions (1950–2000) mapped at a spatial resolution of c.
−1 to +1, where negative and around zero values indi-
2.5 arc min in each raster (Hijmans et al. 2005) from
cate that distributions are no better than random, while
the WorldClim database (http://www.worldclim.org).
values ranging between 0.4 and 0.8 are considered as
From the total set of available bioclimatic variables
acceptable models (Landis and Koch 1977; Fielding and
(BIO1–19), we selected four BIO variables to represent
Bell 1997). To distinguish among models the most
means and seasonality, while minimizing strongly cor-
useful in predicting the presence of mistletoe species,
related variables (Bateman et al. 2012) and allowed us
differences in TSS values among models were tested
to reduce the possibility that the variation in the mod-
with one-way ANOVAs and post hoc mean compari-
els was related to the different number of variables
sons using Tukey’s test in R.
used in each model and not to the different ones in
the modeling strategies that we used here. Our variable
set included annual mean temperature (BIO1), tem-
Effects of adding host species occurrence records to
perature seasonality (BIO4), annual precipitation
mistletoe projection models
(BIO12), and precipitation seasonality (BIO15).
Final models of P. schiedeanus and P. sonorae were The ‘mistletoe’ models and the most useful models
constructed using the occurrence data for each of the under present climate conditions for P. schiedeanus
mistletoe species and the bioclimatic variables of tem- and P. sonorae adding the interacting hosts (‘single
perature (BIO1, BIO4) and precipitation (BIO12 and host’ and ‘multiple host’ models) were then projected
BIO15) with or without the inclusion of layers of one onto future climate conditions and contrasted. Future
or more host species (H) are described in Table 1. Each climate conditions included two concentration path-
model was constructed with 10 cross-validation repli- ways RCP 4.5 (intermediate emission scenarios achiev-
cates without clamping or extrapolation, 10,000 back- ing an impact of 4.5 watts per square meter by 2100)
ground-replicates to estimate the accuracy of predictive and RCP 8.5 (hard emission scenario accomplishing an
maps (see below), 10,000 iterations, and the logistic increase of 8.5 watts per square meter by 2100) (IPCC
format in MAXENT 3.4.1. 2007; van Vuuren et al. 2011), from coupled
6 J. F. ORNELAS ET AL.
atmospheric-ocean general circulation models
(AOGCMs) based on the Community Climate System
Model (CCSM; Gent et al. 2011) and the Model
Interdisciplinary Research on Climate (MIROC;
Watanabe et al. 2010). Changes were investigated sepa-
rately only for the temporal framework 2061–2080
(average in 2070).
Results
The accuracy of predictive maps generated by pre-
sence-only data, i.e., the ideal cut suitability threshold
(TSS) with the highest threshold values for the models
of Psittacanthus schiedeanus was the 10th percentile
training presence logistic threshold (T10LT), while
the lowest values was shown in all cases by the mini-
mum training presence logistic threshold (MinTPLT)
(Table 2). The threshold values were similarly high for
the models of Psittacanthus sonorae using the T10LT
and the equal training sensitivity and specificity logistic
threshold (ETSSLT), while the lowest values was also
shown in all cases by MinTPLT (Table 2). The model
of P. schiedeanus host-generalist mistletoe with the
significantly higher T10LT value was the ‘multiple
host’ model (H1+H2+H3+H4) that included all host
species considered in this study, L. styraciflua, Q. ger-
mana, Q. leiophylla and A. pennatula (Table 2). In
contrast, no significant differences were found among
models of P. sonorae host-specialist mistletoe after post
hoc mean comparisons of higher T10LT and ETSSLT
values (Table 2). Based on these results, we decided to
project onto future climate conditions the ‘mistletoe
models’ of both species to be contrasted with the ‘mul-
tiple host’ model for P. schiedeanus with highest
threshold value (H1+H2+H3+H4) and, for consistency,
the ‘multiple host’ model for P. sonorae (H1+H2) that
included the two Bursera host species considered in
this study, B. microphylla and B. hindsiana.
Mistletoe ENMs under climate change
The potential distributions of P. schiedeanus and P.
sonorae show adequate fit with the known distribution
ranges of the species under both CCSM and MIROC
scenarios (Figures 2 and 3). Host-generalist P. schie-
deanus has a potential distribution area in the cloud
forests of the Sierra Madre Oriental, from southern
Tamaulipas to northern Oaxaca, and cloud forests of
the Sierra Madre de Chiapas, central highlands of
Chiapas, and the Sierra de Las Minas and Sierra de
Cuchumatanes in Guatemala. However, there was
overprediction in certain geographic areas of Mexico,
including those along the Trans-Mexican Volcanic Belt
and dry Central Valleys of Oaxaca, and those on the
Yucatan Peninsula that correspond to the distributions
of its closely related species P. calyculatus and P. maya-
nus, respectively (Figure 2). The potential distribution
area of Bursera-specialist P. sonorae includes arid areas
to the southern half of the Baja California Peninsula
and adjacent portions of Sonora and Sinaloa (Figure 3).
There were marked differences between mistletoe
species in their predicted distributions under future
climate change scenarios, the intermediate emission
scenario RCP 4.5 and the hard emission scenario RCP
8.5, for both the 2070 CCSM and MIROC scenarios
(Figures 2 and 3). When comparing the overlap
between present ranges and those predicted for future
conditions, the results obtained for P. schiedeanus
(‘mistletoe’ model) in general showed that the pre-
dicted distribution areas of suitable conditions contract
under future climate change conditions (Figure 2),
while those obtained for P. sonorae (‘mistletoe’
model) showed range shifts under future climate
change conditions (Figure 3).
Effects of adding host species occurrence records to
mistletoe projection models
When we overlapped the present and future predic-
tions of the two species adding host species occurrence
records to mistletoe projection models (most sup-
ported ‘multiple host’ models), host-generalist P. schie-
deanus was not restricted, since range contraction was
observed in predictive distribution models under both
CCSM and MIROC future climate conditions
(Figure 2). Contrary to our prediction, overlapping
the present and future predictions of the host-specialist
P. sonorae in the ‘multiple host’ model showed expan-
sion along both coastal sides of the Baja California
Peninsula and suitable conditions almost disappeared
in the continental distribution (Figure 3).
Discussion
ENMs under climate change
The current potential distributions of P. schiedeanus
and P. sonorae mistletoes do appear to be affected
under future climate change scenarios. The areas of
suitable environmental conditions for these mistletoes
needed for their survival expand/contract or shift loca-
tion under future climate change scenarios. These
results are not surprising, as current distribution of
suitable environmental conditions have been documen-
ted to change in many taxa under future climate
change scenarios (e.g., Téllez-Valdés et al. 2006;
 ÉCOSCIENCE 7

‘mistletoe’ model ‘multiple host’ model

(H1+H2+H3+H4)

CCSM

Present range Present range

RCP 4.5 range RCP 4.5 range
RCP 8.5 range RCP 8.5 range
Overlap Overlap

MIROC
Present range Present range
RCP 4.5 range RCP 4.5 range
RCP 8.5 range RCP 8.5 range
Overlap Overlap

Figure 2. Predicted distribution of Psittacanthus schiedeanus under two climate change scenarios CCSM and MIROC, from
conservative RCP 4.5 to extreme RCP 8.5 concentration pathways conditions, for 2070. Left models correspond to predictions for
Psittacanthus schiedeanus alone (‘mistletoe’ model) and predictions on the right (‘multiple host’ model) are for P. schiedeanus and
interacting host species (H1+H2+H3+H4), Liquidambar styraciflua (H1), Quercus germana (H2), Quercus leiophylla (H3) and Acacia
pennatula (H4). Black areas indicate overlap between model predictions.

Barrows 2011; Ponce-Reyes et al. 2012; Rojas-Soto et al.
2012; Gomes Vale and Brito 2015). Interestingly, pre-
dictive ‘mistletoe’ models for future conditions suggest
different responses of the studied mistletoe species. The
potential distribution of suitable areas for P. schiedea-
nus broadly matches the current distribution of cloud
forest in Mexico (e.g., Ornelas et al. 2013) and the
apparent contraction under future climate change sce-
narios agrees with that obtained by Ponce-Reyes et al.
(2012) and Rojas-Soto et al. (2012), who used a differ-
ent methodology and showed contraction and frag-
mentation of cloud forest to future climate change.
For instance, Rojas-Soto et al. (2012) used a set of 20
ENMs of cloud forest-adapted species and forecasted a
marked reduction of the predicted cloud forest (54–
76%) under 2050 climate change scenarios, mainly in
the northern region of its current range (Sierra Madre
Oriental) and the Pacific slope of Chiapas. A recent
study by Ramírez-Barahona et al. (2017) found that
populations within the species exhibit significant
genetic structure based on neutral molecular markers
that define three genetically distinct clusters, and range
shifts under past climatic conditions predicted by ENM
suggest post-glacial invasion of P. schiedeanus mistle-
toes to cloud forests (Ornelas et al. 2016).
The results obtained from the ‘mistletoe’ model of P.
sonorae showed contrasting patterns under future envir-
onmental conditions to those observed for P. schiedea-
nus, with range shifts and disappearance of current
suitable conditions under future climate particularly
for the continental populations. This result is surprising
because projected climate changes appear to be most
favorable for the Sonoran Desert, with 79% increase of
habitat suitable for Sonoran Desert scrub type through
2060 and vegetation communities of the Sonoran Desert
will continue to expand between 2060 and 2090
(Friggens et al. 2012). Also, a northern expansion has
been predicted for Bursera species during the intergla-
cial periods and contraction during glacial periods
(Gámez et al. 2014; Ornelas et al. Forthcoming 2018),
suggesting that Bursera host species of P. sonorae dis-
tributed at the northernmost distribution of the genus
should expand further under increased aridity predicted
for the Sonoran Desert (Munson et al. 2012). However,
8 J. F. ORNELAS ET AL.
‘mistletoe’ model
USA
CCSM
Present range
RCP 4.5 range
RCP 8.5 range
Overlap
MIROC
Present range
RCP 4.5 range
RCP 8.5 range
Overlap
Figure 3. Predicted distribution of Psittacanthus sonorae under two climate change scenarios CCSM and MIROC, from conservative
RCP 4.5 to extreme RCP 8.5 concentration pathways conditions, for 2070. Left models correspond to predictions for Psittacanthus
sonorae alone (‘mistletoe’ model) and predictions on the right (‘multiple host’ model) are for P. sonorae and interacting host species
(H1+H2), Bursera microphylla (H1) and B. hindsiana (H2). Black areas indicate overlap between model predictions.
the continental distribution of environmental condi-
tions for P. sonorae contracted (or disappeared) under
future climate change scenarios. A recent study by
Ornelas et al. (Forthcoming 2018) based on sequences
of chloroplast and nuclear molecular markers found
that two genetically distinct clusters (continental and
peninsular populations) within P. sonorae. Regarding
the temporal dynamics of its distribution, they also
found that areas of suitable environmental conditions
are stable over time, from the Last Inter Glacial to
present conditions, which is consistent with the
observed stability for the distribution of areas of ende-
mism of Bursera in Mexico under past conditions
(Gámez et al. 2014), and with the high levels of
Bursera phylogenetic community structure suggesting
low dispersal among vegetation communities (De-
Nova et al. 2012). Future work of developing genetic
information with neutral markers and incorporating
that genetic information into species distribution mod-
els might give more accurate predictions of species dis-
tributions under climate change (e.g., Ikeda et al. 2017),
particularly for testing the basis of local (host) adapta-
tion and limited dispersal between plant communities of
‘multiple host’ model
(H1+H2)
Present range
RCP 4.5 range
RCP 8.5 range
Overlap
Present range
RCP 4.5 range
RCP 8.5 range
Overlap
P. schiedeanus and P. sonorae genetic clusters that differ
in both geography and environmental conditions
(Ornelas et al. 2016, Forthcoming 2018), and whether
the observed stability in the distribution of P. sonorae is
linked to the potential distribution of areas with higher
number of potential Bursera host species and the
marked phylogeographical structure of Bursera species
(De-Nova et al. 2012; Gámez et al. 2014).
Effects of adding host species occurrence records to
mistletoe projection models
Our study compared ENMs of the host-generalist P.
schiedeanus and the host-specialist P. sonorae fitted
with abiotic variables versus models that also included
the biotic variables, i.e., the actual occurrence data of
their host tree species, and projected under future
climate change scenarios. We found that the different
strategies for including known host species with higher
local prevalence values generally resulted in improved
accuracy models for the host-generalist P. schiedeanus
mistletoe species, but no significant differences were

observed in the overall accuracy between abiotic (‘mis-
tletoe’) and biotic (‘multiple host’) models for the
Bursera host-specialist P. sonorae mistletoe. Our results
are consistent with previous studies showing that biotic
interactions can be important in structuring and fore-
casting species distributions at geographical scales (e.g.,
Guisan and Thuiller 2005; Godsoe et al. 2009; Warren
et al. 2010; Lira-Noriega and Peterson 2014), particu-
larly when analyzing impacts of climate change (e.g.,
Brooker et al. 2007; Hegland et al. 2009; Van der
Putten et al. 2010; Giannini et al. 2013). In some
studies the inclusion of biotic predictors generally
improved the models fit (e.g., Heikkinen et al. 2007;
Meier et al. 2010; Pellissier et al. 2010; Giannini et al.
2013) and altered the projections of its future distribu-
tion (e.g., Araújo and Luoto 2007; Hof et al. 2012;
Giannini et al. 2013).
In our study the inclusion of host predictors
improved the model fit of the host generalist P.
schiedeanus predicting contraction in its distribution
under future climatic scenarios, while no significant
differences were observed for the model fit of host-
specialist P. sonorae with the inclusion of biotic
interactions and the projections of its future distri-
bution were altered under future climate scenarios.
There are a number of possible reasons for the dif-
ferences between our findings for P. schiedeanus and
P. sonorae. The results of host generalist P. schiedea-
nus were against the general view that specialized
biotic interactions are more important than weak
generalized biotic interactions in determining regio-
nal-scale distribution patterns (e.g., Giannini et al.
2013). However, correlative distributional patterns
are not necessarily indicative of the strength of inter-
actions. Our results suggest that areas of suitable
conditions under future climate scenarios for P.
schiedeanus may exist in areas suitable for their
hosts, but not the other way around. That is, the
future distribution of P. schiedeanus would be more
influenced by a small number of strong interactions
(most compatible, high-quality host species; Watson
2009) than a large number of weak ones.
Furthermore, the subset of susceptible hosts included
for the model fit of P. schiedeanus comprises a
dynamic assemblage changing over space and time.
Hence, moving from one area to the next along an
environmental gradient, frequency of host infection
would change. Similarly, as conditions change
between seasons or years, individual host plants
would move along the continuum from being sus-
ceptible to non-susceptible (Watson 2009). However,
our results also showed that in P. sonorae adding
information of host species did not improve
ÉCOSCIENCE 9
significantly the fit of the models. Nonetheless, we
found that although abiotic projections of P. sonorae
were similar for the current distribution, projected
distributions under climate change were different to
the inclusion of host interactions. Although P.
sonorae is more specialized on their hosts than P.
schiedeanus, it is possible that the effects of broad
climatic gradients masked those of biotic interactions
on its geographical distribution. We believe this is
unlikely because we use the actual distribution of the
host species to clip the geographic areas over which
mistletoe modeling was performed. Alternatively, dif-
ferent projected distributions under climate change
between the ‘mistletoe’ and ‘multiple host’ models
suggest that host species get infected with mistletoe
only where they range into suitable and accessible
areas for the mistletoe (Lira-Noriega and Peterson
2014; Ramírez-Barahona et al. 2017). As such our
predictive models suggest that P. sonorae will be
absent from the current continental distribution
under the future climate change scenarios evaluated
here, regardless of the northern expansion predicted
for Bursera host species.
Conclusion
We found that the distributions of host species trees that
have interactions with their hemiparasitic mistletoes are
useful predictors in species distribution models.
Furthermore, we showed how projections of future cli-
mate change impacts on mistletoe distributions are sen-
sitive to the addition of host interactions in the models.
However, the projected distributions (responses) under
climate change differed between mistletoe species to the
inclusion of host interactions. Thus, we suggest that more
accurate predictions of species distributions under cli-
mate change need to incorporate genetic information of
neutral markers into species distribution models to
understand as an integrated system how assemblages of
mistletoe/host species interactions would face local adap-
tation under future global climate changes.
Acknowledgments
The authors are grateful to the members of the project
‘Evolución de Psittacanthus en Mesoamérica: Sistemática,
filogeografía, ecología y manejo, y especiación’, particularly
Antonio Acini Vásquez Aguilar, Mariana Hernández Soto,
and Santiago Ramírez-Barahona. Permission to conduct
fieldwork was granted by the Mexican government
(Instituto Nacional de Ecología, Secretaría del Medio
Ambiente y Recursos Naturales, SGPA/DGGFS/712/1299/
12). A doctoral scholarship was granted from CONACyT to
Y.L.V. (155686) and A.E.O.R. (262563).
10 J. F. ORNELAS ET AL.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This project was funded by a competitive grant (155686)
from the Consejo Nacional de Ciencia y Tecnología
(CONACyT; http://www.conacyt.mx) and research funds
from the Departamento de Biología Evolutiva, Instituto de
Ecología, AC awarded to Juan Francisco Ornelas (20030/
10563).
ORCID
Juan Francisco Ornelas http://orcid.org/0000-0002-1124-
1163
Yuyini Licona-Vera http://orcid.org/0000-0001-6616-
361X
Andrés E. Ortiz-Rodriguez http://orcid.org/0000-0003-
4583-6701
References
Allouche O, Tsoar A, Kadmon R. 2006. Assessing the accu-
racy of species distribution models: prevalence, kappa, and
the true skill statistic (TSS). J Appl Ecol. 43:1223–1232.
Araújo M, Luoto M. 2007. The importance of biotic interac-
tions for modelling species distributions under climate
change. Global Ecol Biogeogr. 16:743–753.
Barrows CW. 2011. Sensitivity to climate change for two
reptiles at the Mojave-Sonoran Desert interface. J Arid
Environ. 75:629–635.
Barve N, Barve V, Jiménez-Valverde A, Lira-Noriega A,
Maher SP, Peterson AT, Soberón J, Villalobos F. 2011.
The crucial role of the accessible area in ecological niche
modeling and species distribution modeling. Ecol Model.
222:1810–1819.
Bateman BL, VanDerWal J, Williams SE, Johnson CN. 2012.
Biotic interactions influence the projected distribution of a
specialist mammal under climate change. Divers Distribut.
18:861–872.
Brooker RW, Travis JMJ, Clark EJ, Dytham C. 2007.
Modelling species’ range shifts in a changing climate: the
impacts of biotic interactions, dispersal distance and the
rate of climate change. J Theor Biol. 245:59–65.
Cházaro M, Oliva R. 1988. Loranthaceae del centro de
Veracruz y zona limítrofe de Puebla, IV. Cact Suc Mex.
33:42–48.
De-Nova JA, Medina R, Montero JC, Weeks A, Rosell JA,
Olson ME, Eguiarte LE, Magallón S. 2012. Insights into
the historical construction of species-rich Mesoamerican
seasonally dry tropical forests: the diversification of
Bursera (Burseraceae, Sapindales). New Phytol. 193:276–
287.
Díaz Infante S, Lara C, Arizmendi MC, Eguiarte LE, Ornelas
JF. 2016. Reproductive ecology and isolation of
Psittacanthus calyculatus and P. auriculatus mistletoes.
Peer J. 4:e2491.
Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ.
2011. A statistical explanation of MaxEnt for ecologists.
Diver Dist. 17:43–57.
Fielding AH, Bell JF. 1997. A review of methods for the
assessment of prediction errors in conservation presence/
absence models. Environ Conserv. 24:38–49.
Friggens MM, Warwell MV, Chambers JC, Kitchen SG. 2012.
Modeling and predicting vegetation response of western USA
grasslands, shrublands, and deserts to climate change
(Chapter 1). In: Finch DM, editor. Climate change in grass-
lands, shrublands, and deserts of the interior American West:
a review and needs assessment. Gen. Tech. Rep. RMRS-GTR-
285. Fort Collins (CO): U.S. Department of Agriculture,
Forest Service, Rocky Mountain Research Station; p. 1–20.
Gámez N, Escalante T, Espinosa D, Eguiarte LE, Morrone JJ.
2014. Temporal dynamics of areas of endemism under
climate change: a case study of Mexican Bursera
(Burseraceae). J Biogeogr. 41:871–881.
Gent PR, Danabasoglu G, Donner LJ, Holland MM, Hunke
EC, Hayne SR, Lawrence DM, Neale RB, Rasch PJ,
Vertenstein M, et al. 2011. The community climate system
model version 4. J Clim. 24:4973–4991.
Giannini TC, Chapman DS, Saraiva AM, Alves-dos-Santos I,
Biesmeijer JC. 2013. Improving species distribution mod-
els using biotic interactions: a case study of parasites,
pollinators and plants. Ecography. 36:649–656.
Godsoe W, Strand E, Smith CI, Yoder JB, Esque TC, Pellmyr
O. 2009. Divergence in an obligate mutualism is not
explained by divergent climatic factors. New Phytol.
183:589–599.
Gomes Vale C, Brito JC. 2015. Desert-adapted species are
vulnerable to climate change: insights from the warmest
region on Earth. Global Ecol Conserv. 4:369–379.
Guisan A, Thuiller W. 2005. Predicting species distribution:
offering more than simple habitat models. Ecol Lett.
8:993–1009.
Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø.
2009. How does climate warming affect plant–pollinator
interactions? Ecol Lett. 12:184–195.
Heikkinen RK, Luoto M, Virkkala R, Pearson RG, Körber JD.
2007. Biotic interactions improve prediction of boreal bird
distributions at macro-scales. Global Ecol Biogeogr.
16:754–763.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005.
Very high resolution interpolated climate surfaces from
global land areas. Int J Climatol. 25:1965–1978.
Hijmans RJ, van Etten J, Cheng J, Mattiuzzi M, Sumner M,
Greenberg JA, Lamigueiro OP, Bevan A, Racine EB,
Shortridge A. 2016. raster: geographic data analysis and
modeling. R package version 2.5-8. [accessed 2017
September 22]. http://cran.r-project.org/package=raster.
Hof AR, Jansson R, Nilsson C. 2012. How biotic interactions
may alter future predictions of species distributions: future
threats to the persistence of the arctic fox in Fennoscandia.
Divers Distrib. 18:554–562.
Ikeda DH, Max TL, Allan GJ, Lau MK, Shuster SM,
Whitham TG. 2017. Genetically informed ecological
niche models improve climate change predictions. Global
Change Biol. 23:164–176.
IPCC. 2007. Fourth Assessment Report of the
Intergovernmental Panel on Climate Change. Cambridge
(UK): Cambridge University Press.

Jerome CA, Ford BA. 2002. The discovery of three genetic
races of the dwarf mistletoe Arceuthobium americanum
(Viscaceae) provides insight into the evolution of parasitic
angiosperms. Mol Ecol. 11:387–405.
Kuijt J. 1969. The biology of parasitic flowering plants.
Berkeley (CA): University of California Press.
Kuijt J. 2009. Monograph of Psittacanthus (Loranthaceae).
Syst Bot Monogr. 86:1–361.
Landis JR, Koch GG. 1977. The measurement of observer
agreement for categorical data. Biometrics. 33:159–174.
Lara C, Pérez G, Ornelas JF. 2009. Provenance, guts, and fate:
field and experimental evidence in a host-mistletoe-bird
system. Ecoscience. 16:399–407.
Lira-Noriega A, Peterson AT. 2014. Range-wide ecological niche
comparisons of parasite, hosts and dispersers in a vector-
borne plant parasite system. J Biogeogr. 41:1664–1673.
Liu C, Berry PM, Dawson TP, Pearson RG. 2005. Selecting
thresholds of occurrence in the prediction of species dis-
tributions. Ecography. 28:385–393.
Liu C, White M, Newell G. 2013. Selecting thresholds for the
prediction of species occurrence with presence-only data. J
Biogeogr. 40:778–789.
López de Buen L, Ornelas JF. 1999. Frugivorous birds, host
selection and the mistletoe Psittacanthus schiedeanus, in
central Veracruz, Mexico. J Trop Ecol. 15:329–340.
López de Buen L, Ornelas JF. 2001. Seed dispersal of the
mistletoe Psittacanthus schiedeanus by birds in central
Veracruz, Mexico. Biotropica. 33:487–494.
López de Buen L, Ornelas JF. 2002. Host compatibility of the
cloud forest mistletoe Psittacanthus schiedeanus
(Loranthaceae) in central Veracruz, Mexico. Amer J Bot.
89:95–102.
López de Buen L, Ornelas JF, García-Franco JG. 2002.
Mistletoe infection of trees located at fragmented forest
edges in the cloud forests of central Veracruz, Mexico. For
Ecol Manag. 164:293–302.
Meier ES, Edwards TC, Kienast F, Dobbertin M,
Zimmermann NE. 2010. Co-occurrence patterns of trees
along macro-climatic gradients and their potential influ-
ence on the present and future distribution of Fagus syl-
vatica L. J Biogeogr. 38:371–382.
Morrone JJ. 2005. Hacia una síntesis biogeográfica de
México. Rev Mex Biodivers. 76:207–252.
Morrone JJ. 2014. Biogeographical regionalisation of the
Neotropical region. Zootaxa. 3782:1–110.
Munson SM, Webb RH, Belnap J, Hubbard JA, Swann DE,
Rutman S. 2012. Forecasting climate change impacts to
plant community composition in the Sonoran Desert
region. Global Change Biol. 18:1083–1095.
Nickrent DL, Stell AL. 1990. Electrophoretic evidence for
genetic differentiation in two host races of hemlock
dwarf mistletoe (Arceuthobium tsugense). Biochem Syst
Ecol. 18:267–280.
Norton DA, Carpenter MA. 1998. Mistletoes as parasites:
host specificity and speciation. Trends Ecol Evol. 13:101–
105.
Ollerton J, Stott A, Allnutt E, Shove S, Taylor C, Lamborn E.
2007. Pollination niche overlap between a parasitic plant
and its host. Oecologia. 151:473–485.
Ornelas JF, Gándara E, Vásquez-Aguilar AA, Ramírez-
Barahona S, Ortiz-Rodriguez AE, González C, Mejía
Saules MT, Ruiz-Sanchez E. 2016. A mistletoe tale:
ÉCOSCIENCE 11
postglacial invasion of Psittacanthus schiedeanus
(Loranthaceae) to Mesoamerican cloud forests revealed
by molecular data and species distribution modeling.
BMC Evol Biol. 16:78.
Ornelas JF, García JM, Ortiz-Rodriguez AE, Licona-Vera Y,
Gándara E, Molina-Freaner F, Vásquez-Aguilar AA.
Forthcoming 2018. Tracking host Bursera-trees: phylogeo-
graphy of endemic Psittacanthus sonorae (Loranthaceae), a
hummingbird-pollinated, bird-dispersed mistletoe in the
Sonoran Desert region. Amer J Bot. 00:00.
Ornelas JF, Sosa V, Soltis DE, Daza JM, González C, Soltis
PS, Gutiérrez-Rodríguez C, Espinosa de los Monteros A,
Castoe TA, Bell C, et al. 2013. Comparative phylogeo-
graphic analyses illustrate the complex evolutionary his-
tory of threatened cloud forests of northern Mesoamerica.
PLoS ONE. 8:e56283.
Overton JM. 1994. Dispersal and infection in mistletoe meta-
populations. J Ecol. 82:711–723.
Overton JM. 1996. Autocorrelation and dispersal of mistle-
toes: field and simulation results. Vegetatio. 125:83–98.
Overton JM. 1997. Host specialization and partial reproduc-
tive isolation in desert mistletoe (Phoradendron californi-
cum). SW Nat. 42:201–209.
Pellissier L, Bråthen KA, Pottier J, Randin CF, Vittoz P,
Dubuis A, Yoccoz NG, Alm T, Zimmermann NE,
Guisan A. 2010. Species distribution models reveal appar-
ent competitive and facilitative effects of a dominant spe-
cies on the distribution of tundra plants. Ecography.
33:1004–1014.
Pérez-Crespo MJ, Lara C, Ornelas JF. 2016. Uncorrelated
mistletoe infection patterns and mating success with
local host specialization in Psittacanthus calyculatus
(Loranthaceae). Evol Ecol. 30:1061–1080.
Phillips SJ, Anderson RP, Schapire RE. 2006. Maximum
entropy modeling of species geographic distributions.
Ecol Model. 190:231–259.
Ponce-Reyes R, Reynoso-Rosales VH, Watson JEM,
VanDerWal J, Fuller RA, Pressey RL, Possingham HP.
2012. Vulnerability of cloud forest reserves in Mexico to
climate change. Nature Clim Change. 2:448–452.
Ramírez MM, Ornelas JF. 2009. Germination of
Psittacanthus schiedeanus (mistletoe) seeds after passage
through the gut of Cedar Waxwings and Grey Silky-
Flycatchers. J Torrey Bot Soc. 136:322–331.
Ramírez MM, Ornelas JF. 2010. Pollination and nectar pro-
duction of Psittacanthus schiedeanus (Loranthaceae) in
central, Veracruz, Mexico. Bol Soc Bot Méx. 87:71–77.
Ramírez MM, Ornelas JF. 2012. Cross-infection experiments
of Psittacanthus schiedeanus: effects of host provenance,
gut passage and host fate on mistletoe seedling survival. Pl
Disease. 96:780–787.
Ramírez-Barahona S, González C, González-Rodríguez A,
Ornelas JF. 2017. The influence of climatic niche prefer-
ences on the population genetic structure of a mistletoe
species complex. New Phytol. 214:1751–1761.
Rodríguez-Pacheco T. 2015. Estudio ecológico de las plantas
parásitas en un matorral xerófilo de la costa de Sonora [BS
Thesis]. Hermosillo (Sonora, México): Universidad de Sonora.
Rojas-Soto OR, Sosa V, Ornelas JF. 2012. Forecasting cloud
forest in eastern and southern Mexico: conservation
insights under future climate change scenarios. Biodivers
Conserv. 21:2671–2690.
12 J. F. ORNELAS ET AL.
Téllez-Valdés O, Dávila-Aranda P, Lira-Saade R. 2006. The
effects of climate change on the long-term conservation of
Fagus grandifolia var. mexicana, an important species of
the Cloud Forest in Eastern Mexico. Biodivers Conserv.
15:1095–1107.
Van der Putten WH, Macel M, Visser ME. 2010. Predicting
species distribution and abundance responses to climate
change: why it is essential to include biotic interactions
across trophic levels. Phil Trans R Soc B. 365:2025–2034.
van Vuuren D, Edmonds J, Kainuma M, Riahi K, Thomson
A, Hibbard K, Hurtt G, Kram T, Krey V, Lamarque J-F,
et al. 2011. The representative concentration pathways: an
overview. Clim Change. 109:5–31.
Warren M, Robertson MP, Greeff JM. 2010. A comparative
approach to understanding factors limiting abundance
patterns and distributions in a fig tree–fig wasp mutual-
ism. Ecography. 33:148–158.
Watanabe M, Suzuki T, O’ishi R, Komuro Y, Watanabe S,
Emori S, Takemura T, Chikira M, Ogura T, Sekiguchi M,
et al. 2010. Improved climate simulation by MIROC5:
mean states, variability, and climate sensitivity. J Clim.
23:6312–6335.
Watson DM. 2001. Mistletoe –a keystone resource in forests
and woodlands worldwide. Ann Rev Ecol Syst. 32:219–249.
Watson DM. 2009. Determinants of parasitic plant distribu-
tion: the role of host quality. Botany. 87:16–21.