An Inverse Elevational Species Richness Gradient of Caucasian Vascular Plants and Encyrtidae (Hymenoptera, Chalcidoidea)

Abstract

The elevational gradient in biodiversity, i.e. the decrease in species richness with increasing altitude, is well established in ecology. Here, we examined the respective gradient of parasitic hymenopterans (Encyrtidae) and plants in the Lagodekhi National Park (Country of Georgia) across an elevational gradient from 665 m to 2559 m a.s.l. by means of a year-round sampling of insects and a seasonal sampling of plants. Contrary to expectation, we found species richness of both taxa to peak at highest elevations. This unusual pattern was related to particular shifts in vegetation types, from relatively species-poor forests over rich grasslands towards poorer highland scrub vegetation. Our results call for a closer look at elevational gradients and highlights the need for including vegetation types in the assessment of altitudinal diversity gradients.

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An inverse elevational species richness gradient
of Caucasian vascular plants and Encyrtidae
(Hymenoptera, Chalcidoidea)
Levan Mumladze, Werner Ulrich, Zezva Asanidze & George Japoshvili
To cite this article: Levan Mumladze, Werner Ulrich, Zezva Asanidze & George Japoshvili (2017):
An inverse elevational species richness gradient of Caucasian vascular plants and Encyrtidae
(Hymenoptera, Chalcidoidea), Écoscience, DOI: 10.1080/11956860.2017.1324717
To link to this article: http://dx.doi.org/10.1080/11956860.2017.1324717
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RESEARCH NOTE
An inverse elevational species richness gradient of Caucasian vascular plants
and Encyrtidae (Hymenoptera, Chalcidoidea)
Levan Mumladze
a,b
, Werner Ulrich
c
, Zezva Asanidze
a,b
and George Japoshvili
a,d
a
Invertebrate Research Center (IRC), Tbilisi, Georgia;
b
Biodiversity Research Center, Institute of Ecology and Institute of Zoology, Ilia State
University, Tbilisi, Georgia;
c
Ecology and Biogeography, Nicolaus Copernicus University, Toruń, Poland;
d
Institute of Entomology, Agricultural
University of Georgia, Tbilisi, Georgia
ABSTRACT
The elevational gradient in biodiversity, i.e. the decrease in species richness with increasing
altitude, is well established in ecology. Here, we examined the respective gradient of parasitic
hymenopterans (Encyrtidae) and plants in the Lagodekhi National Park (Country of Georgia)
across an elevational gradient from 665 m to 2559 m a.s.l. by means of a year-round sampling
of insects and a seasonal sampling of plants. Contrary to expectation, we found species richness
of both taxa to peak at highest elevations. This unusual pattern was related to particular shifts in
vegetation types, from relatively species-poor forests over rich grasslands towards poorer high-
land scrub vegetation. Our results call for a closer look at elevational gradients and highlights the
need for including vegetation types in the assessment of altitudinal diversity gradients.
RÉSUMÉ
Le gradient altitudinal de biodiversité, c.-à-d. la diminution de la richesse spécifique suivant
l’augmentation de l’altitude, est bien connu en écologie. Nous avons examiné les gradients
d’hyménoptères parasites (Encyrtidae) et de plantes dans le Parc National de Lagodekhi
(Georgie), entre 665 et 2559 m a.s.l., par un échantillonnage annuel d’insectes et saisonnier de
plantes. Contrairement aux attentes, nous avons trouvé que la richesse spécifique des deux taxa
était plus élevée aux plus hautes altitudes. Ce patron inhabituel était lié à des changements
particuliers des types de végétation, passant de forêts relativement pauvres en espèces, à des
prairies riches, jusqu’à des arbustaies pauvres. Nos résultats indiquent l’importance de mieux
évaluer les gradients altitudinaux et soulignent la nécessité d’inclure les types de végétation dans
l’analyse des gradients altitudinaux de biodiversité.
ARTICLE HISTORY
Received 20 April 2017
Accepted 26 April 2017
KEYWORDS
Elevational gradient;
biogeography; parasitoids;
plants
MOTS CLÉS
gradient altitudinal;
biogéographie; parasites;
plantes
Introduction
The decrease in species richness with increasing lati-
tude is well established for many animal and plant taxa,
thus forming one of the main biogeographical rules
(reviewed in Brown (2014)). Among the few known
examples with inverse latitudinal gradients are at least
two taxa of Hymenoptera, the phytophagous Symphyta
(Kouki et al., 1994) and the parasitoid Inchneumonidae
(Timms et al., 2016; but see Veijalainen et al., 2012;
2014). This is in sharp contrast with the well-estab-
lished and pronounced increase in species richness in
other insect taxa, like Coleoptera, Lepidoptera, Diptera
(Crowson, 1981; Holloway, 1987; Lobo, 2000; Larocque
et al., 2006), but also non-parasitoid Hymenoptera
(Apocrita: Abrahamczyk et al., 2011).
The functional equivalent of the latitudinal richness
gradient is the elevational decrease in species richness
(McCain & Grytnes, 2010; Fischer et al., 2011;Guo
et al., 2013), although the underlying ecological and
evolutionary causes might differ. While latitudinal rich-
ness gradients are apparently triggered by temperature
dependence of ecological and evolutionary rates (Brown
2014), altitudinal richness gradients are more under the
control of ecological processes driven by climate,
resource availability, reduced habitat size and variability
(McCain & Grytnes, 2010). This interplay of mechan-
isms can result either in the typical altitudinal richness
decrease or in mid-altitudinal richness peaks (McCain &
Grytnes, 2010; Guo et al., 2013). In any case, the eleva-
tional gradient seems to be more ‘universal’than the
latitudinal gradient, and so far no counterexample has
been described (Fischer et al., 2011).
In this study, we show that the local diversity of
encyrtid wasps and plant communities forms a
CONTACT Levan Mumladze lmumladze@gmail.com Invertebrate Research Center, Agladze #26, Tbilisi-0119, Georgia
Supplemental data for this article can be accessed here.
ÉCOSCIENCE, 2017
https://doi.org/10.1080/11956860.2017.1324717
© 2017 Taylor & Francis

counterexample to the elevational gradient rule.
Encyrtidae are a hyper-diverse Chalcidoid family con-
taining more than 3000 species worldwide, which
mainly attack lepidopteran, aphid, and scale insect
hosts (Noyes, 2016). We measured encyrtid and plant
richness along an elevational gradient in the Eastern
Caucasian Mountains. Prior studies from these and
surrounding areas have shown hump-shaped patterns
or decreases in richness with increasing elevation in
various arthropod groups (Murvanidze et al., 2004;
Chaladze, 2012; Chaladze et al., 2014; Mumladze
et al., 2015; Aslan et al., forthcoming 2017), plants
and snails (Mumladze et al., 2017). Thus, the increase
in plant and encyrtid richness contrasts with the gen-
eral diversity pattern in this specific region.
Materials and methods
The Lagodekhi National Park (Country of Georgia) is
the oldest protected area in the Caucasus (more than
100 years old) and covered by old-growth primary
mixed forests dominated by beech (Fagus orientalis).
Only at lower elevations (600–700 m) and near the tree
line (2200 m) are other tree species (Carpinus betulus/
Quercus ssp. and Betulla/Acer ssp., respectively) predo-
minant. In the forested area, five small, naturally open
sites (forest edges) with dense herbaceous vegetation
along an elevational transect spanning from 665 m to
1900 m a.s.l. were selected for sampling (Table 1;
Figure 1). We chose this ecotone in order to increase
efficiency of sampling species associated exclusively
with forests and meadows. In addition, we established
two extra sites above tree line (in subalpine/alpine
areas). At each location, a single Malaise trap was set
up from early spring to the end of the vegetation
season to collect Encyrtidae. Samples we collected
every 10 days resulted in a total of 1080 trap-days,
with 190 trap-days at the lowest (665 m) and 130
trap-days at the highest elevation (2559 m).
In each plot,we assessed the richnessof vascular plants
using total counts in four randomly located 10 × 10 m
2
plots within an area of 2500 m
2
around each Malaise trap.
Plant inventories were performed in May, June, and
September. The Encyrtidae were identified using the
keys of Trjapitzin (1989), Gibson et al. (1997), Hayat
(2006), and Guerrieri and Noyes (2000,2005).
Table 1. Summary data on the studied sites and species diversity for each sampling elevation.
Sampling site Elevation Longitude Latitude Herb richness
Woody plant
richness
Total encyrtid
abundance Encyrtid richness
p1 665 41.85248 46.28776 39 12 228 27
p2 845 41.85585 46.29273 35 14 65 22
p3 1345 41.87146 46.31153 28 10 330 51
p4 1850 41.88273 46.32185 22 10 70 29
p5 1900 41.88557 46.32413 69 17 193 50
p6 2230 41.89805 46.33387 127 7 131 34
p7 2559 41.90616 46.33340 112 3 252 48
Figure 1. Location of the study area and sites in Georgia.
2L. MUMLADZE ET AL.

Several singletons and doubletons are typical in
arthropod inventories (Coddington et al., 2009) and
our study is no exception. Therefore, we used abun-
dance-based asymptotic richness estimation to obtain
expected Encyrtid species data according to the estima-
tors of Chao et al. (2014) and Chao et al. (2016), using
the pooled abundance data represented in all traps for
each sampling elevation. For plant species, we used
incidence data of four plots at each sampling elevation
to estimate asymptotic expected richness. We tested the
strength of the altitudinal gradients using ordinary
least squares regression (OLS).
Results and discussion
In total we found 54 woody and 244 herbaceous plant
species (Supplementary Material Tables S1, S2). Woody
species richness decreased with altitude, while herbs had
lowest richness at intermediate altitude and highest rich-
ness above 2200 m (Figure 2(a); Table 1). Interestingly, a
recent study on plant diversity from a nearby mountain
(Mumladze et al., 2017) revealed a linear increase of total
plant richness from 600 to 2200 m. However, this study
dealt with forest plots only, while our data include forest
edges and subalpine/alpine meadows. Consequently, the
linear increase in plant richness reported by Mumladze
et al. (2017) is closely linked to the increased canopy
opening at higher elevation.
A total of 1348 individuals representing 103 named
species and 16 morpho-species of Encyrtidae were
captured (Supplementary Material Table S3), among
which 45 species are new records for the country.
Observed and estimated encyrtid species richness
increased with increasing elevation (Figure 2(b)). At
665 m we found 29 and expected 33 species, while
these values increased to 48 and 70 species, respectively
at 2559 m (Figure 2(b)). The vast majority of
Encyrtidae depend on phytophagous arthropod host
species. Consequently, encyrtid richness should
increase with plant diversity. This was not the case
(Figure 2(c)). In contrast, the proportion of
Encyrtidae with respect to plant species was highest at
intermediate altitude, where herbaceous plant richness
was lowest. Of course, the host range of most of the
encyrtid species is unknown, and thus the plant rich-
ness is only a crude proxy to the potential number of
hosts. Nevertheless, this result combined with the
increase in total encyrtid richness contrasts to the
common altitudinal richness gradient. Clearly, parasi-
toid Hymenoptera need further studies with respect to
common biogeographic patterns. Possibly the parasi-
toid way of life counteracts common climatic con-
straints on richness, making less favourable habitats
still attractive for a larger number of parasitoid species.
Our study design cannot exclude differences in sam-
ple coverage among the study sites. Decreasing woody
Figure 2. (a) Observed herbaceous plant (black circles: second order polynomial OLS regression r
2
= 0.74, p(F
1,5
) = 0.07) and woody
plant (light triangles: linear OLS r
2
= 0.28, p(F
1,5
) > 0.10) species richness in relation to elevation. Straight and broken lines
respectively show the 95% upper and lower confidence intervals of the estimated richness. Note that lower confidence limits are
very close to actual values. (b) Observed (black circles) and estimated (open circles, error bars indicate the 95% confidence limits of
estimation) increase with elevation (observation linear OLS r
2
= 0.30, p(F
1,5
) > 0.10, estimate r
2
= 0.60, p(F
1,5
) = 0.04). (c) The ratio of
encyrtid/plant species richness was highest at intermediate altitude (second order polynomial OLS regression r
2
= 0.73, p
(F
1,5
) = 0.07). d) Estimated encyrtid species richness did not increase with total abundance (d) p(F
1,5
) > 0.30).
ÉCOSCIENCE 3

plant cover might increase the effectivity of Malaise
traps, although we do not have any indication for such
an effect. Prior studies on Ichneumonidae (Timms et al.,
2016) and Parasitica as a whole (Ulrich, 2005)have
found a strong positive allometric dependence of species
richness with local abundance, and we expected to see a
similar pattern if sampling coverage had biased our
richness results. Surprisingly, sampling efficacy was inde-
pendent of elevation, as richness did not co-vary with
abundance (Figure 2(d)). The observed altitudinal
increase in species richness (Figures. 2(a,b)) was linked
to reduced average abundances per species at higher
altitude, dropping from 4.5 individuals per species and
trap below 1000 m to 2.7 individuals per species and trap
above 2000 m. Consequently, our data suggest a change
in the pattern of species abundances towards an
increased proportion of relatively rare species at higher
altitude. However, due to the limited sample size future
studies have to verify this alleged altitudinal abundance
gradient.
Acknowledgments
We would like to express our gratitude to G. Sulamanidze (head
of LNP), G. Kirkitadze, M. Salakaia and M. Bacankalashvili for
helping in field work and sample processing.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the research grant ‘The biodi-
versity of Hymenoptera of Lagodekhi protected area’sup-
ported by the Shota Rustaveli National Science Foundation
(FR/221/7-110/13). W.U. was supported by an institutional
scientific dotation of the Nicolaus Copernicus University;
ORCID
Levan Mumladze http://orcid.org/0000-0002-2172-6973
Zezva Asanidze http://orcid.org/0000-0001-7859-7917
George Japoshvili http://orcid.org/0000-0002-9901-4554
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