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Alpine ecosystems on islands are among the most isolated on Earth, leading to very high rates of endemism. Endemic species on oceanic islands are particularly vulnerable to invasive herbivores. In the alpine zone of Tenerife, which harbors a unique endemic flora, the dominance pattern of the two most dominant species in our days (Spartocytisus supranubius and Pterocephalus lasiospermus) has shifted in the last few decades, which may be a result of increasing rabbit pressure. In this study we explore how rabbits affect the population structure, soil nutrient composition and regeneration of our two target endemics within Teide National Park. For this purpose, we established 90 plots at 30 locations. Within 13 locations we sampled permanent exclosure plots that were established between 7 and 12 years before sampling, applying three treatments (full herbivory, rabbit herbivory and no herbivory). At one site we collected 80 soil samples to evaluate changes in soil chemistry and plant growth using a greenhouse experiment. Our results show that rabbits have a negative effect on the population structure of S. supranubius, while the contrary occurs with P. lasiospermus. Rabbit presence alters soil chemistry leading to a decline in nitrogen, which affects growth in both species. The presence of rabbits leads to a dominance shift in these two keystone endemic species, altering dominance patterns in the summit scrub of Tenerife. The decline of S. supranubius could represent the example of many endemic species of this system. Thus, we call for an immediate control of rabbit population (< 0.5 rabbits/ha) to protect this unique alpine endemic flora.
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ORIGINAL PAPER
Contrasting effects of invasive rabbits on endemic plants
driving vegetation change in a subtropical alpine insular
environment
Jonay Cubas .Jose
´Luis Martı
´n-Esquivel .Manuel Nogales .Severin D. H. Irl .
Raquel Herna
´ndez-Herna
´ndez .Marta Lo
´pez-Darias .Manuel Marrero-Go
´mez .
Marcelino J. del Arco .Juana Marı
´a Gonza
´lez-Mancebo
Received: 20 April 2017 / Accepted: 5 October 2017
ÓSpringer International Publishing AG 2017
Abstract Alpine ecosystems on islands are among
the most isolated on Earth, leading to very high rates of
endemism. Endemic species on oceanic islands are
particularly vulnerable to invasive herbivores. In the
alpine zone of Tenerife, which harbors a unique
endemic flora, the dominance pattern of the two most
dominant species in our days (Spartocytisus supranu-
bius and Pterocephalus lasiospermus) has shifted in
the last few decades, which may be a result of
increasing rabbit pressure. In this study we explore
how rabbits affect the population structure, soil
nutrient composition and regeneration of our two
target endemics within Teide National Park. For this
purpose, we established 90 plots at 30 locations.
Within 13 locations we sampled permanent exclosure
plots that were established between 7 and 12 years
before sampling, applying three treatments (full
herbivory, rabbit herbivory and no herbivory). At
one site we collected 80 soil samples to evaluate
changes in soil chemistry and plant growth using a
greenhouse experiment. Our results show that rabbits
have a negative effect on the population structure of S.
supranubius, while the contrary occurs with P.
lasiospermus. Rabbit presence alters soil chemistry
leading to a decline in nitrogen, which affects growth
in both species. The presence of rabbits leads to a
dominance shift in these two keystone endemic
species, altering dominance patterns in the summit
scrub of Tenerife. The decline of S. supranubius could
represent the example of many endemic species of this
system. Thus, we call for an immediate control of
rabbit population (\0.5 rabbits/ha) to protect this
unique alpine endemic flora.
Keywords Conservation Density-damage
relationship El Teide National Park Exclosure
experiment Oryctolagus cuniculus Vegetation
dynamic
Electronic supplementary material The online version of
this article (doi:10.1007/s10530-017-1576-0) contains supple-
mentary material, which is available to authorized users.
J. Cubas (&)R. Herna
´ndez-Herna
´ndez
M. J. del Arco J. M. Gonza
´lez-Mancebo
Plant Conservation and Biogeography Research Group,
Departamento de Bota
´nica, Ecologı
´a y Fisiologı
´a Vegetal,
Universidad de La Laguna, Avda. Francisco Sa
´nchez s/n,
38206 La Laguna, Tenerife, Islas Canarias, Spain
e-mail: jcubasdi@ull.edu.es
J. L. Martı
´n-Esquivel M. Marrero-Go
´mez
Parque Nacional del Teide, C/Sixto Perera Gonza
´lez 25,
38300 La Orotava, Tenerife, Islas Canarias, Spain
M. Nogales M. Lo
´pez-Darias
Island Ecology and Evolution Research Group (IPNA-
CSIC), Avda. Francisco Sa
´nchez 3, 38206 La Laguna,
Tenerife, Islas Canarias, Spain
S. D. H. Irl
Department of Biogeography, Bayreuth Center of
Ecology and Environmental Research (BayCEER),
University of Bayreuth, Bayreuth, Germany
123
Biol Invasions
DOI 10.1007/s10530-017-1576-0
Introduction
Alpine ecosystems are among the most isolated
systems on Earth in both continental (e.g. Chala
et al. 2017) and island environments (Steinbauer et al.
2012,2013). Alpine ecosystems constitute islands
within islands generating high degrees of endemism,
but at the same time being the most ephemeral
ecosystems on oceanic islands (Ferna
´ndez-Palacios
et al. 2014). Extinction risks are high in alpine
ecosystems on islands due to small range sizes of
endemics (Martı
´n2009; Irl et al. 2017), small popu-
lation sizes (e.g. Pe
´rez et al. 2015) and low genetic
diversity (Steinbauer et al. 2016), therefore their
protection is of high importance.
Endemics on oceanic islands evolved in the absence
of most of invasive mammalian herbivores (Nogales
et al. 2006), resulting in a particularly high vulnera-
bility to introduced herbivores (Bowen and van Vuren
1997). For example, in the summit area of the island of
La Palma endemic plants that lack natural defenses
against rabbit browsing are being replaced by a single
species Adenocarpus viscosus that contains a natural
alkaloid herbivore deterrent (adenocarpine; Irl et al.
2012). In fact, invasive mammals are widely accepted
as one of the leading causes of biodiversity loss
(Didham et al. 2005; Vitousek et al. 1997), especially
on islands (Simberloff et al. 2013; Blackburn et al.
2004). On oceanic islands, these impacts can reach
from species extinctions (Blackburn et al. 2004)to
more complex outcomes such as a switch from
competition to predation-dominated systems (Roemer
et al. 2002), and in extreme cases to a ‘meltdown’ of
ecosystems (see Simberloff and van Holle 1999). Due
to the high degree of endemism in high elevation
systems and their restricted distributions, high eleva-
tion endemics are particularly threatened by intro-
duced herbivores (Irl et al. 2012; Seguı
´et al. 2017).
The European rabbit Oryctolagus cuniculus is
among the 100 most invasive species (Lowe et al.
2004). It is native to southern Europe and northern
Africa, and was successfully introduced to all conti-
nents, except Antarctica and Asia (Smith and Boyer
2008). It has been effectively introduced to more than
800 islands worldwide, making it one of the most
widely distributed animal species on Earth (Flux and
Fullagar 1992). Rabbits are considered ‘ecosystem
engineers’ because their activities produce remarkable
ecosystem-level effects, including changes in soil
structure and composition (Eldridge and Myers 2001;
Willott et al. 2000) but also modifications in richness
and diversity of plant species through selective
browsing (Olofsson et al. 2007). In addition, they
may also cause important disruptions to insular seed
dispersal systems (Nogales et al. 1995,2005; Traveset
and Richardson 2006). As a result, rabbits have had
devastating effects on insular ecosystems worldwide
(Courchamp et al. 2003).
The Canary Islands are part of the Mediterranean
global biodiversity hot-spot, mainly due to their high
share of endemics (Ferna
´ndez-Palacios and Whittaker
2008). Rabbit browsing has likely transformed most of
ecosystems on the Canary Islands. In fact, many rare
or threatened plant species are now confined to areas
that rabbits and other introduced grazers cannot easily
access (Marrero-Go
´mez et al. 2007), possibly affect-
ing island-wide diversity patterns (Irl et al. 2015). The
alpine zone of Tenerife harbors a unique set of
exclusive alpine endemics (37 species) with 56%
being single-island endemics to this island. Usually,
alpine ecosystems exhibit extreme climatic conditions
that prevent the establishment of non-native species
(Irl et al. 2013; Alexander et al. 2016). However,
rabbit density in the alpine zone of Tenerife likely has
increased in the last decades (Martin et al. 2015), as a
result of increasing temperatures at high elevations
(Martı
´n et al. 2012). Indeed, during the last few
decades changes in the distribution of the dominant
plants species were reported from the alpine zone of
Tenerife (Rodrı
´guez-Delgado and Rosello
´2006). The
two dominating species of the summit scrub system
are Spartocytisus supranubius that is currently grad-
ually decreasing in abundance (Kyncl et al. 2006) and
Pterocephalus lasiospermus which has strongly
increased its distribution. In fact, it was reported from
only one location in 1946 (Sventenius 1946) with a
restricted distribution until at least 1977–79 (Rodrı
´-
guez-Delgado and Rosello
´2006). P. lasiospermus has
strongly increased its distribution, presently occurring
in 60% of the alpine zone of Tenerife (Canary Islands
Biodiversity Database).
In this study, we assess the effects of rabbit
herbivory on the population dynamics of S. supranu-
bius (Fabaceae) and P. lasiospermus (Caprifoliaceae)
in the alpine zone of Tenerife (Canary Islands).
Specifically, we assessed: (1) Population structure of
two endemic keystone species and proportion of rabbit
browsing damage for different size classes to identify
J. Cubas et al.
123
the density-damage relationship, (2) Differences in the
population structure of these two species in relation to
the presence or absence of herbivory, (3) Effects of
rabbit browsing on soil chemistry and the subsequent
effects on seedling growth rate of S. supranubius and
P. lasiospermus and, (4) Biotic and abiotic variables
drivers of rejuvenation.
Materials and methods
Study area and species
This study was conducted in the alpine zone of
Tenerife (Canary Islands), which is mainly located
inside El Teide National Park (Fig. 1a, b). Our study
was performed within an elevational range of
1862–3003 m a.s.l., mostly within the area of the
summit scrub vegetation (Spartocitysetum supranubii)
but occasionally also in the transition zone with the
mixed pine forest (Del Arco et al. 2006). With an area
of 18.990 ha, El Teide National Park reaches a
maximum elevation of 3718 m a.s.l. The climate is
mainly determined by elevation and orientation; mean
annual temperature and mean annual precipitation are
around 11.4 ±0.93 °C and 383.2 ±63.3 mm from
2000 to 3000 m, and around 10.8 ±0.9 °C and about
409 ±59.6 mm mm above this elevation to the
highest peak (3718 m). Mean minimum winter tem-
peratures range from 1.7 ±0.7 °C (2000–3000 m) to
0.2 ±0.0 °C (above this elevation range) (Santana
and Martı
´n2013).
Spartocytisus supranubius (Fig. 2a) is an endemic
broom shrub of Tenerife and La Palma (Canary
Islands) (Acebes et al. 2010, Fig. 1c). This shrub can
reach a height of 3 m in optimal conditions and grows
from 1700 to 3000 m a.s.l. (Voggenreiter 1975).
Spartocytisus supranubius is a N-fixing legume
species of the Fabaceae family (Wheeler and Dickson,
1990). Pterocephalus lasiospermus (Caprifoliaceae,
Fig. 2b) is a shrub that can reach 1 m in height; it is
endemic to the high elevation areas of Tenerife
(Acebes et al. 2010; Fig. 1d). This plant has been
described to reach its ecological optimum between
1900 and 2200 m a.s.l. (Rodrı
´guez-Delgado and
Rosello
´2006) and has been considered a nitrophilous
species (Ko
¨hler et al. 2006). These species are the two
most abundant species of the high elevation ecosystem
of the island (Rodrı
´guez-Delgado and Rosello
´2006).
On the Canary Islands, rabbits were introduced
during the 15th and 16th century by the Castillian
conquerors (De Abreu Galindo 1977). European
rabbits are opportunistic and highly adaptable, which
explains their success as colonists (Delibes-Mateos
et al. 2008). Because of their wide distribution and
their potentially high population densities, rabbits
have pronounced effects on biological diversity and
ecosystem functioning (e.g. by using rocks and well-
developed soils for the construction of their borrows).
On the Canary Islands, so far specific studies on rabbit
productivity exist, but ecosystems with strongly
seasonal climates, like the summit scrub on Tenerife,
show sharply defined breeding seasons (Fraser 1988).
In some areas of New Zealand, with similar climate
conditions to the alpine zone of Tenerife, annual
productivity is around 23 juveniles per female (Fraser
1988), which is a factor promoting their rapid spread
of this species in the area.
Sampling method
We selected 30 sites (see Fig. 1) across the distribution
range of S. supranubius (Del Arco et al. 2006). At each
site we established a line transect of 220 m length and
20 m width. Along this transect, we selected three
20 920 m plots distributed at intervals of 80 m.
Mean annual precipitation and mean annual temper-
ature were taken from climate maps (period
1981–2010) for each site (Santana and Martin 2013)
and elevation was measured on site. All vegetation
sampling was done in spring 2014.
In a total of 13 of these 30 sites, three treatment
types of herbivore exclusion plots (20 920 m) were
established by the National Park service (7–12 years
ago): (1) Full herbivory: no exclusion of any of the
introduced mammalian herbivores, (2) Rabbit her-
bivory: exclusion of introduced large mammalian
herbivores (i.e. mouflons, Ovis orientalis, that has
around 200–300 individuals in the study area as
estimated by the administration of the El Teide
National Park), (3) No herbivory: total exclusion of
all mammalian herbivores (mouflons and rabbits). We
surveyed the treatments once in spring 2014.
Plant size of both species was measured by two
perpendicular diameters and maximum growth height.
We distinguished different size classes for the two
species; although the age of S. supranubius can be
estimated from their known development stage (see
Contrasting effects of invasive rabbits on endemic plants
123
Gough 2010). For S. supranubius we proposed a
combined rating considering size and plant vitality,
measured by the proportion of green branches on each
individual, classifying them into four main classes.
The first two corresponding to the growth phase (with
more than 70% of green branches), and the last two
belonging to the decay phase (less than 70% of green
branches). The first class represents the juvenile stage
where individuals reach a maximum height of 65 cm
and a diameter less than 100 cm, making them an easy
target for rabbit browsing (Gough 2010). The mature
stage included young cone-shaped individuals (from
70 to 100 cm height and from 100 to 300 cm diameter)
which had managed to grow beyond the lethal rabbit
browsing height and hemispherical-shaped individu-
als at their optimum growth, that have exceeded
300 cm in diameter. The senescent stage included
individuals that start their decay reflected by the low
proportion of green branches (50–69%) and showing
variable diameters. The fourth class (dead stage)
included all dead individuals counted in the plots.
With respect to P. lasiospermus, individuals with a
high proportion of dry branches were observed in all
plant sizes, since mortality can occur at any stage. For
that reason, we classified this species into four classes,
where the first three were based on the canopy
diameter. The juvenile stage corresponded to living
individuals with a diameter range of 1–20 cm, the
mature stage to individuals with a range of 21–100 cm
and the senescent stage those with a maximum
diameter of 101–300 cm including all larger plants,
usually with a high proportion of dry branches. The
last class (dead stage) were dead individuals, inde-
pendent of their diameter (1–300 cm).
Browsing damage for each species produced by
rabbits was recorded. Damage produced by rabbits is
Fig. 1 a Map of the Canary Islands showing the location of the
El Teide Nationa Park within Tenerife. bMap displaying the
location of our sample sites for the vegetation survey and the
exclosure experiment within the study area. cand dshow the
distribution of our two target species S. supranubius and P.
lasiospermus within our study area. The size of the circles is
proportional to the % cover of the respective species at that site
J. Cubas et al.
123
quite obvious, e.g. characteristic scissor-like cutting of
flower heads or twigs, gnawing of bark and browse-
lines on foliage 40–50 cm (Cooke and McPhee 2007).
Rabbit damage was identified as oblique chisel-like
cuts through stems and small branches (Mutze et al.
2016; Cooke et al. 2008). The clean 45°cut distin-
guished their bite marks from the more ragged
evidence left by mouflons that tear off vegetation.
However, we are aware that if freshly germinated
seedlings are selectively eaten while still very small,
damage may be completely overlooked.
Soil nutrient analyses and growth trial of S.
supranubius and P. lasiospermus
To assess how rabbit presences changes soil and
growth conditions for the two target species, we
collected soil samples under varying conditions of
rabbit presence and sowed seeds of the target species
under standard greenhouse growing conditions at the
University of La Laguna, Tenerife. To take soil
samples we chose the area with the highest rabbit
density (*7.9 rabbits/ha; 2232 m a.s.l., see site 4 in
Table S1 and S2). We chose this site because here both
target species were well represented (cover of S.
supranubius and P. lasiospermus under full herbivory
conditions 25 and 15%, respectively, and 20% in the
rabbit herbivory as well as 40% in the no herbivory
treatment for S. supranubius). At the same time this
site had enough bare ground soils to find samples
without vegetation influence. In this site, 80 soil
samples were collected to study the relationship
between plant growth and possible differences in
nutrients (organic matter, total nitrogen, nitrates and
potassium) attributable to rabbits. We used official
methods (MAPA 1994) for all nutrient analyses.
Furthermore, pH was tested in soils freshly suspended
in 25 ml of deionized water (1:2.5).
Soil samples were collected at 5 cm depth in
October (2015), in 3 groups: (1) presence of latrines
(i.e. soils under latrines) with a minimum distance to
the nearest of vegetation at least 10 m. Thereby
latrines are defined as sites with an agglomeration of
more than 200 pellets within a single patch, even
though latrines are often defined using lower values
(Mutze et al. 2014). (2) absence of latrines (with a
minimum distance of 10 m to the nearest latrine)
outside the exclosure and, (3) inside exclosure (i.e. a
fenced exclosure plot established by El Teide NP with
a total of 6 years of exclusion). A total of 4000 seeds
of P. lasiospermus and S. supranubius (2000 seeds per
species) were sown in homogeneous greenhouse
conditions using the three soil groups described above.
For each germinated plant, root and stem length were
measured 50 days after its germination. Of the
germinated seeds, we measured 394 individuals for
latrines, 484 individuals for no latrines and 116
individuals for inside exclosure for S. supranubius,
whereas we measured 247 individuals for latrines, 408
individuals for no latrines and 99 individuals inside
exclosure for P. lasiospermus.
Rabbit density
We established 24 square plots (1 m
2
) every 20 m
along the two 220 m transects (12 plots per transect)
that contained the vegetation plots. In each of these 24
plots rabbit droppings (a total of 720 square plots)
were counted and removed to be able to re-count them
two months later (Ferna
´ndez-de-Simo
´n et al. 2011).
Considering these previous data, rabbit density was
calculated following the equation proposed by Eber-
hardt and Van Etten (1956): D=d/rt, where dis the
mean number of recent droppings per square meter,
ris the mean number of droppings [rabbits/day =350
droppings as assessed for Mediterranean environ-
ments (Ferna
´ndez-de-Simo
´n et al. 2011), similar to
that found in other countries, Wood 1988] and tis the
number of days.
Data analyses
Mann–Whitney tests were performed to analyze the
differences in the percentages of plants with damage
for each species at every location (S. supranubius and
P. lasiospermus) and proportions of size classes of
both species. Size classes reached by each species
were correlated with the environmental variables
measured (mean annual temperature, annual precipi-
tation, elevation, slope, and rabbit density) using
Spearman correlations.
We performed a non-parametric Kruskal–Wallis
test using the kruskalmc() function in the R package
‘pgirmess’ to test for significant differences between
all size-classes (with the exception of dead individu-
als) of the two focus plant species (S. supranubius and
P. lasiospermus) both inside and outside the plots,
considering the treatments: (1) full herbivory, (2)
Contrasting effects of invasive rabbits on endemic plants
123
rabbit herbivory and, (3) no herbivory. Significant
groups are given if p\0.05. We also analyzed the
differences in the percentage of juveniles, mature and
senescent in the same way. The relationship between
abundance of regeneration measured by the juveniles
of each species, and rabbits/ha was explored using a
linear regression model. We used standard transfor-
mations to find the best-fit for our model (untrans-
formed, log, square root, quadratic, unimodal).
We assessed the relationship between the most
important biotic (rabbit density) and abiotic variable
(mean annual temperature, mean annual precipitation
and elevation) using linear regression models. As
above, a non-parametric Kruskal–Wallis test was
applied to analyze for significant differences between
the three soil types (i.e. presence/absence of latrines
and no herbivory plots) and with regard to the two
target species. The Kruskal–Wallis test is robust for
differences in sample size.
Results
Population structure of Spartocytisus supranubius
and Pterocephalus lasiospermus in the study area
and damage produced by rabbits
A total of 1138 individuals of S. supranubius and
10354 of P. lasiospermus were measured in 90 plots. A
clear significant difference in the proportion of plants
with damage produced by rabbits between both
species (96.02% in S. supranubius and 8.50% in P.
lasiospermus; Z =6.63: p\0.0001) was obtained.
The distribution of the individuals among the size
classes is shown in Fig. 3. The size-class distribution
of the two species showed the opposite trend. While P.
lasiospermus showed a typical structure of a popula-
tion in expansion (54% juveniles, 32% mature and 8%
senescent among the living individuals), the popula-
tion of S. supranubius decreased (2% juveniles, 32%
mature and 30% senescent), with the proportions of
these three groups differing significantly between the
juveniles of both species (juvenile Z=3,65;
p\0.01). In addition, for S. supranubius a high
proportion of the individuals was dead (36.64%),
compared to only 5.80% of P. lasiospermus
(Z=5.04; p\0.0001).
The correlations between environmental variables
and size classes for each species were significant for
temperature in mature and senescent individuals of P.
lasiospermus (rho =0.39 and rho =0.36, respec-
tively; p\0.05 and n =30 for both) and the dead
class of S. supranubius (rho =0.46; p\0.01,
n=30). Significant negative correlations with eleva-
tion were found for the classes mature, senescent and
dead individuals of P. lasiospermus (rho =-0.40,
p\0.05; rho =-0.48, p\0.001; rho =-0.41,
p\0.05, respectively, for all n =30) and positive
correlation were found for mature and dead individ-
uals of S. supranubius; (rho =0.67, p\0.001;
rho =0.38, p\0.05, respectively, for both n =30).
Significant negative correlations were found with
slope for P. lasiospermus with all size classes (all
p\0.05 and n =30) and dead S. supranubius
(rho =-0.47, p\0.01, n =30). No correlations
were found between the remaining abiotic variables
and rabbit density values for either species, when the
exclosure plots were not included.
Population structure of Spartocytisus supranubius
and Pterocephalus lasiospermus under treatments:
full herbivory, rabbit herbivory and no herbivory
A total of 471 individuals of S. supranubius and 7167
of P. lasiospermus in 39 plots (three treatments) were
measured (Table S3). For S. supranubius juveniles
significantly profited from herbivory exclusion
(Fig. 4a), whereas the picture is more complicated
for mature (Fig. 4b) and senescent individuals
(Fig. 4c). For P. lasiospermus no differences were
found between all three treatments in all age classes
(Fig. 4d–f), indicating that this species reacts indif-
ferently to herbivore presence.
A linear regression using all plots showed a
notable drop in the regeneration of S. supranubius
(Fig. 5a) with increasing rabbit density, even with less
than one rabbit per ha (R
2
=0.242; p\0.001). No
relationship was found for P. lasiospermus
(R
2
=0.01; p[0.05, Fig. 5b).
Biotic and abiotic drivers of rejuvenation
Univariate correlations between the number of juve-
niles for both species showed weak relationships with
biotic (rabbit density) and abiotic variables (mean
annual temperature, mean annual precipitation, eleva-
tion). For S. supranubius we found a positive corre-
lation with mean annual temperature (R
2
=0.18*).
J. Cubas et al.
123
For P. lasiospermus we found a positive correlation
with mean annual temperature (R
2
=0.14*) and a
negative correlation with elevation (R
2
=0.16*; see
Table 1).
Soil nutrient changes produced by rabbits
and growth rate of seedlings of Spartocytisus
supranubius and Pterocephalus lasiospermus
The results obtained in the soil nutrient analysis
showed significant effects of rabbit presence for all
three treatments (presence of latrines, absence of
latrines, inside the exclosure) with regard to nitrogen,
organic matter, nitrates and potassium (Fig. 6a–e).
With regard to the greenhouse experiment, the
percentage of germination obtained for the two target
species was 49.0% for S. supranubius and 36.1% for P.
lasiospermus. For both S. supranubius and P.
lasiospermus seedlings, we obtained significant dif-
ferences for both root and stem growth between the
three treatments (see Fig. 7a–d). The general trend
was that root and stem growth increased towards
higher soil fertility for S. supranubius, whereas for P.
lasiospermus this trend was not as pronounced.
Discussion
In this study, we show that introduced rabbits have
long-term contrasting effects on the two most abun-
dant plant species in the alpine zone of Tenerife. While
S. supranubius has a clear negative density-damage
relationship as a result of rabbit browsing, with
rejuvenation being virtually absent, P. lasiospermus
has increased its distribution and abundance despite
the presence of a non-native generalist herbivore.
Therefore, one species might be profiting from the
reduction of the other species, leading to a shift in
dominance within this community and possible
changes in ecosystem functioning. Differences in the
palatability of both species are likely responsible for
their antagonistic response to the rabbit effect. Rabbit
impact on soil nutrients represents a decline in
nitrogen content as a result of a reduction of the
N-fixing legume S. supranubius, which negatively
affects both species regeneration. At this stage, the
long-term consequences for this system are still not
discernible, but pre-emptive conservation action
seems advisable (e.g. rabbit control measures within
the national park limits or establishment of large-scale
exclosures which have proven effective against intro-
duced herbivores) (Fig. 2).
Population structure of Spartocytisus supranubius
and Pterocephalus lasiospermus and damage
produced by rabbits
The results indicate that the population of P.
lasiospermus is well structured (inverted J-shaped)
(Fig. 3b) with a clear rejuvenating pattern. In the past,
this has resulted in a massive expansion from one
single location in the 1940s (Sventenius 1946)toa
distribution occupying 60% of the summit area of the
island above 1800 m a.s.l (Canaries Biodiversity
Database). However, for S. supranubius—the most
emblematic shrub from the alpine zone of Tenerife—
an unstructured population reveals inhibited rejuve-
nation within this species and a clear density-damage
relationship (Mutze et al. 2016). Two major historical
events could explain the current population structure
Fig. 2 Two dominant species in El Teide National Park
(Author: M. del Arco)
Contrasting effects of invasive rabbits on endemic plants
123
of S. supranubius. The species was considered in
decline in the 1940s (Sventenius 1946), but the
establishment of El Teide National Park in 1954
prohibited the human use of S. supranubius (previ-
ously used as pasture, for firewood and bedding for
livestock). As a result of the establishment of the
National Park, goats (Capra hircus) were eradicated
within its limits, which lead to a dramatic reduction of
herbivore pressure (Rodrı
´guez-Delgado and Rosello
´
2006). These important conservation measures led to a
strong increase in the population of S. supranubius in
subsequent years with a notable expansion in later
decades, as demonstrated by the mapped distribution
of this species (Del Arco et al. 2006), and aerial
photographs (Kyncl et al. 2006). The declining trend
of S. supranubius seems to be relatively recent,
starting approximately in 1995 (Kyncl et al. 2006).
Judging from its current population structure and size
class distribution, this species’ status could change to
‘threatened’ or even ‘endangered’ within the next
30 years, since the estimated life-span of S. supranu-
bius is about 50–60 years (Gough 2010).
Our results indicate that rabbit browsing is a serious
threat to S. supranubius and possibly other endangered
endemics, thus supporting studies from the summit
scrub of the neighboring island of La Palma (Irl et al.
2012). Kyncl et al. (2006) pointed out that rabbits
might be responsible for the decline of S. supranubius.
Indeed, the differences obtained in the proportion of
individuals of both species with rabbit damage are
notable (nearly 100% for S. supranubius and only
around 20% for P. lasiospermus). Thus, the difference
in the palatability of these two species may be the most
important driver in explaining the substantial changes
in the alpine zone of the island.
Significant differences in rabbit impact were
detected between the juvenile classes (individuals
under 70 cm) of S. supranubius growing in the
Fig. 3 Distribution of size
classes for aS. supranubius
and bP. lasiospermus under
herbivore presence
conditions in the study area
J. Cubas et al.
123
exclosure plots. These differences may be attributed
only to rabbits; since plots with mouflon herbivory
showed similar results to those obtained in the full
herbivory plots (without exclosure). Indeed, Fabaceae
species are considered as high-quality food for rabbits
(Delibes-Mateos et al. 2008). On the other hand, no
significant differences where apparent in the popula-
tion structure of P. lasiospermus with regard to
herbivory presence. A reduction in the cover of S.
supranubius, a plant that can grow up to 3 m tall and
8 m in diameter (Gough 2010), might reduce disad-
vantages in light competition for P. lasiospermus with
a maximum height of only 1.70 and 3 m in diameter.
The O. cuniculus can be considered a generalist
herbivore, consuming more than 25 different species
in El Teide NP (Hemdorff 2013). Indeed, most native
and endemic plant species have not evolved under
herbivory pressure (Nogales et al. 2006), thus intro-
duced rabbit presence obviously produces substantial
damage to the vegetation in the alpine zone of Tenerife
and can have potentially dramatic effects on island
biodiversity (Garzo
´n-Machado et al. 2010; Irl et al.
2014). Lack of regeneration inevitably leads to
reduction of population sizes as old shrubs die without
being replaced by younger ones.
Rabbit presence seems to lead to a higher abun-
dance of mature S. supranubius individuals (Fig. 4b).
This, however, is likely an artifact of the selection for
suitable exclosure sites. The National Park adminis-
tration specifically establish exclosure in sites with a
low cover of S. supranubius in order for rejuvenation
to be possible at all.
Soil nutrient changes due to rabbits and growth rate
of Spartocytisus supranubius and Pterocephalus
lasiospermus seedlings
Our results reveal notable differences in soil pH and
nitrogen, nitrates, potassium and organic matter in the
exclosure plots compared to soils collected under
Fig. 4 Changes in number
of individuals of S.
supranubius (ac) and P.
lasiospermus (df) during
our exclosure experiment
using three treatments (full
herbivory, rabbit herbivory
and no herbivory). To
identify age-specific effects
within the population of
each species, we divided the
population into three age
classes (juvenile, mature,
senescent). Significant
groups are indicated with
lowercase letters (p\0.05)
Contrasting effects of invasive rabbits on endemic plants
123
latrines and without latrines outside the exclusion.
Rabbits have a negative effect on surface soils in the
studied site. This negative effect is known from other
areas (e.g. Parsons et al. 2016; Eldridge and Koen
2008; Eldridge et al. 2006; Willott et al. 2000), thus
our soil analysis supports more general findings.
Rabbits produce an impoverishment in total soil
nitrogen (correlated with the proportion of soil organic
material). Even below the latrines the proportion of
soil nitrogen is lower than in the exclosure samples.
The effects of rabbits on soil nitrogen content are
spatially variable, stimulating nitrogen cycling under
latrines and decelerating the nitrogen cycling outside
the exclosure in areas without latrines. This is
probably caused by the selective grazing on N-fixing
S. supranubius. Inside the exclosure plots we found a
43% increase in soil organic matter and 58% in total
soil nitrogen with respect to the soils outside the
exclosure. These values are comparable with those
obtained in other exclosure experiments in New
Zealand (61%) after 16 years of rabbit and sheep
exclusion (McIntosh and Allen 1998). Litter rich in
nitrogen is accumulated over time in the exclosure
plots, leading to a higher proportion of soil organic
matter and total soil nitrogen (Sirotnak and Huntly
2000; Bazely and Jefferies 1986).
Important changes in nutrient composition can
result in a significant change in biodiversity (Delibes-
Mateos et al. 2008), since different species often have
different nutrient requirements (e.g., Parsons et al.
2016). We expected differences in the stem and root
growth in the seedlings of both species (S. supranubius
and P. lasiospermus) in the soils situated under
latrines, since P. lasiospermus is considered a
nitrophilous species (Ko
¨hler et al. 2006). Our results
suggest that the changes produced by rabbits on the
soils are not responsible for the differential population
structure of both species. However, latrines represent
an extra source of nitrogen that may help the
expansion of Pterocephalus independent of Sparto-
cytisus. Stem growth of both species responded
positively to latrine presence, which suggests that
Fig. 5 Linear regression of both species for juvenile individ-
uals and rabbits density (rabbits/ha)
Table 1 Univariate correlations of the number of juveniles for S. supranubius and for P. lasiospermus
Variable S. supranubius number of juveniles P. lasiospermus log (number of juveniles)
R
2
Direction R
2
Direction
Mean annual temperature (°C) n.s. 0.14* ?
Mean annual precipitation (mm/a) 0.18* ?n.s.
Elevation (m) n.s. 0.16*
Rabbit Density (Ind./ha) n.s. n.s.
R
2
values result from a linear regression model. Asterisk indicate significance with p\0.05. Direction indicates if a correlation is
positive (?) or negative (-). Number of juveniles for P. lasiospermus was log-transformed to account for the large range of number
of individuals within this species
J. Cubas et al.
123
the difference in palatability seems to be the most
important factor determining the dissimilarity in
population structure of both species. We suggest that
future studies should target the palatability of endemic
species to generalist herbivores, to assess the potential
impact on endemic-dominated communities.
Biotic and abiotic drivers of rejuvenation
Biotic and abiotic variables only weakly influence
rejuvenation processes of both target species. Never-
theless, S. supranubius seems to be limited by water
availability, while P. lasiospermus is limited by
temperature. Indeed, Perera-Castro et al. (2017)
showed that P. lasiospermus is sensitive to freezing,
suffering initial damage at -7.6 °C and irreversible
damage at -9.97 °C, thus limiting its expansion
towards higher elevation. In the past decades temper-
ature has increased in the alpine zone of Tenerife,
especially minimum temperatures (Martı
´n et al. 2012).
This ongoing temperature increase might facilitate
future range expansion of the less palatable P.
lasiospermus.
Interestingly, rabbit density does not have an effect
on the rejuvenation of S. supranubius. This seems to
contradict our results from the exclosure experiment.
However, if looking at the data more closely we see
that throughout the entire study area rejuvenation of S.
Fig. 6 Analysis of soil chemistry (5 cm depht) for for soil
sampled from three treatment types (latrines, no latrines and
exclosure plots) at one site within El Teide National Park. Soil
analysis was done for anitrogen content, borganic matter
content, cnitrate content, dpotassium content and epH value.
Significant groups are indicated in lowercase letters (p\0.05)
Contrasting effects of invasive rabbits on endemic plants
123
supranubius is so strongly impeded by rabbit browsing
that virtually no rejuvenation exists. For S. supranu-
bius the maximum number of juveniles we found per
site was extremely low (n =4 individuals) and 70%
of the sampled sites did not show any rejuvenation at
all, while the maximum number for P. lasiospermus
was almost 1300 individuals per site. As shown for the
summit scrub of neighboring La Palma (Irl et al.
2012), this clearly indicates the negative effect that the
presence of rabbits has on the rejuvenation of S.
supranubius.
Concluding conservation remarks
Here, we present the first detailed study that demon-
strates that rabbit browsing is directly related to the
decreasing population of a keystone endemic plant
species, S. supranubius, preventing its regeneration
and rejuvenation in El Teide National Park. From a
conservation perspective, taking into account that
complete rabbit eradication on the whole island of
Tenerife is socially and technically very difficult, we
urgently advocate for decisive measures for the
Fig. 7 Growth response in
root and stem length of S.
supranubius (ab) and P.
lasiospermus (cd) to three
different soil treatments
(latrines, no latrines and
exclosure plots) for a
greenhouse growing
experiment. Significant
groups are shown in
lowercase letters (p\0.05)
J. Cubas et al.
123
control of rabbit density at least in El Teide National
Park to target densities of \0.5 rabbits/ha, if the
conservation goal is to preserve the S. supranubius-
dominated summit scrub (sensu Rocha et al. 2017).
Another, although quite costly option that could be
helpful in creating sanctuaries for endangered ende-
mics could be to establish more and bigger exclosures,
as they have proven effective against introduced
herbivores. Future research should target how ongoing
and future climate change, which will severely affect
high elevation ecosystems on islands (Expo
´sito et al.
2015; Harter et al. 2015), might shift distribution
ranges of introduced herbivores and thus change the
exposure of native and endemic plant species to
introduced herbivores.
Acknowledgements We thank Julio Leal Pe
´rez, Alexandra
Rodrı
´guez-Romero, Josue
´A
´lvarez and Vı
´ctor Bello-Rodrı
´guez
for their great assistance assembling the plots and quadrats, and
taking data in the field. Also Julien Piquet, Natalia Dı
´az Cristina
Jime
´nez Gomı
´s and Ministerio del Interior (army), for their help
in some part of the field work. We also thank the Ministerio de
Agricultura, Alimentation y Medio Ambiente (REF 1621/2015)
for the financial support and the service of El Teide National
Park provided use with all kind of facilities for development of
this study. Jonay Cubas holds a PhD studentship from La
Laguna University.
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Contrasting effects of invasive rabbits on endemic plants
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... The activity of this invasive species includes changes in the soil composition (Willott et al., 2000;Eldridge and Myers, 2001), the richness and diversity of plant species through selective browsing (Olofsson et al., 2007), and disruptions to insular seed dispersal systems (Nogales et al., 1995(Nogales et al., , 2005Traveset and Richardson, 2006). As a result, rabbits have been considered as 'ecosystem engineers' (Jones et al., 1994;Cubas et al., 2018). ...
... Marrero- Gómez et al., 2007), so the typically higher endemic richness in steep areas is likely a result of their inaccessibility. Recent studies have demonstrated the strong negative effect of rabbits on the Canarian pine forests and Canarian alpine ecosystem (Irl et al., 2012;Cubas et al., 2018), where they have a negative effect on the population structure of keystone species such as Spartocytisus supranubius, while other species have been favored (Cubas et al., 2018). Though rabbits are present in all the ecosystems of these islands, the higher browsing occurs on endemic species rather than on non-endemic species . ...
... Marrero- Gómez et al., 2007), so the typically higher endemic richness in steep areas is likely a result of their inaccessibility. Recent studies have demonstrated the strong negative effect of rabbits on the Canarian pine forests and Canarian alpine ecosystem (Irl et al., 2012;Cubas et al., 2018), where they have a negative effect on the population structure of keystone species such as Spartocytisus supranubius, while other species have been favored (Cubas et al., 2018). Though rabbits are present in all the ecosystems of these islands, the higher browsing occurs on endemic species rather than on non-endemic species . ...
Article
Disruptive effects have been described on the plants and ecosystems of oceanic islands due to the introduction of invasive herbivores. In the Canary Islands the European rabbit (Oryctolagus cuniculus L.) was introduced five centuries ago and currently is widespread in all ecosystems, although in the laurel forests it is very scarce. However, on Morello-Ericetum woodland mostly represented by disturbed laurel forest areas, rabbit density is higher. Here we analyzed the impact of rabbits on the Morello-Ericetum woodland using exclusion and control plots located in 11 sites in the Garajonay National Park (La Gomera Island). Rabbit browsing was assessed for 36 endemic species, 15 of them threatened, which were sowed in both control and exclusion plots. After three years of monitoring, our results show a significant negative effect on the establishment and seedling recruitment for 55% of the analyzed species, especially in summer when the rabbit density increases by nearly 30%. Also, plant growth (in 91% of the species) and flowering rate (36% of the species), were disrupted, which could cause a depletion of the seed bank. Among the five tree species included in the experiment, three were also significantly damaged, so rabbits could be even influencing canopy species, delaying forest recovery. The management of Morello-Ericetum woodland should be countered the effects produced by the rabbits on their tree composition, and to allow the development of an understory where endemic species recover their abundance.
... El objetivo era detectar qué especies podían estar experimentando un aumento debido a la eliminación de la predación de herbivoría (cuando se compraban resultados a lo largo de los años de zonas valladas con la zona de control) o a los cambios en el clima (cuando se comparaban los resultados a lo largo de los años solo en los vallados libres de la presión de herbivoría). Martín-Esquivel et al. (2020) evidenciaron un apreciable aumento en la cantidad de ejemplares de las especies más palatables dentro de los vallados de exclusión del sector frío del NE, sobre todo en Spartocytisus supranubius (la retama), cuyo reclutamiento se está viendo muy afectado por la presencia de herbívoros (Cubas et al. 2018). Sin embargo, la exclusión de los herbívoros no supuso un aumento significativo en la cantidad de retamas ni en su cobertura en el sector cálido del SW, y lo mismo ocurrió con otra leguminosa que es, de hecho, la segunda más abundante en el retamar, el codeso (Adenocarpus viscosus). ...
... La retama está sufriendo las consecuencias del calentamiento climático como se comprueba en los sectores más cálidos del parque, donde ni siquiera la exclusión de herbívoros permite su desarrollo, al menos en la forma que lo hace en los sectores fríos, donde la exclusión favorece una alta regeneración (Cubas et al. 2018) y un aumento explosivo en sus densidades Martín-Esquivel et al. (2020). ...
... Esta expansión es más notable si tenemos en cuenta que la especie era muy escasa a mediados del siglo pasado (Sventenius 1946). Entre sus atributos para ser considerada como un ganador se encuentran: su baja palatabilidad a los herbívoros (Cubas et al. 2017), su carácter termófilo (Perera-Castro et al. 2017, su alta capacidad de dispersión y su capacidad de aprovechar el aporte extra de nutrientes de las letrinas de los herbívoros (Cubas et al. 2018, de modo que la presencia de conejos podría estar favoreciendo su expansión. Si tenemos en cuenta que Oryctolagus cuniculus también se puede considerar un ganador del cambio climático (Bello-Rodríguez et al. 2020), estamos ante un ejemplo de asociación positiva entre una especie invasora beneficiada por el cambio climático (conejos) que, a su vez, beneficia a otra que también se está viendo favorecida por él (rosalillo). ...
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La vegetación de alta montaña de Tenerife está formada actualmente por un matorral ralo con retama (Spartocytisus supranubius) y rosalillo (Pterocephalus lasiospermum) como especies dominantes. Este ecosistema está sufriendo un calentamiento importante que está teniendo consecuencias en la estructura y composición de la vegetación. En efecto, mientras especies como la retama se encuentran en declive, otras como el rosalillo se expanden cada vez más. Al efecto de las temperaturas hay que unir el de la herbivoría, que en algunos casos se ve amplificado por las consecuencias del cambio climático, de modo que, igual que hay diferencias en la palatabiidad de las especies a los herbívoros, se pueden identificar especies a las que el cambio climático favorece (ganadores del cambio climático) y especies a las que el cambio climático perjudica (perdedores del cambio climático). Todo ello está modificando la vegetación de forma ostensible, con la aparición de comunidades vegetales cada vez más diferenciadas respecto a las definidas para este ecosistema.
... However, these were far from being its only problem, as in this ecosystem it also has to cope with several other biotic and abiotic stresses. In the decade 1980-1990, the favorable trend due to N.P. protection reversed and S. supranubius populations started to recede (Cubas et al., 2018;Ibarrola-Ulzurrun et al., 2019;Bello-Rodríguez et al., 2020). ...
... In recent decades, regeneration of S. supranubius populations has been compromised by introduced herbivores, mainly rabbits (Cubas et al., 2018). Although present in the N.P. since their introduction in the sixteenth century, larger populations of rabbits have been favored by the milder climatic conditions in the last few decades (Bello-Rodríguez et al., 2020). ...
... Spartocytisus supranubius, the dominant species in the Teide N.P. is currently experiencing a decrease in population (Cubas et al., 2018;Martín-Esquivel et al., 2020). In order to slow down this decline, periodic transplanting of juvenile individuals is a frequent strategy in Teide N.P. ...
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The Teide broom, Spartocytisus supranubius , is an endemism of the Canary Islands (Spain) and the dominant legume of the Tenerife high-mountain ecosystem in Teide National Park (N.P.). Biotic and abiotic stresses are causing a progressive deterioration and decline of the population of this keystone legume. Since its symbiosis with rhizobia is the main nitrogen (N) input into these soils, diminishing the biological nitrogen fixation could compromise the maintenance of this alpine ecosystem. Symbiotically efficient nitrogen-fixing rhizobia have been widely and successfully used as inoculants for agronomic purposes. However, only rarely has rhizobial inoculation been used for legume species conservation in natural ecosystems. In this study, we assessed three Bradyrhizobium sp. strains as inoculants for S. supranubius on seedlings grown in a greenhouse experiment and on juvenile individuals (2-years-old) transplanted on a field trial in the N.P. Plant growth as well as symbiotic and plant physiological parameters were measured to evaluate the effect of rhizobia inoculation. Our results show that broom plants responded positively to the inoculation both in the greenhouse and field trials. The SSUT18 inoculated plants had significantly higher number and weight of nodules, greater sizes (biovolume) and biomass and also showed the highest N which, being not significant in our experimental conditions, it still contributed to more N per planted hectare than control plants, which could be important for the ecosystem maintenance in these N-poor soils. Positive effects of inoculation were also detected on the plant survival rate and water content. The bradyrhizobial inoculation, by accelerating the plant growth can shorten the greenhouse period and by producing more robust juvenile plants, they could help them to cope better with stresses in its natural habitat. Therefore, inoculation with selected rhizobia is a successful strategy to be integrated into conservation campaigns for this threatened legume species.
... However, variations in rabbit density on islands have been poorly studied. Most studies concern rabbits' effects on endemic plant species richness and composition Donlan et al., 2002;Nogales et al., 2005), the recovery of vegetation after rabbit eradication (Hess & Jacobi, 2011) or using rabbit exclusion plots (e.g., Cubas et al., 2018;Garzón-Machado et al., 2010;Irl et al., 2012). However, ecological responses to rabbit abundance in different habitats are still little understood on oceanic islands. ...
... In each of these 24 permanent plots, we counted fresh pellets (avoiding latrines, where droppings are not randomly distributed). All faecal pellets were then removed, and plots were revisited in the next season to repeat the process (Cubas et al., 2018;Fernández-de-Simón et al., 2011a). Rabbit density (D) was calculated following the equation proposed by Eberhardt and Van Etten (1956): ...
... The higher densities of rabbits recorded here are higher than those in semi-arid Australia, where rabbits cause significant changes in the flora at densities of between 1 and 2 rabbits per hectare (Mutze et al., 2016). In the Canary Islands, densities even below one rabbit per hectare may be dangerous for the endemic flora in the poorest ecosystems (Cubas et al., 2018). ...
Article
The European rabbit (Oryctolagus cuniculus) is a key prey species in Mediterranean ecosystems. However, it is also considered a pest on many oceanic islands, even though its true abundance and ecological effects on different island habitats are poorly understood. We present data on rabbit abundance for the best-preserved habitats of the Canary Islands, Spain (National Parks), including ecosystems differing in climate, topography, plant species richness and composition. Three methods of assessing rabbit abundance from faecal pellet density are compared to ascertain the best method to compare highly distinct habitats. The Cleaning method was used during spring, summer, autumn and winter to check whether there were differences in pellet degradation among habitats that could prevent comparisons between them. Rabbit abundance is determined by complex interactions among abiotic and biotic factor. Despite differences in climate conditions, the results obtained for rabbit density with fast methods correlated well with the slow Cleaning method. The Circular method was the most useful to work with for extensive sampling in different habitats. The best models for explaining rabbit density for all habitat types combined included tree cover, abiotic and topographic and climatic variables. Thus, factors influencing rabbit density vary depending on habitat type with Macaronesian laurel forests being the ecosystem least likely to be invaded by rabbits. The present study highlights that rabbits reach damaging densities for plant conservation in most areas on the Canary Islands.
... Previous work has also reported that endemics are highly susceptible to introduced herbivorous mammals (e.g. rabbits, feral goats or deer; Bowen & Van Buren, 1997;Cubas et al., 2018Cubas et al., , 2019, and a recent meta-analysis found that non-endemic plant taxa native to islands were more heavily attacked by introduced mammals on islands than on mainland areas . Having said this, other studies have reported no differences or lower levels of herbivory on insular plants (e.g. ...
Article
Aim It is predicted that insular plant taxa have evolved reduced defences in response to lower herbivore pressure on islands. However, the few studies testing this hypothesis have addressed variation in individual defensive traits, without paying attention to patterns of correlated trait expression (i.e. defence syndromes). Location Balearic and Canary Islands. Taxon Ninety-one woody plant species. Methods We tested whether plant species with contrasting histories of insularity (namely, endemics, non-endemic natives and exotics) differed in their defensive syndromes using a suite of morphological, physical, and chemical traits putatively associated with herbivory. For this, we measured eight leaf traits of 42 endemic, 29 native non-endemic and 20 introduced species for which specimens were sourced from botanical gardens found in two archipelagos: the Balearic and Canary Islands. Results We conducted phylogenetic-controlled analyses which showed that, contrary to predictions, insular taxa (endemics and non-endemic natives) across both archipelagos were more defended (thicker, smaller leaves with less nutrients) than exotic species. There were no differences in chemical defence (phenolic compounds) between endemics, non-endemic natives and exotics. Finally, we also found different defence syndromes between archipelagos: whereas species from the Balearic Islands were more physically defended, on average, those from the Canary Islands had higher chemical defences. Main conclusions Overall, these results point to a defence syndrome based on low-nutrient and physically defended leaves characteristic of insular plant taxa that is indistinct for endemic and non-endemic taxa, relative to introduced species, as well as quantitative and qualitative differences in defences between archipelagos owing to changes in species composition and likely also to different histories of biotic or abiotic pressure.
... Nevertheless, in many forests, a clear recovery process occurs when the causes of disturbance end (Trejo and Dirzo, 2000;Whittaker and Fernández-Palacios, 2007), through a set of successional vegetation stages (Oliver and Larzon, 1996;Chazdon, 2008;Chanthorn et al., 2016). Regeneration involves a complex multivariable process that depends on climate conditions (Holl et al., 2000;Ssali et al., 2018), time since disturbance (Martin et al., 2016), landscape spatial configuration (Mitchell et al., 2013), availability of propagules and dispersers (Zobel et al., 1998;Duncan et al., 2009), and biotic plant-animal interactions such as pollination or herbivory (Holl et al., 2000;Ssali et al., 2018), the latter acting as a disruptive function in many island ecosystems by the impact of alien herbivorous Schweizer et al., 2016;Cubas et al., 2018). Although there have been studies on the influence of different forest drivers, frequently these refer to only some of the factors (Guariguata and Ostertag, 2001;Letcher and Chazdon, 2009;Martin et al., 2016). ...
Article
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Deforestation and forest fragmentation have serious negative consequences for biodiversity and species distribution, but many studies approach species distributions and speciation processes without taking in account the local history of human disturbances. Nevertheless, the complex recovery process after forest destruction is widely distributed around the world and takes place under a wide mosaic of biotic and abiotic factors that may be influencing the species distribution. In this study aerial pictures from 1951 and 2019 were used to assess forest recovery during about sixty years. We tested if the initial stage (forest completely destroyed or young growth forest in 1951) determines the successional process, evaluating the role of different spatial drivers (distance from remnant forest fragments and unfelled areas around each site) and mesoclimate conditions, by examining 40 disturbed sites and 18 old-growth forest sites distinguished in 1951 aerial photos. The final stage during this successional process was assessed using 2019 aerial photos, covering the same these sites. At each plot, plant species composition and forest structure were studied, which allowed us to obtain a maturity index. Our results reveal that the initial stage is not the only driver explaining forest structure and species composition at the end of the 60-year period analyzed. The role of each forest recovery driver varies depending on each stage. In the early successional stages, the slope aspect (exposure) was the most important factor, which is correlated with mesoclimatic conditions, followed by the distance from young-growth forest in 1951. However, in intermediate successional stages the cover of old-growth forest around each plot in 1951 was the main factor in the recovery. At the end of the study period (2019), the differences in species richness between young-growth and old-growth forest were not significant, although old-growth forests were characterized by high densities of endemics, threatened species and β-diversity, showing the species composition a strong dependence on forest structure. Our results reveal the important need to consider human disturbance history in forest research and how climate conditions and the lack of nearby remnants can negatively affect the forest recovery process, greatly increasing the time needed to return to old-growth laurel forest conditions, which requires specific management recommendations.
Chapter
Invasive herbivores represent one of the biggest conservation problems of the island floras. This problem, widespread throughout the Canary Islands, has been managed by the National Park since its creation, when cattle started to be removed. However, recent research highlights new management needs in the Park. Global warming is becoming a key factor that increases the invasive herbivore effects. Increasingly, we have new data showing the lack of knowledge about the original species composition of the flora of this vegetation belt. The studies show that effects of invasive herbivores (especially the European rabbit) are widespread in the area, which affects not only the plant populations, but also the soil nutrient composition and seed banks. This chapter shows the research advances in recent years, providing not only recent references but also includes some conclusions of studies to be published in the coming months. All this makes it possible to propose future management and research lines that contribute to improve the problem caused by invasive herbivores in the Teide National Park.
Chapter
El Parque Nacional del Teide alberga los principales núcleos poblacionales de cedro canario (Juniperus cedrus) en la isla de Tenerife. Los estudios científicos que aquí se recopilan han supuesto un importante avance en el conocimiento de esta especie y sientan la base para futuras investigaciones y actuaciones de gestión orientadas a la conservación y mejora de estas poblaciones. Distintas líneas de evidencia apuntan a una situación actual de fragilidad. Por un lado, la dispersión de semillas a larga distancia se ha visto mermada tras la desaparición de las parejas nidificantes de cuervo (Corvus corax) en el Parque, y actualmente depende en gran medida de la llegada invernal del mirlo capiblanco (Turdus torquatus), un ave que a su vez presenta problemas de conservación. Por otro lado, existe una marcada estructura genética local que evidencia la existencia de grupos de individuos emparentados con un nivel significativo de endogamia. Además, las condiciones ambientales a las que se ven sometidos los individuos relegados a zonas muy escarpadas tienen un efecto negativo en el potencial reproductivo. Pese a la protección que le confiere su presencia dentro de los límites del Parque, hoy en día el cedro sigue siendo una especie amenazada, especialmente por su incapacidad para resistir el fuego. Futuras investigaciones que permitan conocer la distribución original del cedro en la alta montaña y desvelar el potencial del mirlo capiblanco para conectar poblaciones distantes, permitirían llevar a cabo un reforzamiento más eficaz de las poblaciones que garantice su conservación a largo plazo.
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Lagomorphs show extensive seasonal variation in their reproduction. However, the factors causing this large variation have so far mostly been investigated intraspecifically and therefore provide only some exemplary comparisons of lagomorph reproductive seasonality. The present study applies both a categorical description (birth season categories 1-5) and a quantitative measure (birth season length in months) to summarize the degree of birth seasonality in the wild of 69 lagomorph species. Using a comparative approach, I tested the influence of 13 factors, comprising six habitat, five life history and two allometric variables on birth season length in lagomorphs. Leporids mainly show non-seasonal birthing patterns with high intraspecific variation. Their opportunistic breeding strategy with high reproductive output and their large distribution areas across wide latitude and elevation ranges might be the reasons for this finding. Ochotonids reproduce strictly seasonally , likely because they live at northern latitudes, are high-altitude specialists, and occur in limited distribution areas. The most important factors associated with variation in lagomorph birth seasonality are mid-latitude, mean annual temperature and precipitation of a species' geographical range and life history adaptations including fewer but larger litters in seasonal habitats. Birth seasons become shorter with increasing latitude, colder temperatures, and less precipitation, corresponding to the decreasing length of optimal environmental conditions. Leporid species with shorter breeding seasons force maternal resources into few large litters to maximise reproductive output while circumstances are favourable. Since allometric variables were only weakly associated with reproductive seasonality, life history adaptations and habitat characteristics determine birth seasonality in Lagomorpha.
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Aim: Rarity—an important measure for conservation biogeography—can vary over many orders of magnitude. However, it is unclear which regional-scale abiotic conditions drive processes affecting rarity of endemic species on islands. To support conservation efforts, we (1) assess the main abiotic drivers of endemic rarity, (2) determine how well existing protected areas (PAs) coincide with hotspots of endemic rarity and (3) introduce and evaluate a new hypervolume-based rarity estimator. Location: La Palma (Canary Islands). Methods: We recorded all present endemic vascular plant species in 1,212 plots covering the entire island. We calculated endemic rarity (corrected range-rarity richness for endemics) using a rarity estimation approach based on kernel density estimations (hypervolume approach). We performed a sensitivity analysis based on multiple linear regressions and relative importance estimations of environmental drivers to estimate the performance of the hypervolume-based rarity estimation compared to standard methods (occurrence frequency, convex hulls, alpha hulls). Results: Climate variables (mean annual temperature, climatic rarity, precipitation variability) best explained archipelago endemic (AE) and single-island endemic (SIE) rarity. Existing PAs covered the majority of AE and SIE rarity, especially national and natural parks as well as the Natura 2000 sites. In our study system, hypervolumes performed better than standard measures of range size. Main conclusion: Both AE and SIE rarity on La Palma show a clear spatial pattern, with hotspots of endemic rarity found at high elevations and in rare climates, presumably owing to geographical and climatic constraints and possibly anthropogenic pressure (e.g., land use, introduced herbivores, fire). Areas of high rarity estimates coincide with the distribution and extent of PAs on La Palma, especially since the recent addition of the Natura 2000 sites. The hypervolume approach is a promising tool to estimate species range sizes, and can be applied on all scales where point/plot data are available.
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The tropical alpine ecosystem in eastern Africa is highly fragmented among biological ‘sky islands’, where populations of frost-tolerant organisms are isolated from each other by a ‘sea’ of tropical lowlands. One-third of the species in the afroalpine flora are exclusively alpine, but the other species can to varying degrees extend into grasslands and open forests of lower vegetation belts. A long-debated question is whether colonization of the alpine zone of these mountains and subsequent intermountain gene flow entirely depend on long-distance dispersal across unsuitable habitats, or whether suitable habitats shifted far enough downslope under past colder climates to form bridges enabling gradual migration. Here we address this question using a classification tree model. We mapped the extent of the current alpine habitat and projected it to the last glacial maximum (LGM) climate to assess whether gradual migration was possible for exclusively alpine taxa during this glacial period, and thus potentially also during earlier Pleistocene glaciations. Next, we modelled landcover under current and LGM climates to assess whether grassland and open forests could have served as migration corridors for alpine taxa that today extend into lower vegetation belts. We estimated that the LGM treeline was about 1000 m lower and the alpine habitat was about eight times larger than that today. At the LGM, we found that most of the currently fragmented alpine habitat of the Ethiopian highlands was interconnected except across the Great Rift Valley, whereas the solitary mountains of East/Central Africa remained isolated for exclusively alpine species. However, for drought-tolerant alpine species that today extend below the treeline, gradual migration through habitat corridors may have been possible among mountains during the dry glacial periods, and possibly also under the current climate before agriculture transformed the low-lying landscapes.
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Ecosystems that provide environmental opportunities but are poor in species and functional richness generally support speciation as well as invasion processes. These processes are expected not to be equally effective along elevational gradients due to specific ecological, spatial, and anthropogenic filters, thus controlling the dispersal and establishment of species. Here, we investigate speciation and invasion processes along elevational gradients. We assess the vascular plant species richness as well as the number and percentage of endemic species and non‐native species systematically along three elevational gradients covering large parts of the climatic range of La Palma, Canary Islands. Species richness was negatively correlated with elevation, while the percentage of Canary endemic species showed a positive relationship. However, the percentage of Canary–Madeira endemics did not show a relationship with elevation. Non‐native species richness (indicating invasion) peaked at 500 m elevation and showed a consistent decline until about 1,200 m elevation. Above that limit, no non‐native species were present in the studied elevational gradients. Ecological, anthropogenic, and spatial filters control richness, diversification, and invasion with elevation. With increase in elevation, richness decreases due to species–area relationships. Ecological limitations of native ruderal species related to anthropogenic pressure are in line with the absence of non‐native species from high elevations indicating directional ecological filtering. Increase in ecological isolation with elevation drives diversification and thus increased percentages of Canary endemics. The best preserved eastern transect, including mature laurel forests, is an exception. The high percentage of Canary–Madeira endemics indicates the cloud forest's environmental uniqueness—and thus ecological isolation—beyond the Macaronesian islands.
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Summit areas of oceanic islands constitute some of the most isolated ecosystems on earth, highly vulnerable to climate change and introduced species. Within the unique high-elevation communities of Tenerife (Canary Islands), reproductive success and thus long-term survival of species may depend on environmental suitability as well as threat by introduced herbivores. By experimentally modifying the endemic and vulnerable species Viola cheiranthifolia along its entire altitudinal occurrence range, we studied plant performance, autofertility, pollen limitation and visitation rate and the interactive effect of grazing by non-native rabbits on them. We assessed the grazing effects by recording (1) the proportion of consumed plants and flowers along the gradient, (2) comparing fitness traits of herbivore-excluded plants along the gradient, and (3) comparing fitness traits, autofertility and pollen limitation between plants excluded from herbivores with unexcluded plants at the same locality. Our results showed that V. cheiranthifolia performance is mainly affected by inter-annual and microhabitat variability along the gradient, especially in the lowest edge. Despite the increasingly adverse environmental conditions, the plant showed no pollen limitation with elevation, which is attributed to the increase in autofertility levels (≥ 50% of reproductive output) and decrease in competition for pollinators at higher elevations. Plant fitness is, however, extremely reduced owing to the presence of non-native rabbits in the area (consuming more than 75% of the individuals in some localities), which in turn change plant trait-environment interactions along the gradient. Taken together, these findings indicate that the elevational variation found on plant performance results from the combined action of non-native rabbits with the microhabitat variability, exerting intricate ecological influences that threaten the survival of this violet species.
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Recent years have seen a surge of interest in understanding patterns and processes of plant invasions into mountains. Here, we synthesise current knowledge about the spread of non-native plants along elevation gradients, emphasising the current status and impacts that these species have in alpine ecosystems. Globally, invasions along elevation gradients are influenced by propagule availability, environmental constraints on population growth, evolutionary change and biotic interactions. The highest elevations are so far relatively free from non-native plants. Nonetheless, in total nearly 200 non-native plant species have been recorded from alpine environments around the world. However, we identified only three species as specifically cold-adapted, with the overwhelming majority having their centres of distribution under warmer environments, and few have substantial impacts on native communities. A combination of low propagule availability and low invasibility likely explain why alpine environments host few non-native plants relative to lowland ecosystems. However, experiences in some areas demonstrate that alpine ecosystems are not inherently resistant to invasions. Furthermore, they will face increasing pressure from the introduction of pre-adapted species, climate change, and the range expansion of native species, which are already causing concern in some areas. Nonetheless, because they are still relatively free from non-native plants, preventative action could be an effective way to limit future impacts of invasions in alpine environments.
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Foraging by herbivores alters individual plants and vegetation communities directly, and engineering behaviors such as bioturbation (digging and turning soil) and biodeposition (deposition of feces and urine) can affect soils and physical properties that indirectly influence vegetation and other organisms. Patchy environments often concentrate the activities of animals, potentially increasing the magnitude of their impacts on the vegetative community over time. To evaluate the potential for herbivorous engineers to enhance existing heterogeneity, we quantified the direct and indirect effects of a burrowing herbivore, the pygmy rabbit (Brachylagus idahoensis), on soil and vegetation in the sagebrush steppe ecosystem of the western United States, and we evaluated whether the effects were related to duration of occupancy by rabbits. Mounded microtopography (i.e., mima mounds) creates distinct resource islands with relatively tall and dense sagebrush shrubs where pygmy rabbits concentrate burrowing and foraging activities. We quantified soil and vegetation characteristics on mima mounds occupied by rabbits for 1-12 yr and on unoccupied mounds. We expected that browsing would negatively influence slow growing sagebrush shrubs, but that digging and biodeposition would enhance soil nutrients and water infiltration. In addition, we hypothesized that the net effect on sagebrush reproduction would be positive because indirect effects on soil would enhance seed production by mature sagebrush and seedling growth, and because bioturbation would increase seed retention and germination. Pygmy rabbit occupancy had significant cumulative effects on both soil and vegetation properties on occupied mima mounds. Over time, browsing reduced sagebrush canopy cover and percent of individual shrubs that were alive. Soil properties were less influenced by the duration of occupancy of mima mounds than by the localized spatial influence of burrowing; elevated nitrogen levels were associated with burrow entrances. Two measures of sagebrush reproduction (seedling recruitment and inflorescence biomass) increased with duration of burrow occupancy, suggesting that over longer time frames pygmy rabbits enhanced reproduction and recruitment of sagebrush shrubs. Our data demonstrate multiple pathways by which an herbivorous engineer can influence habitat heterogeneity, and they suggest that although pygmy rabbits are inconspicuous on the landscape, the species might play an important role in maintaining and augmenting heterogeneity in the sagebrush steppe.
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A comparison between maximum quantum yield of PSII photochemistry (Fv/Fm) and chlorophyll fluorescence decrease ratio (Rfd) for low and high temperature resistance was assessed in a seasonal study of the acclimation in Pterocephalus lasiospermus. Analyzing the regression adjustment of both parameters and the lethal temperatures (LT50), Rfd resulted in being a more sensitive indicator for low and high temperature treatments, since the thermic resistance estimated with Rfd parameter was never higher than those estimated with Fv/Fm. Furthermore, the use of Fv/Fm led to an overestimation of the acclimation phenomena, with 6ºC of a maximum difference between both parameters. Using Rfd as the indicator parameter, P. lasiospermus acclimated to low temperatures but it kept on being a sensitive species (the lowest LT50 values only achieved–9.9 ± 0.3ºC). However, no heat acclimation was observed (LT50 around 43.5ºC). Thus, according to Rfd evaluation of the thermic threshold, this species could be in risk of damage at low temperatures in this alpine ecosystem.
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Herbivores can directly increase nitrogen mobility by increasing the quality of organic matter entering the decomposition cycle, but they also may decrease nitrogen mobility by decreasing the biomass of high-nitrogen species in the plane community. We assessed effects of voles (Microtus) on nitrogen dynamics using exclosures in two riparian meadows (Crystal Bench and Blacktail Deer Creek) in Yellowstone National Park (USA). At both sites, the quantity of plant litter was decreased by herbivory following a vole population peak in 1992. At Crystal Bench, removal of voles caused a decrease in the nitrogen concentration and an increase in the C:N ratio of plant litter over the four years of the study. The higher quality litter produced in the presence of voles at Crystal resulted in a larger pool of potentially mineralizable nitrogen in soil from control plots relative to soils from plots that had not been accessible to voles. At Crystal, vole removal did not cause a change in plant community composition. However, at Blacktail, after several years of vole exclusion, legumes became more common in exclosures than in control plots that were accessible to voles. Selective herbivory on high-nitrogen legumes kept the litter quality outside exclosures low, whereas higher legume biomass caused a decrease in C:N ratio of plant litter inside exclosures. The removal of voles at Blacktail caused a 15% increase in the fraction of the soil nitrogen that was rapidly mineralizable. Our results show that voles increased nitrogen mobility, especially during and after population peaks. However, that increase was offset by decreases in nitrogen mineralization over longer periods when voles caused a decrease in high-quality plant litter produced by preferred forage plants, especially legumes: Thus, both the mechanisms by which voles affected nitrogen dynamics and the net effects of voles varied over time and space. The balance of direct and indirect effects may provide a general mechanistic explanation of whether herbivores increase or decrease the rate of nitrogen cycling.
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Introduced European rabbits, Oryctolagus cuniculus, can severely damage Australian native vegetation but the problem is difficult to quantify because simple methods to estimate rabbit impacts are lacking. Management decision-making is often uncertain because of unknown relationships between rabbit density and damage. We tested simple quantitative sampling methods using belt transects to detect differences in critical characteristics of perennial vegetation communities affected by rabbit browsing: damage to individual juvenile shrubs and trees, and loss of recruitment cohorts. Rabbit density and relative abundance of larger herbivores were estimated from dung pellet density. The prevalence of identifiable rabbit browse on juvenile plants increased with increasing rabbit density and was higher for plant species considered by previous authors to be highly palatable than for moderately palatable or unpalatable species. At densities of ≥0.5rabbitsha-1, highly palatable plant species were severely damaged as juveniles and cohorts in 0.3-1.0m height classes and 5-20mm basal diameter classes were missing. Similar damage became apparent in moderately palatable species at 2rabbitsha-1 but was rarely seen in unpalatable species. Within species, size cohort evenness was inversely related to the proportion of surviving juveniles with identifiable rabbit damage. The effect of rabbits on native vegetation condition can be recorded in a simple manner suitable for identifying density-damage relationships and changes in vegetation condition over time. It is particularly useful in setting target densities below which rabbits must be managed to maintain natural plant recruitment and ecosystem function in conservation reserves and pastoral grazing properties of southern Australia.