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As the need to better understand the ecology of hotspots of endemism intensifies, the insurance hypothesis is drawing increasing attention from policy-makers and scenario-planners. The hypothesis states that biodiversity increases ecosystem stability. When species numbers fluctuate, there is potential for further perturbation, loss of function and increased opportunity for invasive species to fill vacated niches. Southern Africa is predicted to be disproportionately impacted by global change, and high altitude systems as foci of endemism are particularly vulnerable to warming. Using ants, a group key to ecosystem function, we assess effects of temperature, season, aspect, vegetation and soil conditions on montane ant species richness, stability of ant community composition, and stability of ant species richness across an altitude gradient. Over six consecutive years of bi-annual sampling, we gathered one of the largest standardized data sets to date. We showed for the first time that stability of ant species richness decreases with increasing altitude, whilst compositional similarity of ant communities is higher with increasing altitude. Findings reveal more similar, species-poor, less stable ant communities at high altitude at the same sites over time.
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Original Research Article
Stability of Afromontane ant diversity decreases across an
elevation gradient
Grant S. Joseph
a
,
b
,
*
, Mulalo M. Muluvhahothe
a
, Colleen L. Seymour
b
,
c
,
Thinandavha C. Munyai
a
,
d
, Tom R. Bishop
e
,
f
, Stefan H. Foord
a
a
SARChI-Chair on Biodiversity Value and Change, Department of Zoology, School of Mathematical and Natural Science, University of
Venda, Private Bag X5050, Thohoyandou, 0950, South Africa
b
Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, Department of Biological Sciences, University of Cape
Town, Rondebosch, 7701, South Africa
c
South African National Biodiversity Institute, Kirstenbosch Research Centre, Private Bag X7, Claremont, 7735, South Africa
d
School of Life Science, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Private Bag X01, Scottsville, 3209,
South Africa
e
Department of Earth, Ocean and Ecological Sciences, University of Liverpool, Liverpool, UK
f
Department of Zoology &Entomology, University of Pretoria, Pretoria, 0002, South Africa
article info
Article history:
Received 24 November 2018
Received in revised form 11 March 2019
Accepted 11 March 2019
Keywords:
Ant compositional similarity
Ant species richness
Climate change
Ecological community thresholds
Altitude gradient
Insurance hypothesis
abstract
As the need to better understand the ecology of hotspots of endemism intensies, the
insurance hypothesis is drawing increasing attention from policy-makers and scenario-
planners. The hypothesis states that biodiversity increases ecosystem stability. When
species numbers uctuate, there is potential for further perturbation, loss of function and
increased opportunity for invasive species to ll vacated niches. Southern Africa is pre-
dicted to be disproportionately impacted by global change, and high altitude systems as
foci of endemism are particularly vulnerable to warming. Using ants, a group key to
ecosystem function, we assess effects of temperature, season, aspect, vegetation and soil
conditions on montane ant species richness, stability of ant community composition, and
stability of ant species richness across an altitude gradient. Over six consecutive years of
bi-annual sampling, we gathered one of the largest standardized data sets to date. We
showed for the rst time that stability of ant species richness decreases with increasing
altitude, whilst compositional similarity of ant communities is higher with increasing
altitude. Findings reveal more similar, species-poor, less stable ant communities at high
altitude at the same sites over time.
©2019 Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
Global anthropogenic change is shifting distributions of vertebrate and invertebrate assemblages at a range of scales, and
the nal outcome is likely to be deleterious to biodiversity and ecosystem function (Joseph et al., 2018a., Davis and Vincent,
*Corresponding author. University Of Cape Town, FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, Cape Town, 7701, South
Africa.
E-mail addresses: karoogrant@gmail.com (G.S. Joseph), mulalomary@gmail.com (M.M. Muluvhahothe), C.Seymour@sanbi.org.za (C.L. Seymour), caswell.
munyai@gmail.com (T.C. Munyai), thomasrhys.bishop@gmail.com (T.R. Bishop), Stefan.Foord@univen.ac.za (S.H. Foord).
Contents lists available at ScienceDirect
Global Ecology and Conservation
journal homepage: http://www.elsevier.com/locate/gecco
https://doi.org/10.1016/j.gecco.2019.e00596
2351-9894/©2019 Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/
4.0/).
Global Ecology and Conservation 17 (2019) e00596
2017;Duffy et al., 2015;García-Palacios et al., 2018). Ecological stability is therefore important, and has become a focal topic in
ecological circles, as the impacts of global change to ecosystem stability through altered species richness and composition
patterns become better appreciated (García-Palacios et al., 2018;Hautier et al., 2015).
The insurance hypothesis postulates that species richness can increase ecosystem stability. The hypothesis has received
wide research attention (Doak et al., 1998;García-Palacios et al., 2018;Isbell et al., 2009;Lehman and Tilman, 2000;Loreau
et al., 2001;Pennekamp et al., 2018;Yachi and Loreau, 1999), and is emerging as a key issue politically, as impacts to
biodiversity threaten ecosystem services and mutualistic networks (e.g., Intergovernmental Science-Policy Platform on
Biodiversity and Ecosystem Services; Isbell et al., 2017;Simba et al., 2018). Stability, the inverse of variation over time, has long
been recognised as a fundamental ecosystem property that offers insights into biodiversity and ecosystem processes (Doak
et al., 1998). The insurance hypothesis posits that species respond to environmental perturbations in different ways, uc-
tuating in their abundance and contribution to ecosystem functioning under different conditions. In a system with high
species richness, these different species responses are more likely to complement each other, conferring overall stability, than
in a low species richness system. Species richness thus acts as a buffer against environmental perturbation (García-Palacios
et al., 2018;Loreau et al., 2001;Tilman, 1999).
Mountain-inhabiting ectotherm assemblages across elevational gradients can be particularity vulnerable (García-Robledo
et al., 2016), as the exibility of adaptive traits that inuence organism tness and ecosystem function become tested by the
rapid changes in thermal regimes that are predicted to occur in these regions (Modiba et al., 2017;Petchey and Gaston, 2006;
Salas-Lopez et al., 2017). Mountain-dwelling communities need to adapt to specic temperature niches, microhabitats and
soils. Furthermore, landscape heterogeneity means that montane assemblages can be effectively isolated and surrounded by
an ecological matrix to which they are not well adapted (Bishop et al., 2017;Suggitt et al., 2011). The modication of cooler
microclimates (which can enhance ectotherm persistence; Duffy et al., 2015;G.S.Joseph et al., 2016), and microhabitat loss
(e.g. loss of shade provided by vegetation through herbivory; G. Joseph et al., 2018b;Minor et al., 2016;Suggitt et al., 2011) are
anticipated to impact community composition, species richness, and increase the likelihood of localised extinctions (Stocker
et al., 2013;Thomas et al., 2004).
As anthropogenic impacts to ecological systems intensify, identifying patterns and conditions that affect biodiversity over
time become increasingly relevant. Research in arid systems has revealed that climate can modulate the relationships be-
tween diversity and ecosystem stability, leading to climate dependency of the biodiversityeecosystem stability relationship,
and that species richness can play an important stabilizing role with increasing aridity (García-Palacios et al., 2018;
Pennekamp et al., 2018). Despite ample evidence of the biodiversity-stability relationship (García-Palacios et al., 2018;Loreau
et al., 2001;Pennekamp et al., 2018), and that global change is impacting ecosystem stability (Donohue et al., 2016), predictive
modelling efforts addressing ecosystem stability at regional and global scales require studies conducted over protracted
timescales (García-Palacios et al., 2018). For the most part, such studies do not exist.
Insects, amongst the most species-rich and functionally important of animals, have evolved specic traits and thermal
tolerances to suit their habitat, impacting distribution, tness and ultimately functioning of ecosystems dependent on their
services (Wilson, 1987). Amongst insects, ants (Hymenoptera: Formicidae) are critical to ecosystem processes at a range of
scales, and are indicators of environmental change (Tiede et al., 2017). Recent studies highlight that ant species richness can
decrease linearly, or with mid-elevational peaks, as altitude increases and temperatures decrease (Bishop et al., 2014;Yusah
et al., 2012). Despite the central role of ants to ecological systems, and the vulnerability of isolated montane communities to
environmental perturbation, few studies examine temporal trends in biodiversity, and to our knowledge no study has to date
addressed the stability of invertebrate diversity over time across an elevation gradient.
As maintaining species number can buffer and modulate an ecosystem's response to change, preventing niches from
becoming available to invasive species and restructuring communities (García-Palacios et al., 2018;Yachi and Loreau, 1999),
we test the implications of an altitudinal gradient for stability of ant species richness (stability
asr
) and ant community
composition over time. We sampled ant communities in an Afrotropical mountain range recognised for its high endemism of
several taxa, the Soutpansberg, in southern Africa. The Vhembe biosphere planning group has recently proposed that all areas
in the Soutpansberg be proclaimed core conservation areas, prompting the South African government's Department of
Environmental Affairs, and the South African National Spatial Biodiversity Assessment (NSBA) to include the Soutpansberg
complex as a national priority area for conservation action (Depatment of Environmetal Affairs, 2018). We used an extensive
dataset collected biannually for six consecutive years, making it amongst the largest standardized, spatio-temporal inver-
tebrate community datasets in existence.
To date, research conrms the negative relationship between ant species richness and increasing altitude (Bishop et al.,
2017;Munyai and Foord, 2012;Szewczyk and McCain, 2016). Given that the presence of more species enhances stability,
we predicted decreased stability
asr
at altitude. In the knowledge that endemic, altitude-adapted taxa often occur at higher
elevations, and that this holds for the Soutpansberg (Munyai and Foord, 2015), we expected increasing altitude to impact
community similarity through time, with community composition being more variable between years. As ant diversity de-
creases with altitude, we anticipated that species-poor communities at high altitude might be dominated by a small number
of similar species able to survive the environmental ltering of high altitude. To test these hypotheses, we asked:
(1) does species richness of ants vary with altitude, aspect and with variables of habitat structure and soils?
(2) does stability
asr
change across altitude?
G.S. Joseph et al. / Global Ecology and Conservation 17 (2019) e005962
(3) is similarity of composition of ant communities constant across an altitudinal gradient?
(4) are there elevational thresholds that inuence occurrence of ant taxa across an altitudinal gradient?
2. Methods
2.1. Study site
Ants were sampled in a recognised southern African centre of endemism (Van Wyk and Smith, 2001), the Soutpansberg
Mountains within the Vhembe Biosphere Reserve. We sampled along an elevational transect beginning at 23
02
0
16.91
00
S,
29
26
0
34.22
00
E, running in a north-south direction, starting at 800 m above sea level (a.s.l.) on the southern aspect, and
climbing to 1700 m a.s.l., before descending to 800 m a.s.l. on the northern aspect. The transect is characterised by sandstone,
erosion-resistant quartzite, conglomerate, basalt, and shale rocks (Mostert et al., 2008), experiencing summer rainfall, dry
winters and mean annual precipitation of about 450 mm (Mucina and Rutherford, 2006).
2.2. Ant sampling
Epigaeic ant sampling took place biannually for 6 years, from 2009 to 2015. Given that sampling can vary even at the same
time of year through uctuating environmental variables (e.g. rainfall events, res, temperature variability), we mitigated
against short-term temporal variation in foraging activity by (1) sampling at the same time each year, during January (wet
season) and September (dry season), (2) ensuring that sampling was not coupled to rainfall events, (3) only sampling on sites
not impacted by re, (4) sampling during 5 day periods in which full sun (no cloud) was present for an averageof over 6 h per
day. Sampling was done at eleven sites, spaced 200 vertical metres apart, for each elevational band. Each site contained four
replicates, spaced at least 300 horizontal metres apart to avoid pseudo-replication (McKillup, 2011). At each replicate, ten
pitfall traps (each ø 62 mm) were laid out in a grid composed of two parallel lines (2 5) with 10 m spacing between traps,
following Munyai and Foord (2012) and Bishop et al. (2014). Traps contained a 50% solution of propylene glycol and were left
open for ve days during each survey. Ants were identied to morphospecies or species when possible.
2.3. Environmental variables
Temperature was recorded in two replicates at each site. Within each replicate, one Thermocron iButton (Semiconductor
Corporation, Dallas/Maxin/Texas) was buried 1 cm below the soil to record temperature at hourly intervals. Mean, minimum
and maximum temperatures were calculated for wet and dry season for each year at each elevational band.
Vertical and horizontal habitats were quantied. During each survey, a 1 m
2
grid was placed over each pitfall trap, and
imaged to establish horizontal habitat structure by estimating percentage area covered by bare ground, vegetation, rock and
leaf litter. For vertical structure, a 1.5 m measuring rod was placed at four corners of the grid, 1.5 m from the pitfall trap. The
number of vegetation contacts on the rod was recorded along 25 cm intervals (0e25 cm, 25e50 cm, 50e75 cm, 75e100 cm,
100 e125 cm, 125e150 cm, >150 cm).
In January 2010, ten soil samples were taken randomly from each replicate using a soil auger, and analysed for particle size
composition (clay, sand, rock and silt), pH, conductivity, Carbon (C), Potassium (K), Sodium (Na), Calcium (Ca), Magnesium
(Mg), Phosphorus (P), and Nitrate (NO3) by BemLab, South Africa.
Principal component analysis (PCA) was performed to summarize the variation for vertical and horizontal habitat
structure respectively. The rst two principal coordinates explained 37% and 24% of variation for vertical (cumulative vari-
ation ¼61%) and 41% and 30% (cumulative variation ¼71%) for horizontal habitat structure. The rst principal component
axis for vertical habitat structure (PC1
intermediate.vertical.habitat
) was positively correlated with sites harbouring intermediately
tall vegetation structure (50e75 cm, 75e100 cm, 100e125 cm), and negatively with habitats lacking vertical structure. The
second principal component (PC2
canopy.vertical.habitat
) was positively correlated with tall canopy cover (125e150 cm, 150þ) and
negatively with vertical vegetation below 25 cm and no canopy cover. The rst principal component axis for horizontal
habitat structure (PC1
bare.ground.horizonal.habitat
) was positively correlated with bare ground and negatively correlated with
vegetation cover. The second principal component (PC2
leaf.litter.horizonal.habitat
) was positively correlated with leaf litter
presence and negatively to exposed rock.
For soil characteristics the rst two axes explained 46% and 15% of the variation. The rst principal component axis
(PC1
acid.soils
) was positively correlated with acidic soil and negatively with basic soils. The second principal component axis
(PC2
sandy.soils
) was positively correlated with sandy soil and negatively with clay soil.
2.3.1. Statistical analysis
For each of the 528 ant communities in the dataset [i.e. 4 replicates per sampling site x 11 sites 6 years x 2 sea-
sons ¼528), we calculated species richness. Species richness was modelled using linear mixed effect models with Gaussian
distribution and replicates specied as random intercept to account for temporal pseudo-replication while all predictor
variables were included as xed effects, with various subsets of variables and in various combinations. Certain variables
G.S. Joseph et al. / Global Ecology and Conservation 17 (2019) e00596 3
(altitude, mean temperature, minimum temperature, and maximum temperature) were collinear, therefore none of the
candidate models contained more than one of these as the explanatory variable. For measures of vertical (vegetation height,
canopy cover) and horizontal (percentage bare ground, vegetation, rock, leaf litter) vegetation structure, and soil parameters
(particle size, pH, conductivity, and chemical composition), we used the values generated by the principal correspondence
analyses. Along with these, other predictor variables used in the model were aspect, year and season. The best model was
chosen using Akaike information criterion (AIC). Marginal R
2m
(variation explained by effects only) and conditional R
2c
(variation explained by xed and random effects) were calculated for the best random-intercept model (Nakagawa and
Schielzeth, 2013) in R programming environment version 3.5.0 (R Core Team, 2017).
Next we calculated stability
asr
over time using mean species richness and its standard deviation, using each replicate set of
traps at each site (n ¼4 replicate x 11 sites ¼44). These were used to calculate the coefcient of variation, the inverse of which
yielded a measure of stability, following various authors (Isbell et al., 2009;Lehman and Tilman, 2000). Thus stability was
calculated as:
CV1¼mean ðXÞ
standard deviation x100
We calculated community similarity using two methods, Bray-Curtis similarity (1 minus the Bray-Curtis dissimilarity,
which quanties compositional similarity between different sites, based on abundance at each site), and Sorensen's index
(which uses presence and absence to discriminates as to whether a species is common at a site or not, giving greater emphasis
to species common to sites than to those found at only one site). Replicates from each site were lumped to yield the total
community caught at each site. We compared the similarity of community composition for each site from each year and
season with the composition of the community at that site for every other year and season, using the Vegan package in R
(Oksanen et al., 2016). We then assessed these similarity values for each of the sites with the similarity values for sites at other
altitudes and aspects, using a multiple linear regression.
To better understand which species drive community similarity at altitude, we used community abundance data,
exploring the directionality, magnitude and uncertainty of individual taxa threshold responses and community threshold
responses to an altitudinal gradient for each year separately using Threshold Indicator Taxa Analysis in TITAN2 package in R,
(Baker et al., 2015;Baker and King, 2010). Z scores are standardized against the mean and standard deviation of permuted
samples, and so emphasise degree of change, thus prioritising taxa with infrequent occurrence. We used untransformed
abundances on taxa occurring three or more times in the different sites over the entire period (2009e2015), with all par-
titions having at least three observations on both sides. TITAN also identies taxon-specic community thresholds. Boot-
strapping is used to estimate indicator reliability and purity as well as uncertainty around the location of individual taxa and
community change points. Standardized taxa responses increasing at the change point (zþ) are distinguished from those that
decrease (z-).
3. Results
3.1. Patterns of species richness
Our traps contained a total of 102496 ants representing 35 genera from 128 species. Altitude and mean temperature were
correlated (t ¼8.8, n ¼438, p <0.001). We therefore ran two sets of models, one using altitude, and the other using mean
temperature as one of a number of explanatory variables. We adopted an information theoretic approach, based on the bias-
corrected Akaike information criterion (AIC
c
) to choose the best model. The t of altitude (AIC
c
¼2377; variation explained
42%) to the data was better than mean temperature (AIC
c
¼2378; variation explained 39%). Species richness (1) declined
signicantly with increasing altitude and was lower (2) on south-facing slopes (3) at the end of the dry season, and (4) in 2009
than in other years. The decrease in richness with increasing altitude was more marked on northern aspects. Species richness
was signicantly greater for sites with sandy soils with lowclay content (Table 1a; Fig. 1.). An interaction between altitude and
southern aspect was observed, with richness declining with altitude on the northern aspect, but remaining almost constant
across altitudes on southern slopes.
3.2. Patterns of stability
Overall, stability
asr
declined signicantly with altitude, and was signicantly lower on south-facing aspects. There was an
interaction between altitude and aspect, such that stability
asr
decreased with increasing altitude on northern slopes, but
increased slightly on southern slopes (Fig. 2.).
Stability
asr
also varied with vegetation, increasing with both axis 1 (more bare ground and little live vegetation cover) and
2 (increasing leaf litter with minimal exposed rock) of the PCA for horizontal vegetation structure, and with the second axis
for soils (sandy soils with low clay content; Table 1b).
G.S. Joseph et al. / Global Ecology and Conservation 17 (2019) e005964
3.2.1. Patterns of similarity
Using the Bray-Curtis index, overall for the system similarity increased with altitude and this was the case for both
northern and southern aspects. There was an interaction between aspect and altitude, with a more rapid increase in similarity
Table 1
Summary of the AIC
c
ebased model selection for variables explaining ant species richness (a), stability of ant species richness (b), compositional similarity of
ant communities using Bray-Curtis (c) and Sorensen's (d) indices. The change in AICc between the best model, the next best, and worstare reported. Marginal
R
2
(R
2m
), measuring variation explained by xed effects only, and conditional R
2
(R
2c
), measuring variation explained by both xed and random effects, are
given.
Response variable Model AIC
c
D
AIC
c
(next best)
D
AIC
cnull
R
2m
R
2c
(a) ant species richness ~ elevation x aspect þseason þPC2
sandy.soils
þyear 2377.4 3.2 101.4 0.30 0.42
Best Model:
North aspect: y ¼16.2 ( ±1.7) e0.004 ( ±0.001)elevation e1.5 ( ±0.4)wet þ8.0 ( ±1.8)PC2
sandy.soils
þ1.6 ( ±0.6)year
2010
þ
3.3 ( ±0.6)year
2011
þ2.4 ( ±0.6)year
2012
þ4.5 ( ±0.6)year
2013
þ3.1 ( ±0.8)
South aspect: y ¼7.5 ( ±1.7) þ0.001 ( ±0.001)elevation e1.5 ( ±0.4)wet þ8.0 ( ±1.8)PC2
sandy.soils
þ1.6 ( ±0.6)year
2010
þ
3.3 ( ±0.6)year
2011
þ2.4 ( ±0.6)year
2012
þ4.5 ( ±0.6)year
2013
þ3.1 ( ±0.8)
(b) stability of ant species richness ~ elevation x aspect þ
PC1
bare.ground.horizonal.habitat
þPChor2 þPC2
sandy.soils
115.5 2.6 12.2 0.47 e
Best Model
y¼7.7 ( ±1.0) e0.003 ( ±0.001)elevation e6.7 ( ±1.3)aspect þ39.5 ( ±17.0) PC1
bare.ground.horizonal.habitat
þ42.2 ( ±13.7) PC2
leaf.litter.horizonal.habitat
þ1.9 ( ±0.9)PC2
sandy.soils
(c) similarity: Bray-Curtis ~ elevation x aspect 694.9 25.3 187.3 0.23 e
Best Model:
North aspect: y ¼0.23 ( ±0.03) þ1.9 x 10
4
(±2.6 x 10
5
)elevation
South aspect: y ¼-0.08 ( ±0.03) þ4.1 x 10
4
(±2.6 x 10
5
)elevation
(d) similarity: Sorensen's ~ elevation x aspect 1691.1 32.2 214.5 0.21 e
Best Model:
North aspect: y ¼0.73 ( ±0.02) e8.3 x 10
4
(±2.2 x 10
5
)elevation
South aspect: y ¼0.44 ( ±0.02) e6.7 x 10
4
(±2.2 x 10
5
)elevation
Fig. 1. Ant species richness as a function of aspect and increasing altitude (a), aspect alone (b), season (c), sandy soils low in clay content (d).
G.S. Joseph et al. / Global Ecology and Conservation 17 (2019) e00596 5
on southern aspects. However, it is notable that at low elevations of 800 m similarity between communities was lower on the
southern than on the northern aspect, but that by 1700 m, similarity had become higher on the southern aspect (Table 1c;
Fig. 3a). With Sorensen's index, overall, similarity also increased with altitude, but similarity underwent a slight decrease on
the northern aspect with increasing altitude (Table 1d; Fig. 3b).
3.2.2. Threshold Indicator Taxa Analysis
Threshold Indicator Taxa Analysis cumulatively identied 37 individual ant taxa that declined in response to increasing
altitude, with an observed environmental change point occurring around 1200 m. For 20 species, a positive change point was
observed at 1400 m, and these species increased in response to increasing altitude (Fig. 4).
4. Discussion
We found that the stability of invertebrate richness, using Afrotropical montane ants as an example, decreased with
increasing altitude. This study is the rst to evaluate stability of species richness and composition along an elevational
gradient over time. Unsurprisingly, patterns of ant species richness echo previous studies (decreasing with higher altitude,
cooler south-facing slopes, and the dry season, conditions with lower forage availability, temperatures and humidity; Bishop
et al., 2014;Mauda et al., 2018;Yusah et al., 2012), emphasising that broad changes in temperature are a strong driver of ant
richness patterns (Bishop et al., 2017;H
olldobler and Wilson, 1994;Sanders et al., 2007).
In general, the presence of many species increases stability (García-Palacios et al., 2018;Loreau et al., 2001), and the
nding that stability
asr
displayed a strong elevational pattern, with species number uctuating increasingly with altitude,
supported our hypothesis of deceasing stability
asr
at higher elevations, in line with a decrease in ant species richness at
altitude (Bishop et al., 2014;Munyai and Foord, 2015). Stability
asr
was lower on southern slopes, which are colder across
seasons, and receive less exposure to sunlight in the southern hemisphere. Although stability
asr
remained lower than on
northern slopes, it increased marginally on southern slopes with increasing elevation. Vegetation structure was not shown to
Fig. 2. Stability of ant species richness decreased signicantly with increasing altitude on northern slopes, yet increased negligibly on southern slopes.
Fig. 3. The relationship between ant community similarity and altitude using Bray-Curtis (a) and Sorensen's (b) similarity indices.
G.S. Joseph et al. / Global Ecology and Conservation 17 (2019) e005966
be a driver of stability
asr
in our study, but these southern slopes are known to receive more precipitation, and are charac-
terised by more woody vegetation, resulting in shading and cooler microclimates (Munyai and Foord, 2015). This in turn may
inuence stability
asr
on southern slopes, but remains untested. It is more likely that species richness, which did not decrease
on southern slopes (also perhaps due to the vegetation and precipitation properties of this southern aspect; Fig. 3), exerts a
modulating effect, given the expectation that presence of more species can enhances stability (García-Palacios et al., 2018;
Loreau et al., 2001).
Bare ground with little intermediate vegetation structure increased stability
asr
, as did increased leaf litter with minimal
exposed rock, perhaps as a consequence of additional habitat complexity minimising variation of species richness over time
(Mauda et al., 2018;Tiede et al., 2017). Stability
asr
also increased with sandy soils with low clay content, a substrate known to
favour ant species richness (Mauda et al., 2018). Stability
asr
, lower in the rst year, is interpreted in the context of both mean
annual temperature, which was lower in 2009 than in all other years (by at least 1
C), and minimum annual temperature,
which was >1
C higher in 2010, but 5
C higher by 2014e2015 (Appendix Fig.S1;Sanders et al., 2007).
Compositional similarity of ant communities was higher overall with increasing altitude regardless of the index used, but
the ndings for aspect were more complex. On both northern and southern slopes, the Bray-Cutis index showed that on both
northern and southern slopes, ant communities become more similar with higher altitude. As this index determines simi-
larity by using species abundance, ndings suggests that species that are common (altitude-adapted) at high elevations,
remain common as altitude increases, and that ant taxa poorly adapted to altitude disappear, or become less common with
increasing elevation. Sorensen's index revealed the same pattern for the southern slope, but that communities were slightly
less similar with increasing altitude on northern slopes. Given that Sorensen's index uses presence-absence, it is sensitive to
the appearance or disappearance of a given species, and results may reect a lower degree of environmental ltering on the
relatively warmer, more hospitable northern slopes. Furthermore, within the context of there being fewer species at
elevation, Sorensen's index can be expected to be sensitive to adding or taking away species, because the number of species at
altitude is low to start off with.
Given the thermophilic nature of ants (Bishop et al., 2017;H
olldobler and Wilson, 1994;Sanders et al., 2007), and studies
conrming that ability to tolerate cold temperatures at altitude can be important for ant distribution (Bishop et al., 2017), it is
likely that at higher altitude, the limited species that are best adapted to elevation come to dominate high altitude com-
munities, which gradually become more similar with increasing elevation. In summary, ndings reveal that there are few
species at higher relative to lower altitudes, and that these few species tend to be dominant at higher altitudes as only they
can persist in such conditions. Conversely, at lower altitudes, more species are able to persist in the relatively benign low-
elevation conditions, limiting opportunities for specic species to emerge as dominant over the protracted period of six years.
Fig. 4. Signicant ant indicator taxa identied in threshold indicator taxa analysis (TITAN), across an altitudinal gradient. Red symbols correspond to negative (z-)
indicator taxa, and denote taxa that decrease with increasing elevation, and blue correspond to positive (zþ) taxa, namely those that increase as altitude increase.
Symbols are in size proportional to z scores. Horizontal lines show 5th and 95th percentiles among 500 bootstrap replicates. (For interpretation of the references
to colour in this gure legend, the reader is referred to the Web version of this article.)
G.S. Joseph et al. / Global Ecology and Conservation 17 (2019) e00596 7
Threshold Indicator Taxa Analysis conrmed that there were 85% more indicator species that decreased with increasing
altitude, nearly double the small number of indicator species that increased with increasing altitude (Fig. 4). This facilitates
interpretation of similarity indices (which increased with increasing altitude), and stability
asr
measures, if one considers that
not only do the threshold indicator taxa reveal a smaller species pool at altitude, but also reveal a threshold altitude, above
which the majority of indicator species are poorly represented. The majority of indicator ant taxa decrease consistently as
elevation increases to 1200 m. The small number of altitude-adapted indicator species dominate at altitudes above 1420 m,
and as altitudes declines below 1420 m, such species no longer dominate as they did at higher altitudes. Findings reveal that
these high altitude ant communities are (1) species poor (2) have lower stability
asr
(and with low-species numbers, even
alteration of a few species can cause uctuation to richness over time), and are (3) more similar to one another by virtue of
there being only a limited suite of ant species able to tolerate high altitude (and the variables correlated with elevation, e.g.
lower minimum, mean and maximum temperatures, decreased humidity, differing soils and vegetation structure).
At a regional scale, currently within the Soutpansberg, a few altitude-adapted species appearto be holding the fortat high
elevation, living in communities that increasingly resemble one another as altitude increases. The new Vhembe biosphere
reserve zonation proposes that all areas above 1200 m in the Soutpansberg be proclaimed core conservation areas, and our
ndings identify 1200 m as the change point where the lower elevation species start falling out of assemblages, whilst al-
titudes approaching 1400 m become important for the high altitude species. At the scale of the Soutpansberg complex itself,
1200 m also coincides with the appearance of Afromontane forests on southern aspects, and 1400 m corresponds with a
switch to more open, Soutpansberg Mountain Sourveld habitat (Depatment of Environmetal Affairs, 2018;Mucina and
Rutherford, 2006).
Given that montane assemblages across elevational gradients are often dominated by rare or endemic species, they can be
particularly vulnerable to temperature changes (García-Robledo et al., 2016), so at the broadest scales, uctuation of species
numbers at higher elevations disproportionality places them at risk from global change. In southern Africa, temperatures are
anticipated to rise by up to 2.5
C over three decades (Davis and Vincent, 2017), potentially opening niches to thermophilic,
heat-adapted invertebrates. Although this study does not address the impact of global change, it can be speculated that with
the buffer that stability of species richness can confer already compromised at altitude, communities at higher elevation may
be at increased risk of invasion and restructuring as new niches form. Suitable microclimates and microhabitats may
modulate this (Duffy et al., 2015;G.S.Joseph et al., 2016), as was the case with e.g. sandy soils and leaf litter in this study, but
further research will be needed to determine whether the lowered stability
asr
will allow thermophilic, low-altitude ants and
invasive species to restructure communities at high altitudes.
Acknowledgements
We thank the DST-NRF Centre of Excellence for Invasion Biology, through the South African Research Chairs Initiative Chair
on Biodiversity Value and Change in the Vhembe Biosphere Reserve, hosted by the University of Venda.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.org/10.1016/j.gecco.2019.e00596.
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G.S. Joseph et al. / Global Ecology and Conservation 17 (2019) e00596 9
... This approach therefore has considerable potential for addressing the influence of both the successional stage and strata on ant communities. Ecological stability, the inverse of variation over time, is a fundamental ecosystem property that offers insights into biodiversity and ecosystem processes (Doak et al., 1998;Joseph et al., 2019;Tonkin et al., 2017). Critically, β-diversity can be decomposed into the turnover and nestedness components, which provide complementarity insights into community ecological stability: the turnover component reflects species replacement, while the nestedness component reflects species richness differences driven by a pattern of community subsetting (Baselga, 2010). ...
... This result is somewhat surprising, especially because there is a significant change in the richness and composition of ant species with the advance of the successional secondary vegetation (Marques et al., 2017;Neves et al., 2013). Studies carried out in savannas and mountain ecosystems have found that greater habitat complexity should minimize the variation of ant diversity over time (Joseph et al., 2019;Mauda et al., 2018;Tiede et al., 2017), which is contrary to our finding of high variation even in the late stage. However, it is important to note that tropical dry forests are strongly seasonal, and the ant fauna might have evolved to cope with natural variations under these habitat conditions. ...
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... In general, warmer locations and time periods host greater ant abundance and species richness. These patterns can be seen at the local scale (Joseph et al., 2019), across elevational gradients (Bishop et al., 2014;Sanders et al., 2007), latitudinal gradients (Dunn et al., 2009;Economo et al., 2018;Gibb et al., 2015;Jenkins et al., 2011), and seasons (Andersen, 1983;Bishop et al., 2014). This link between temperature and community-level richness at a range of scales and contexts suggests that communities will support a greater diversity of ant species as temperatures rise. ...
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