CC BY
34Russian Journal of Nematology, 2021, 29 (1), 31 - 48
Biodiversity and distribution of soil nematodes in
Mount Ararat, Turkey
Taylan Çakmak1' 2, Çigdem Gozel3, Ugur Gozel3, Denis Tange Achiri4' 5 and
Mehmet Bora Kaydan6' 7
^Departamento de Protección Vegetal, Instituto Canario de Investigaciones Agrarias, Valle Guerra La Laguna, 38270,
Tenerife, España
2Department of Agricultural Biotechnology, Faculty of Agriculture, Düzce University, 81620, Düzce, Turkey 3Department of Plant Protection, Faculty of Agriculture, Canakkale Onsekiz Mart University, 17100, Çanakkale, Turkey ^Department of Plant Protection, Faculty of Agriculture, Çukurova University, 01330, Balcali, Adana, Turkey 5Department of Agronomic and Applied Molecular Sciences, Faculty of Agriculture and Veterinary Medicine, University of
Buea, P.O. Box 63, Buea, Cameroon 6Biotechnology Application and Research Centre, Çukurova University, 01330, Balcali, Adana, Turkey 7lmamoglu Vocational School, Çukurova University, 01330, Balcali, Adana, Turkey e-mail: [email protected]
Accepted for publication 13 April 2021
Summary. The diversity and distribution of soil nematodes were studied in Mount Ararat from the altitude of 1523 to 5000 m a.s.l., in habitats with different ecological characteristics. A total of 2,561 individuals were identified belonging to 31 families, 62 genera and 70 species. The nematode diversity (species richness) and the nematode abundance display recognisable patterns of altitudinal distribution as the number of species reaches a maximum at intermediate elevations, whereas the nematode abundance was significantly higher at the elevated altitudes. The nematode community associated with the marshland habitat was significantly different from those associated to the other four types of habitat. Key words: altitude, community analysis, distribution patterns, mountain ecology.
Nematodes (phylum Nematoda) are a diverse group of ecdysozoa, i.e. invertebrate animals characterised by a simple body plan, nearly ubiquitous distribution, wide variety of feeding habits and life strategies, and they play an important role in the food webs of the habitats in which they dwell. With nearly 25,000 nominal species (Zhang, 2011), some conservative estimates of their existing diversity reach up to 1,000.000 of living forms (Hugot et al., 2001), certainly being the most diverse animal phylum after Arthropoda. Many species are free-living, inhabiting soils and both freshwater and marine sediments, and displaying a wide feeding spectrum, including predation, algivore, fungivore, omnivore, saprovore, etc. (Yeates et al., 1993). Other species are parasites of plants and animals, including humans where they cause severe diseases (Jasmer et al., 2003).
Spatial distribution of nematodes remains a poorly explored area of study. Soil nematodes are not an exception in this regard, even though they are important for fundamental and applied purposes, and there has been some recent progress in the research area (van den Hoogen et al., 2019). Many
important contributions, including Yeates (1979), Freckman & Caswell (1985), Procter (1990), Neher (2010) and Liu et al. (2019), compiled the most relevant advances in the knowledge of the general ecology of nematodes. However, less work was devoted to detect major distributional patterns, for instance, latitude (Procter, 1984), elevation, and soil and sediment depth gradients (Weischer & Almeida, 1995), and only a few papers tried to elucidate the causal agents (processes) of the observed distributional patterns of particular taxa as it occurred with the members of the family Longidoridae (Dalmasso, 1970; Topham & Alphey, 1985; Navas et al., 1993). Several authors (Yeates, 2003; Hanel, 2010; McSorley, 2011) showed that most ecological studies used genera and families as taxonomical units in their analyses and suggested species-level identification should be a requirement to reach more significant progress in the discipline.
Elevation gradients are regarded as interesting natural environments to conduct field observations and to test experimental ecological hypotheses as both abiotic and biotic variations may take place over short distances (Hodkinson & Jackson, 2005).
© Russian Society of Nematologists, 2021; doi: 10.24411/0869-6918-2021-10004 Published online 30 July, 2021
Table 1. Altitudes, coordinates, eco-habitat, time, date and air temperature at 29 sampling sites in Mount Ararat, Turkey.
Sample no. Altitude (m a.s.l.) UtmX UtmY Sub-ranges (m a.s.l.) Habitat
1 4957 39°42'5.34" N 44°17'31.68" E - Frozen igneous Soil
2 4752 39°41'52.74" N 44°17'21.48" E - Igneous Soil
3 4531 39°41'42.96" N 44°17'13.14" E - Igneous Soil
4 4372 39°41'34.62" N 44°17'9.36" E - Igneous Soil
5 4184 39°41'24.72" N 44°17'3.84" E 3500-4000 Wildflower meadow
6 3972 39°41'11.64" N 44°17'1.26" E 3500-4000 Mountain grassland
7 3972 39°41'11.09" N 44°17'2.00" E 3500-4000 Wildflower meadow
8 3757 39°41'3.91" N 44°16'49.80" E 3500-4000 Wildflower meadow
9 3754 39°41'2.22" N 44°16'46.98" E 3500-4000 Wildflower meadow
10 3562 39°41'2.51" N 44°16'54.26" E 3000-3500 Wildflower meadow
11 3563 39°40'50.40" N 44°16'38.74" E 3000-3500 Mountain grassland
12 3372 39°40'46.86" N 44°16'1.77" E 3000-3500 Mountain grassland
13 3372 39°40'46.37" N 44°16'1.43" E 3000-3500 Wildflower meadow
14 3144 39°40'33.30" N 44°15'41.46" E 2500-3000 Mountain grassland
15 3140 39°40'33.29" N 44°15'41.45" E 2500-3000 Mountain grassland
16 3053 39°40'21.48" N 44°15'24.12" E 2500-3000 Chalk grassland
17 2952 39°40'14.64" N 44°15'12.72" E 2500-3000 Riverbed
18 2756 39°39'51.66" N 44°15'0.06" E 2500-3000 Mountain grassland
19 2742 39°39'51.26" N 44°15'0.25" E 2500-3000 Mountain grassland
20 2554 39°39'39.59" N 44°14'36.53" E 2000-2500 Chalk grassland
21 2552 39°39'39.21" N 44°14'36.73" E 2000-2500 Mountain grassland
22 2488 39°39'35.12" N 44°14'27.68" E 2000-2500 Riverbed
23 2486 39°39'35.51" N 44°14'27.29" E 2000-2500 Riverbed
24 2337 39°39'16.46" N 44°13'54.55" E 2000-2500 Mountain grassland
25 2337 39°39'16.76" N 44°13'54.55" E 2000-2500 Mountain grassland
26 1900 39°38'28.47" N 44°12'7.30" E 1500-2000 Wildflower meadow
27 1900 39°38'28.47" N 44°12'7.50" E 1500-2000 Wildflower meadow
28 1524 39°36'19.66" N 44° 8'45.45" E 1500-2000 Marsh
29 1523 39°36'19.26" N 44°8'45.15" E 1500-2000 Marsh
However, there is only limited knowledge about the distribution of soil nematode communities over elevation gradients.
In Mount Ararat, which is the highest peak in Turkey (5,137 m a.s.l.), due to harsh and long winter periods, flora and fauna change drastically in different elevations. Depending on the geographical side of Mount Ararat, mainly flora are located between 21003800 m a.s.l., which is dominated by grasslands
(Koyuncu, 2005). The general purpose of this contribution is to explore the altitudinal distribution of nematode fauna in Mount Ararat, using species as taxonomical units and covering a large elevation transect. More specifically, this work aims: i) to characterise the nematode fauna associated with such transect; ii) to know the distribution of every species; iii) to detect tentative patterns of nematode diversity, and iv) to study the distribution of nematodes.
Table 2. Species abundance and occurrence in Mount Ararat, Turkey.
Taxon name Order Total abundance Relative abundance(%) Occurrence (%)
Eucephalobus mucronatus Rhabditida 305 12.2 a 88 A
Plectus spp. Plectida 238 9.5 a 80 A
Aphelenchoides spp. Rhabditida 204 8.1 a 72 B
Panagrolaimus rigidus Rhabditida 202 8.0 a 68 B
Rotylenchus sp. Rhabditida 162 6.4 a 28 C
Acrobeloides nanus Rhabditida 133 5.3 a 68 B
Mesodorylaimus sp. Dorylaimida 129 5.1 a 28 C
Aphelenchus spp. Rhabditida 113 4.5 a 64 B
Seleborca complexa Rhabditida 110 4.4 a 24 D
Acrobeles andalusicus Rhabditida 98 3.9 b 48 C
Geocenamus koreanus Rhabditida 79 3.1 b 56 B
Malenchus sp. Rhabditida 59 2.3 b 68 B
Chiloplacus bisexualis Rhabditida 57 2.2 b 40 B
Chronogaster sp. Plectida 47 1.8 b 8 D
Paratylenchus sp. Rhabditida 47 1.8 b 32 C
Heterodorus magnificus Dorylaimida 41 1.6 b 28 C
Acrobeles ciliatus Rhabditida 38 1.5 b 8 D
Aporcelaimellus spp. Dorylaimida 36 1.4 b 36 C
Tylencholaimellus montanus Dorylaimida 33 1.3 b 32 C
Tylenchus sp. Rhabditida 30 1.2 b 44 C
Enchodelus lucinensis Dorylaimida 28 1.1 b 36 C
Nagelus camelliae Rhabditida 27 1.0 b 16 D
Monhystera sp. Monhysterida 23 0.9 c 8 D
Tylocephalus auriculatus Plectida 23 0.9 c 12 D
Ecumenicus monhystera Dorylaimida 20 0.8 c 16 D
Geomonhystera sp. Monhysterida 18 0.7 c 16 D
Aporcelaimellus obtusicaudatus Dorylaimida 17 0.6 c 12 D
Eudorylaimus subdigitalis Dorylaimida 17 0.6 c 8 D
Tylenchorhynchus mangiferae Rhabditida 17 0.6 c 16 D
Eudorylaimus sabulophilus Dorylaimida 16 0.6 c 40 C
Cervidellus vexilliger Rhabditida 15 0.6 c 36 C
Chiloplacus trilineatus Rhabditida 14 0.5 c 28 C
Tylencholaimus teres Dorylaimida 14 0.5 c 32 C
Acrolobus longigubernaculum Rhabditida 13 0.5 c 8 D
Coslenchus sp. Rhabditida 12 0.4 d 28 C
Teratocephalus terrestris Rhabditida 12 0.4 d 16 D
Table 2 (continued). Species abundance and occurrence in Mount Ararat, Turkey.
Taxon name Order Total abundance Relative abundance(%) Occurrence (%)
Dorylaimus lineatus Dorylaimida 11 0.4 d 8 D
Pratylenchus neglectus Rhabditida 10 0.4 d 12 D
Crassolabium cylindricum Dorylaimida 6 0.2 d 8 D
Longidorella okhlaensis Dorylaimida 6 0.2 d 8 D
Nagelus hexagrammus Rhabditida 6 0.2 d 12 D
Pungentus sp. Dorylaimida 6 0.2 d 24 D
Rhabdolaimus sp. Plectida 6 0.2 d 12 D
Tylenchorhynchus maximus Rhabditida 6 0.2 d 16 D
Discolaimium sp. Dorylaimida 5 0.2 d 8 D
Heterodera trifolii Rhabditida 5 0.2 d 4 D
Tylencholaimus proximus Dorylaimida 5 0.2 d 4 D
Funaria cf. obtusa Dorylaimida 4 0.1 d 4 D
Microdorylaimus sp. Dorylaimida 4 0.1 d 12 D
Stegelletina spp. Rhabditida 3 0.1 d 8 D
Tobrilus sp. Triplonchida 3 0.1 d 8 D
Alaimus sp. Enoplida 2 0.08 d 8 D
Ditylenchus sp. Rhabditida 2 0.08 d 8 D
Dorylaimellus sp. Dorylaimida 2 0.08 d 8 D
Helicotylenchus sp. Rhabditida 2 0.08 d 8 D
Hoplolaimus sp. Rhabditida 2 0.08 d 8 D
Nygolaimus sp. Dorylaimida 2 0.08 d 4 D
Pratylenchus thornei Rhabditida 2 0.08 d 8 D
Zeldia sp. Rhabditida 2 0.08 d 8 D
Achromadora sp. Chromadoridae 1 0.04 d 4 D
Anaplectus sp. Plectida 1 0.04 d 4 D
Criconema sp. Rhabditida 1 0.04 d 4 D
Kochinema sp. Dorylaimida 1 0.04 d 4 D
Mesorhabditis sp. Rhabditida 1 0.04 d 4 D
Nothacrobeles sp. Rhabditida 1 0.04 d 4 D
Paracrobeles sp. Rhabditida 1 0.04 d 4 D
Propanagrolaimus hydrophilus Rhabditida 1 0.04 d 4 D
Scutellonema sp. Rhabditida 1 0.04 d 4 D
Trichodorus sp. Triplonchida 1 0.04 d 4 D
Xiphinema sp. Dorylaimida 1 0.04 d 4 D
Total abundance - 2561 - -
*The total abundance number was a sum from 29 samples. Each soil sample was a volume of 200 cm 3.
Fig. 1. Geographic location of Mount Ararat, Turkey.
Fig. 2. Vertical distribution of sampling sites and corresponding ecological characteristics in Mount Ararat.
MATERIAL AND METHODS
Geographical area. Mount Ararat is a dormant volcanic cone, located in the Eastern Anatolia Region of Turkey, between Dogubayazit and Igdir, near the border with Iran, Armenia and Nahcivan (Fig. 1), in the most thinly populated region of the country. It last erupted in 1840 and has a permanent ice cap of 400 m diameter at the summit. The mountain is a stratovolcano (conical volcano), made of many layers (strata) of hardened lava, tephra, pumice and volcanic ash. Farming is difficult because of the long, severe winters, steep slopes and eroded soil. However, grain, chiefly summer wheat and barley, are grown at its foothills, and there are pastoral nomads who raise sheep and goats at its lower parts. Due to harsh and long winter periods, flora and fauna change drastically with elevation. The surface of the mountain is covered by many endemic plant species (Koyuncu, 2005).
Sampling. A total of 30 (29 soil and one ice) samples (Table 1) were collected following an elevational transect/gradient ranging from 1523 to 5000 m a.s.l., along five habitats with different ecological characteristics, namely wildflower meadow, mountain grassland, chalk grassland, riverbed and marshland (Fig. 2). The total elevation range (1523-5000 m a.s.l.) was divided into five (sub) ranges in order to study and to analyse the distribution of the nematode fauna. Each sample was taken from a 15 * 15 plot at 30 cm depth, put into zip lock sampling bags, stored in portable cooler during the transportation, and brought to nematology laboratory of Department of Plant Protection, Faculty of Agriculture, University of Canakkale, Turkey. The survey was conducted on 20-26th July, 2013.
Extraction and mounting of nematodes. Nematodes were extracted by using the Baermann's (1917) funnel technique. After separating rocks and big organic particles, a volume of 200 cc soil was used for each sample site. Samples were placed on plastic trays lined with paper towels and incubated on the laboratory. Nematodes were collected after 48 h by pouring the extraction tray over a 500-mesh sieve (25 ^m opening) and put into DESS solution according to Yoder et al. (2006). Each extract was then labelled with corresponding sample number and transported in plastic tubes to the University of Jaén, Spain where all the preserved nematodes were rinsed with purified water to remove the debris. The staining blocks for each sample containing 1.25 cm deep volume of 96% ethanol plus a few drops of glycerol-formalin (4%) (1:99) with extracted nematodes was then placed in an airtight jar and left
overnight at room temperature. Next morning, the staining block was removed from the jar and a few drops of five parts glycerol and 95 parts 96% ethanol solution were added, two thirds of the staining block's cavity was covered with a glass square, and the block placed in an incubator at 40°C. For gradual transition of glycerin, a few drops of glycerol-ethanol (5:95) solution was added every 2 h. The day after, individual nematodes were permanently mounted on glass slides (Yoder et al., 2006). A total of 2561 nematodes were examined.
Light microscopy. Mounted nematodes were studied and identified using an Olympus BHS microscope (Olympus Optical, Tokyo, Japan). Morphometrics, including Demanian ratios and other measurements, were taken by means of a drawing tube (camera lucida) attached to the microscope.
Data analyses. For comparative purposes, species were classified into four groups based on their abundance and occurrence. For abundance the classifications were very abundant (a) (more than 4.0% of the total community), abundant (b) (1.04.0%), rare (c) (0.5-1.0%) and very rare (d) (< 0.5%); for occurrence, the classifications were: very frequent (A) (occurrence > 75%), frequent (B) (> 50%), infrequent (C) (> 25%), and scarce (D) (< 25%). The abundance set of classifications was designed based on the total number of nematodes in respect to total community. On the other hand, the occurrence set of classification was focused on their distribution along the mountain. The nematode community structure was analysed through correspondence analysis and non-metric MultiDimensional Scaling (MDS) applying the Euclidean and Chord similarity tests. One-way ANOVA and post-hoc Tukey tests were performed to assess the significant differences of species abundance and richness among different altitudinal ranges. MDS and correspondence analyses were performed with the PAST 2.17c software (Hammer et al., 2001). STATISTICA 7 software was used for ANOVA and post-hoc Tukey tests.
RESULTS
General composition of nematodes of Mount Ararat
Table 2 provides the basic data of the nematode fauna found in this study, including species composition, absolute abundance (number of specimens of each species), relative abundance (percentage of the total), and occurrence or frequency (number of samples in which each species was collected, expressed as percentage of the total number of 29 soil samples). The lowest nematode
distribution range was 1500-2000 m a.s.l., and the greatest range was 3500-4200 m a.s.l.; nematodes were not found in samples from above 4200 m a.s.l.
A total of 70 species, belonging to 62 genera, 31 families and 3 orders were identified. The nematode fauna was dominated by members of the order Rhabditida/Tylenchina (35 species and 31 genera), followed by those of the order Dorylaimida (22 species and 19 genera).
According to relative abundance, nine species were determined as very abundant, 13 species were abundant, 12 species belonged to rare taxa and 36 species were very rare. Among very abundant species were Aphelenchus spp., Aphelenchoides spp., Plectus spp., Seleborca complexa, Acrobeloides nanus, Eucephalobus mucronatus, Mesodorylaimus sp., Panagrolaimus rigidus, Rotylenchus sp. Considering their occurrence, two species, namely Eucephalobus mucronatus and Plectus spp., were very frequent, 7 species were determined as frequent, 14 species less frequent, and 47 species very less frequent.
Elevational distribution of nematodes
Altitudinal distribution of the nematode fauna. 1. Nematode abundance. Table 3 provides the nematode abundance in different altitudinal subranges of Mount Ararat. The number of nematodes did not differ statistically at level 1500-3000 m a.s.l. and the greatest nematode abundance was found at the highest sub-range (3500-4000 m a.s.l.). An increase in the nematode population density was generally caused by the increase in the numbers of species determined as very abundant (Tables 2 & 4). Distribution data have been statistically tested resulting in the existence of significant differences in the number of nematodes detected with increasing altitude (P = 0.003675). Remarkably, the nematode density at the highest altitudinal range was significantly greater than that at other ranges (Table 3). No nematodes were found in samples from over 4200 m a.s.l.
2. Species occurrence. The species found are ordered alphabetically and the abundance is provided as the number of specimens per soil sample (Table 4). Taking into consideration the presence/absence data, nematode species may be classified according to three basic distributional patterns.
(i) Widely distributed forms. Those species that were present in at least four altitudinal ranges:
Acrobeloides nanus, Aphelenchoides spp., Aphelenchus spp., Aporcelaimellus spp., Cervidellus vexilliger, Eucephalobus mucronatus, Eudorylaimus sabulophilis, Geocenamus koreanus, Malenchus sp.,
Panagrolaimus rigidus, Paratylenchus sp., Plectus spp., Tylencholaimellus montanus and Tylenchus sp.
(ii) Species showing a more restricted but recognisable pattern. Those forms occurred in two or three continuous ranges with a distinguishable tendency. In this case, it is possible to separate three (sub) patterns. Firstly, a group of species only dwelling in lower altitudes: Seleborca complexa, Chiloplacus bisexualis, Chronogaster sp, Coslenchus sp., Eudorylaimus subdigitalis, Monhystera sp., Nagelus hexagrammus and Stegelletina sp. Secondly, species restricted to median altitudes: Dorylaimellus sp., Heterodorus magnificus, Pratylenchus thornei, Tylencholaimus teres, Tylenchorhynchus maximus and Tylenchorhynchus mangiferae. Thirdly, species inhabiting the high altitudes: Acrobeles andalusicus, Geomonhystera sp., Mesodorylaimus sp., Plectus spp. and Rhabdolaimus sp.
Table 3. Altitudinal distribution of nematodes in Mount Ararat, Turkey.
Elevation (m a.s.l.) n1* Abundance2
1500-2000 4 75.75 ± 19.50 (a)
2000-2500 6 91.6 ± 19.65 (a)
2500-3000 6 74.1 ± 13.63 (a)
3000-3500 4 86.2 ± 9.10 (a)
3500-4000 5 192.8 ± 46.46 (b)
Total 25
'Number of soil samples collected from each altitudinal range.
*Four samples at the altitudinal range 4372-4957 m a.s.l. had a mean of zero nematodes so they were not included in the analysis.
2Number (mean ± s.d.) of specimens (200 cm-3 soil). Different letters indicate significant differences between means (P < 0.05, one-way ANOVA following post-hoc Tukey test).
(iii) Species with no recognisable pattern. Some taxa do not show a distinguishable distribution pattern as they are either rare or very rare or are present in several discontinuous ranges without a marked tendency.
3. Species richness. The distribution of nematode diversity, here focused on the number of species, is other interesting aspect of this study. Table 5 presents the results, which include the variation in the total number of species and the average of species per soil sample for each
Table 4. Altitudinal distribution (m a.s.l.) of species abundance (mean number of specimens per each soil sample).*
Taxon name 1500-2000 2000-2500 2500-3000 3000-3500 3500-4000
Achromadora sp. 0.0 0.0 0.0 0.0 0.2
Acrobeles andalusicus 0.0 0.0 7.0 12.3 1.4
Acrobeles ciliatus 0.0 7.6 0.0 0.0 0.0
Seleborca complexa 15.8 9.4 0.0 0.0 0.0
Acrobeloides nanus 0.0 0.4 2.2 4.5 20.0
Acrolobus longigubernaculum 0.0 0.0 0.0 0.0 2.6
Alaimus sp. 0.0 0.2 0.2 0.0 0.0
Anaplectus sp. 0.0 0.0 0.0 0.0 0.2
Aphelenchoides spp. 3.3 8.2 6.5 14.0 11.0
Aphelenchus spp. 4.3 5.8 9.0 2.8 0.4
Aporcelaimellus obtusicaudatus 0.0 3.2 0.0 0.3 0.0
Aporcelaimellus spp. 1.5 1.6 0.8 3.3 0.2
Cervidellus vexilliger 0.0 0.2 0.5 1.5 1.0
Chiloplacus trilineatus 0.0 0.0 1.3 0.5 0.8
Chiloplacus bisexualis 4.5 6.6 1.0 0.0 0.0
Chronogaster sp. 11.8 0.0 0.0 0.0 0.0
Coslenchus sp. 1.3 0.4 0.7 0.0 0.0
Crassolabium cylindricum 0.0 1.2 0.0 0.0 0.0
Criconema sp. 0.0 0.0 0.0 0.3 0.0
Discolaimium sp. 1.0 0.0 0.2 0.0 0.0
Ditylenchus sp. 0.0 0.2 0.0 0.3 0.0
Dorylaimellus sp. 0.0 0.0 0.2 0.3 0.0
Dorylaimus lineatus 0.0 0.0 0.0 0.0 2.2
Ecumenicus monohystera 0.0 0.4 0.0 4.3 0.0
Enchodelus lucinensis 0.0 2.4 0.0 3.0 0.8
Eucephalobus mucronatus 0.3 3.6 8.2 17.5 28.8
Eudorylaimus sabulophilis 0.0 0.6 0.7 0.5 1.4
Eudorylaimus subdigitalis 1.3 2.4 0.0 0.0 0.0
Funaria cf. obtusa 0.0 0.8 0.0 0.0 0.0
Geocenamus koreanus 0.5 5.0 2.5 3.3 4.8
Geomonhystera sp. 0.0 0.0 0.0 0.5 3.2
Helicotylenchus sp. 0.0 0.0 0.0 0.3 0.2
Heterodera trifolii 0.0 0.0 0.8 0.0 0.0
Heterodorus magnificus 0.0 4.0 3.0 0.8 0.0
Hoplolaimus sp. 0.3 0.0 0.2 0.0 0.0
Longidorella okhlaensis 0.0 1.2 0.0 0.0 0.0
Table 4 (continued). Altitudinal distribution (m a.s.l.) of species abundance (mean number of specimens per each soil sample).*
Taxon name 1500-2000 2000-2500 2500-3000 3000-3500 3500-4000
Malenchus sp. 1.0 3.6 1.3 4.3 2.4
Mesodorylaimus sp. 0.0 0.0 0.2 0.5 25.2
Mesorhabditis sp. 0.0 0.0 0.2 0.0 0.0
Microdorylaimus sp. 0.0 0.6 0.0 0.3 0.0
Monhystera sp. 5.8 0.0 0.0 0.0 0.0
Nagelus camelliae 0.0 0.0 0.0 0.0 5.4
Nagelus hexagrammus 0.3 1.0 0.0 0.0 0.0
Nothacrobeles sp. 0.0 0.2 0.0 0.0 0.0
Nygolaimus sp. 0.0 0.4 0.0 0.0 0.0
Panagrolaimus rigidus 1.5 0.8 4.7 4.8 29.0
Paracrobeles sp. 0.0 0.2 0.0 0.0 0.0
Paratylenchus sp. 0.5 7.8 0.3 1.0 0.0
Plectus spp. 0.0 0.8 3.2 0.8 38.4
Pratylenchus thornei 0.0 0.0 0.2 0.3 0.0
Pratylenchus neglectus 0.0 2.0 0.0 0.0 0.0
Propanagrolaimus hydrophilus 0.3 0.0 0.0 0.0 0.0
Pungentus sp. 0.3 0.6 0.2 0.0 0.2
Rhabdolaimus sp. 0.0 0.0 0.0 0.5 0.8
Rotylenchus sp. 0.3 0.8 1.0 0.0 30.2
Scutellonema sp. 0.0 0.0 0.2 0.0 0.0
Stegelletina sp. 0.5 0.2 0.0 0.0 0.0
Teratocephalus terrestris 0.0 0.0 0.7 0.0 1.6
Tobrilus sp. 0.8 0.0 0.0 0.0 0.0
Trichodorus sp. 0.0 0.0 0.0 0.0 0.2
Tylencholaimellus montanus 0.3 0.4 1.7 3.5 1.2
Tylencholaimus teres 0.0 1.0 0.3 1.8 0.0
Tylencholaimus proximus 0.0 0.0 0.8 0.0 0.0
Tylenchorhynchus maximus 0.0 0.0 0.5 0.5 0.2
Tylenchorhynchus mangiferae 1.0 0.0 1.5 1.0 0.0
Tylenchus sp. 0.0 0.2 1.0 4.0 1.4
Tylocephalus auriculatus 0.0 0.0 0.0 0.0 4.6
Xiphinema sp. 0.0 0.2 0.0 0.0 0.0
Zeldia sp. 0.0 0.0 0.2 0.0 0.2
*Each altitude range was consisted of five sub samples. Each soil sample was a volume of 200 cm 3.
Table 5. Distribution of nematode species richness at five altitudinal intervals in Mount Ararat, Turkey.
Interval (m a.s.l.) n1* S2 Ss3
15QQ-2QQQ 4 25 9.8 i 1.2 (a)
2QQQ-25QQ 6 39 18.Q i 2.1 (b)
25QQ-3QQQ 6 36 16.3 i 2.2 (b)
3QQQ-35QQ 4 32 16.Q i 1.3 (b)
35QQ-4QQQ 5 32 14.Q i 2.5 (b)
Total 25 70
'Number of soil samples collected from each altitudinal range.
*Four samples at the altitudinal range 4372-4957 m a.s.l. had a mean of zero nematodes so they were not included in the analysis.
2Total number of species collected from each altitudinal range. 3Number (mean ± s.d.) of species (200 cm-3 soil). Different letters indicate significant differences between means (P < 0.05, one-way ANOVA following post-hoc Tukey test).
altitudinal range. In both cases, it is possible to note that there is a maximum species richness at medium altitudes and the number of species decreases at both the lowest and the highest altitudes.
4. MDS comparison of altitudinal ranges. A non-metric Multi-Dimensional Scaling (MDS) analysis was performed on the distribution of nematode genera into five altitudinal ranges (Fig. 3)
relating to the presence of dissimilarities according to increasing altitude effects on the nematode composition. In relation to the similarity of nematode assemblages with altitudinal range, there were three main groups: (i) the lowest altitudinal range from 1500-2000 m a.s.l.; (ii) the mid-zone range from 2500-3500 m a.s.l.; and (iii) the highest altitudinal range between 3500-4000 m a.s.l.
Distribution of the nematode fauna according to habitat type. 1. Nematode abundance. The total number of collected nematodes in five habitats with different ecological characteristics showed high variability. The highest number of specimens per sample was found in the wildflower meadow habitat with 136.25 individuals. It was followed by mountain grassland (111.1 individuals per sample), chalk grassland (78 individuals per sample), riverbed (74 individuals per sample) and marshland (43 individuals per sample) (Table 6).
2. Species occurrence. Table 7 presents the distribution of species abundance at each habitat type with different ecological characteristics. The species are ordered alphabetically and the abundance is provided as the number of specimens per soil sample. Taking into consideration the presence/absence data, nematode species may be classified according to five basic distributional patterns for each ecological characteristic.
(i) Widely distributed forms. Those species that are present in all habitats. They are four in total: Aphelenchus spp., Chiloplacus bisexualis, Eucephalobus mucronatus andMalenchus sp.
Fig. 3. Distance between five different altitudinal ranges. Species distribution was analysed by MDS (nonmetric Multi-Dimensional Scaling).
Table 7. Species distribution in habitats with different ecological characteristics with corresponding abundance (mean number). *
Taxon name Wildflower meadow Mountain grassland Chalk grassland Riverbed Marshland
Achromadora sp. 0.0 0.1 0.0 0.0 0.0
Acrobeles andalusicus 1.4 10.3 1.0 0.0 0.0
Acrobeles ciliates 0.0 0.0 2.6 2.1 0.0
Seleborca complexa 7.6 5.9 0.0 0.0 0.3
Acrobeloides nanus 12.8 2.6 1.0 0.3 0.0
Acrolobus longigubernaculum 0.5 1.1 0.0 0.0 0.0
Alaimus sp. 0.0 0.3 0.0 0.0 0.0
Anaplectus sp. 0.1 0.0 0.0 0.0 0.0
Aphelenchoides spp. 13.9 9.5 1.1 1.0 0.0
Aphelenchus spp. 3.4 5.0 2.6 3.0 0.1
Aporcelaimellus obtusicaudatus 0.1 1.9 0.5 0.0 0.0
Aporcelaimellus spp. 1.9 1.9 0.5 0.4 0.0
Cervidellus vexilliger 0.9 1.0 0.0 0.0 0.0
Chiloplacus trilineatus 0.4 0.3 0.1 0.8 0.0
Chiloplacus bisexualis 2.1 3.3 1.1 0.5 0.1
Chronogaster sp. 0.0 0.0 0.0 0.0 5.9
Coslenchus sp. 0.1 0.6 0.0 0.1 0.5
Crassolabium cylindricum 0.0 0.5 0.0 0.3 0.0
Criconema sp. 0.0 0.1 0.0 0.0 0.0
Discolaimium sp. 0.5 0.0 0.1 0.0 0.0
Ditylenchus sp. 0.0 0.3 0.0 0.0 0.0
Dorylaimellus sp. 0.0 0.3 0.0 0.0 0.0
Dorylaimus lineatus 0.3 1.1 0.0 0.0 0.0
Ecumenicus monohystera 0.0 2.4 0.0 0.0 0.0
Enchodelus lucinensis 1.4 1.0 0.0 1.1 0.0
Eucephalobus mucronatus 13.5 19.1 3.6 1.9 0.1
Eudorylaimus sabulophilis 0.9 1.0 0.3 0.0 0.0
Eudorylaimus subdigitalis 0.1 1.5 0.0 0.0 0.0
Funaria cf. obtusa 0.5 0.0 0.0 0.0 0.0
Geocenamus koreanus 3.9 3.6 1.5 0.9 0.0
Geomonhystera sp. 0.6 1.6 0.0 0.0 0.0
Helicotylenchus sp. 0.0 0.3 0.0 0.0 0.0
Heterodera trifolii 0.0 0.0 0.0 0.6 0.0
Heterodorus magnificus 0.0 2.3 0.4 2.5 0.0
Hoplolaimus sp. 0.0 0.1 0.0 0.0 0.1
Kochinema sp. 0.1 0.0 0.0 0.0 0.0
Table 7 (continued). Species distribution in habitats with different ecological characteristics with corresponding
abundance (mean number).*
Taxon name Wildflower meadow Mountain grassland Chalk grassland Riverbed Marshland
Longidorella okhlaensis 0.0 0.8 0.0 0.0 0.0
Malenchus sp. 2.8 3.9 0.1 0.5 0.1
Mesodorylaimus sp. 12.6 3.5 0.0 0.0 0.0
Mesorhabditis sp. 0.0 0.0 0.0 0.1 0.0
Microdorylaimus sp. 0.1 0.4 0.0 0.0 0.0
Monhystera sp. 0.0 0.0 0.0 0.0 2.9
Nagelus camelliae 3.3 0.1 0.0 0.0 0.0
Nagelus hexagrammus 0.1 0.6 0.0 0.0 0.0
Nothacrobeles sp. 0.0 0.0 0.0 0.1 0.0
Nygolaimus sp. 0.0 0.3 0.0 0.0 0.0
Panagrolaimus rigidus 12.3 10.9 0.6 1.5 0.0
Paracrobeles sp. 0.1 0.0 0.0 0.0 0.0
Paratylenchus sp. 0.5 5.3 0.0 0.1 0.0
Plectus spp. 9.5 20.0 0.0 0.3 0.0
Pratylenchus thornei 0.0 1.0 0.1 0.1 0.0
Pratylenchus neglectus 0.1 0.0 0.1 0.1 0.0
Propanagrolaimus hydrophilus 0.0 0.0 0.0 0.0 0.1
Pungentus sp. 0.3 0.4 0.0 0.1 0.0
Rhabdolaimus sp. 0.8 0.0 0.0 0.0 0.0
Rotylenchus sp. 17.8 1.8 0.6 0.0 0.1
Scutellonema sp. 2.8 0.1 0.0 0.0 0.0
Stegelletina sp. 0.3 0.1 0.0 0.0 0.0
Teratocephalus terrestris 1.0 0.4 0.1 0.0 0.0
Tobrilus sp. 0.0 0.0 0.0 0.0 0.4
Trichodorus sp. 0.0 0.1 0.0 0.0 0.0
Tylencholaimellus montanus 0.5 3.4 0.3 0.0 0.0
Tylencholaimus teres 0.5 1.3 0.0 0.0 0.0
Tylencholaimus proximus 0.0 0.6 0.0 0.0 0.0
Tylenchorhynchus maximus 0.1 1.3 0.3 0.0 0.0
Tylenchorhynchus mangiferae 0.5 1.8 0.0 0.0 0.0
Tylenchus sp. 0.9 2.0 0.6 0.1 0.0
Tylocephalus auriculatus 2.8 0.1 0.0 0.0 0.0
Xiphinema sp. 0.0 0.1 0.0 0.0 0.0
Zeldia sp. 0.0 0.1 0.1 0.0 0.0
*A total number of 29 samples were analysed. Each soil sample was a volume of 200 cm-3. The number of samples varied between 2-10 samples per habitat.
Fig. 4. Distance between nematode communities from different habitats. Distribution of nematode genera was analysed by MDS (nonmetric Multi-Dimensional Scaling).
(ii) Species that were only collected from the wildflower meadow: Anaplectus sp., Funaria cf. obtusa, Kochinema sp., Paracrobeles sp., Rhabdolaimus sp.
(iii) Species that were only collected from mountain grassland: Achromadora sp., Alaimus sp., Criconema sp., Ditylenchus sp., Dorylaimellus sp., Ecumenicus monohystera, Helicotylenchus sp., Heterodera trifolii, Longidorella okhlaensis, Nygolaimus sp.
(iv) Species that were only collected from the riverbed: Mesorhabditis sp., Nothacrobeles sp.
(v) Species that were only collected from marshland: Chronogaster sp., Monhystera sp., Propanagrolaimus hydrophilus and Tobrilus sp.
3. MDS comparison of ecological characteristic types. A non-metric MultiDimensional Scaling (MDS) analysis was performed on the distribution of nematode genera resulting in five ecological characteristic types (Fig. 4). MDS ordination analysis showed that the nematode communities were grouped into two main groups according to their ecological characteristics. Remarkably, the nematode community from marshland was almost entirely different from
communities in mountain grassland, wildflower meadow, chalk grassland and riverbed.
Table 6. Nematode abundance in five ecological characteristics of Mount Ararat, Turkey.
Ecological characteristic n1* Abundance2
Wildflower meadow 9 136.2 ± 16.1 (a)
Mountain grassland 10 111.1 ± 15.3 (a)
Chalk grassland 2 78 ± 2.6 (ab)
Riverbed 2 74 ± 2.4 (ab)
Marshland 2 43 ± 3.1 (b)
Total 25
'Number of soil samples collected in each altitudinal range. *Four samples at the altitudinal range 4372-4957 m a.s.l. had a mean of zero nematodes so they were not included in the analysis.
2Number (mean ± s.d.) of specimens (200 cm-3 soil). Different letters in the column indicate significant differences between means (P < 0.05, one-way ANOVA following post-hoc Tukey test).
DISCUSSION
Species distribution. To understand the complete distributional patterns of nematode communities at Mount Ararat, we will discuss the matter of species distribution using three different approaches.
Firstly, species were examined according to their relative abundance and occurrence with an integrative and comparative approach. The results fit a very general pattern, as a few species (Eucephalobus mucronatus and Plectus spp. among others) are simultaneously very abundant or abundant and very frequent or frequent, whereas most species are rare or very rare and less frequent or very less frequent. For instance, Rotylenchus sp. is a very abundant but less frequent species since this taxon occurs in a few soil samples, but always with high density of specimens. This may be explained by the limitations of host plant availability for plant-parasitic nematodes.
Regarding the altitudinal distribution of nematode species, several patterns were distinguished, which should be tested and confirmed with further studies as there are no comparable studies in the specialised literature. Remarkably, several species were distributed only in the highest altitudes of habitable zone (3500-4000 m a.s.l.): Acrobeles andalusicus, Geomonhystera sp., Mesodorylaimus sp. and Rhabdolaimus sp. The presence of these nematodes in higher altitudes might be related to their general cold tolerance capabilities. Of special interest is the distribution of two cephalobid genera, which are represented by two or more species with a markedly different altitudinal distribution. Thus, together with two representatives of the genus Acrobeles and the only representative of the genus Seleborca, these can be spatially (altitudinally) ordered as Seleborca complexa, found only in the lowest range (15002000 m a.s.l.), A. ciliatus in the medium range (2000-2500 m a.s.l.) and A. andalusicus at higher altitudes (2500-4000 m a.s.l.) of the mountain. A similar distribution was observed in the two species belonging to the genus Chiloplacus, with C. bisexualis only occurring in the 1500-3000 m a.s.l. range, whereas C. trilineatus was found in the 2500-4000 m a.s.l. range. Acrobeles and Chiloplacus species are distributed world-wide. Acrobeles ciliatus and A. compexus have been reported from many different localities (e.g., Vinciguerra, 1972; Andrássy, 1953, 1958, 1962, 1978, 2002, 2009; Bostrom, 1992; Abolafia & Peña-Santiago, 2004). However, A. andalusicus was frequently found at high altitudes in the Iberian Peninsula (Abolafia & Peña-Santiago, 2005).
Species distribution was analysed on the basis of five different ecological characteristics, resulting in a marked difference between the community associated with marshland habitat and the remaining ones. Several species were found to be restricted to only one ecological characteristic, in particular a few rare species collected from wildflower meadow, for instance Anaplectus sp., Funaria cf obtusa and Kochinema sp. Generic composition of the nematofauna on meadow habitat is known to be the most stable community (Hanel, 1995). This can explain the tendency and presence of the rare taxa in wildflower meadow habitats of Mount Ararat. Moreover, species, which occurred only in marshland (Chronogaster sp., Monhystera sp. and Tobrilus sp.), were also those found to be tolerant of fluctuating oxygen conditions (Abebe et al., 2006). Since the marshland was in a wetland area, it may be expected to have fluctuations in oxygen level. Also, it has been mentioned by several authors that Chronogaster species have great abilities for physiological change (Heyns & Coomans, 1980; Poinar & Sarbu, 1994), whilst Tobrilus species are more known to have morphological plasticity in freshwater environments (Tsalolikhin, 2001).
Other interesting feature of the nematode community inhabiting Mount Ararat's soils is the presence of several genera that are considered to be commonly found in various extreme conditions (Abebe et al., 2006), namely Monhystera, Geomonhystera, Plectus, Mesodorylaimus and Eudorylaimus. All of them are ecologically generalists and, additionally, Monhystera and Plectus are bacteriovorous forms without specialised stoma structures. They are considered to have high plasticity to physiological changes. Also, the dorylaims are known to be highly omnivorous and very abundant in terrestrial habitats (Yeates et al., 1993). Some plant-parasitic nematodes are also well known and studied for their extreme survival strategies (Perry, 1999, 2002; Perry & Gaur, 1996), e.g., cyst nematodes exhibit diapause, a physiological state where hatching does not occur until specific requirements have been satisfied. The survival strategies of cyst nematodes, which enables Heterodera trifolii to overcome harsh winters, is a nice example of their ability to adapt extreme conditions at Mount Ararat.
Nematode abundance. The total nematode abundance was correlated with increasing altitude and it was significantly higher in the highest altitudinal range. Unfortunately, a very limited number of studies (Sohlenius & Bostrom, 1984; Popovici, 1984; Freckman et al., 1987; Hoschitz & Kaufmann, 2004) have been conducted to assess the
altitudinal gradient effects on nematode abundance. The results of these studies did not show any consistent pattern or correlation between abundance and altitude. In this context, our results, showing the highest abundance at the highest elevational range, should be regarded as a plausible hypothesis to test in the future. Actually, our survey was conducted during the summer season, a time in which environmental variables are optimal in high altitudes (Yeates & Bird, 1994; Stamou et al., 2005).
Species richness. General knowledge about species richness and diversity of organisms presumes that biodiversity has a decreasing trend with increasing latitude and altitude due to increasingly severe climatic conditions (Procter, 1984; Meyer & Thaler, 1995; Heal et al., 1998). Nevertheless, other patterns are known to occur (Rahbek, 1995) and several studies on nematode communities showed differing results (Boag & Yeates, 1998; Porazinska et al., 2012). Our data follow a common general pattern in which the highest value of species richness is found at intermediate altitudes (cf. Rahbek, op. cit.), with a total of 39 species (55% of the total) inhabiting the 2000-2500 m a.s.l. range in association with chalk grassland and riverbed habitats. Previous studies from high alpine areas (Hánél, 1998; Popovici & Ciobanu, 2000) also reported high species richness in more or less comparable habitats. Nevertheless, available literature does not provide totally comparable results.
The survey conducted on soils from Mount Ararat has revealed patterns of altitudinal distribution of nematode diversity (species richness) and nematode abundance. The number of species reaches a maximum at intermediate elevations, whereas the nematode abundance is significantly higher at the highest altitudes. Moreover, the nematode community associated with the marshland habitat becomes significantly different from those associated with the other four habitat types. These geographical and ecological trends, however, should be confirmed by future studies.
ACKNOWLEDGEMENTS
This study was supported by Ghent University, Scientific Research Unit, Nematology Department, Belgium, grant project European Master of Science in Nematology (2012-2014 EUMAINE Programme).
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Резюме. Исследованы биологическое разнообразие и распределение в местообитаниях с различными экологическими характеристками почвенных нематод на горе Арарат на высотах от 1523 до 5000 м над уровнем моря. Всего было определено 2561 экземпляров нематод, относящихся к 31 семейству, 62 родам и 70 видам. Разнообразие нематод (богатство видового состава) и численное обилие нематод показывают четкую приуроченность к высотам над уровнем моря. Было показано, что число видов достигает максимума на средних высотах, тогда как численное обилие нематод заметно увеличивалось с высотой. Сообщества нематод болотистых участков существенно отличались от сообществ нематод в других местообитаниях.
